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Extending the natural adaptive capacity of coral holobionts

Abstract

Anthropogenic climate change and environmental degradation destroy coral reefs, the ecosystem services they provide, and the livelihoods of close to a billion people who depend on these services. Restoration approaches to increase the resilience of corals are therefore necessary to counter environmental pressures relevant to climate change projections. In this Review, we examine the natural processes that can increase the adaptive capacity of coral holobionts, with the aim of preserving ecosystem functioning under future ocean conditions. Current approaches that centre around restoring reef cover can be integrated with emerging approaches to enhance coral stress resilience and, thereby, allow reefs to regrow under a new set of environmental conditions. Emerging approaches such as standardized acute thermal stress assays, selective sexual propagation, coral probiotics, and environmental hardening could be feasible and scalable in the real world. However, they must follow decision-making criteria that consider the different reef, environmental, and ecological conditions. The implementation of adaptive interventions tailored around nature-based solutions will require standardized frameworks, appropriate ecological risk–benefit assessments, and analytical routines for consistent and effective utilization and global coordination.

Key points

  • Coral reefs are degrading globally from anthropogenic climate change and local environmental impacts; deteriorated reefs are facing severe and widespread loss without active intervention.

  • Ongoing efforts aim to extend the natural adaptive capacity of reef-forming coral holobionts through incorporation of novel tools, methods, and environments to manipulate coral adaptive responses to survive under more extreme or variable conditions.

  • Emerging nature-based adaptive approaches spur novel intervention strategies that hold the promise to be feasible and scalable in the real world but must be tailored to address the diverse reef, environmental, and ecological conditions.

  • Implementing an adaptive intervention framework focused on naturally evolved solutions will require standardized methodology, appropriate ecological risk–benefit assessments, and analytical routines for consistent and effective utilization and global coordination.

Introduction

Tropical coral reefs cover only 0.1% of the seafloor yet provide habitat for >30% of all marine multicellular species1. Ecosystem services delivered through healthy tropical reefs are economically valued at around US $9,900,000 million per year2 and sustain almost a billion people3,4,5. Despite their importance, catastrophic global loss of coral reefs owing to anthropogenic activity is fast becoming a reality6. For example, the 2015–2018 global coral bleaching event affected 74% of reefs worldwide, with >30% of coral cover lost on the Great Barrier Reef alone7. Additionally, coral cover in the Florida Reef Tract has declined by upwards of 90% over the last 50 years8,9,10,11.

A global contributing factor to reef degradation is coral bleaching12,13. Without their microalgal symbionts (Fig. 1), corals lose their primary source of nutrition, leading to starvation, reduced fecundity, and reduced growth, often resulting in widespread coral mortality14,15. Trajectories for coral reefs under present CO2 emission scenarios are dire, with 60% of all remaining coral reefs critically threatened, and 98% exposed to environmental conditions above the current thresholds considered necessary to maintain ecosystem function as soon as 2030 (ref.16). The impact of ocean warming is exacerbated by the effects of ocean acidification17, deoxygenation18, and salinity changes19. Combined with local factors such as overfishing, coastal development, disturbance of the nutrient environment (water quality), and disease or predator outbreaks, the interrelated cumulative impacts all contribute to reduction in coral cover and declining reef ecosystem health20,21,22,23,24,25,26,27.

Fig. 1: The coral holobiont (metaorganism).
figure1

The holobiont is composed of the coral animal host, obligate intracellular algal symbionts (Symbiodiniaceae), and an assemblage of bacteria and viruses160, among many other organismal entities (such as fungi, endolithic algae, and archaea) that are less well understood functionally. Viruses putatively intersect all coral holobiont compartments, can transfer genetic material between holobiont member species, and contribute to the holobiont’s genetic diversity193,199. Known and inferred functional roles and relationships between holobiont member species as well as their contribution to metabolic cycling (carbon, nitrogen, phosphorus, sulfur) are depicted. Bold numbers indicate inferred functional roles. Coral holobionts constitute the foundation (meta)organisms of reef ecosystems, which explains their importance in efforts to devise strategies and interventions to save coral reefs.

Given the rate and extent at which climate change unfolds28, a widespread and shared concern is that the rate of environmental change could outpace the ability of coral holobionts to adapt to the changing environment29, concomitant with the increasing loss of coral reef cover30. Global mitigation of CO2 emissions is unquestionably needed to stem the rate of declining reef health30,31,32. However, biological, ecological and socio-economic adaptations are critical partners to preserve reefs and delay the loss of coral populations until carbon mitigation is effectively implemented30. Reef protection through Marine Protected Areas and management practices reduces how local stressors compound global climate change impacts27,31. Nevertheless, the current state of reefs and their predicted further decline have sparked initiatives to prioritize reefs or corals that are less vulnerable to climate change and best positioned for regenerating other degraded reefs in the future33,34,35.

An active area of investigation is the development of intervention management tools to maintain or even rebuild reefs, enhance recovery rates, and promote resistance to environmental pressures through ecological engineering, assisted evolution, and managed relocation36,37,38,39,40. Success of any of these initiatives requires detailed knowledge on the long-term survivability of reefs, which, in turn, relies on better understanding of the biotic and abiotic factors that underlie increased coral stress tolerance and the identification of colonies with such characteristics41,42,43,44. Projecting further, active manipulation of the natural adaptive capacity of coral holobionts might be needed to slow or reverse the trend of ongoing reef loss.

Understanding how corals function is fundamental to the success of any approach that exploits or manipulates their natural capacity to adapt45,46,47. Consequently, all of the entities that constitute the coral holobiont (Fig. 1) must be considered. Given the vastly different biologies of sessile coral animals, their eukaryotic Symbiodiniaceae microalgae, prokaryotes (bacteria and archaea), and viruses (amongst others), the adaptive responses operate on different timescales and are subject to unique evolutionary and ecological contexts of adaptation46,48. Knowledge about how coral holobionts respond or adapt to stressors provides the opportunity to modify these responses, employing or manipulating the same mechanisms that corals have naturally evolved to cope with and survive stress. Although detailed knowledge of how corals adapt to environmental stress is limited, emerging information on the biological entities that constitute the coral holobiont (and improved methods to manipulate them) provides opportunities to harness their individual and collective natural adaptive responses36,41,49,50,51,52,53,54,55,56.

In this Review, we describe an adaptive intervention framework aimed at harnessing the natural adaptive capacity of the coral holobiont. Expanding the adaptive capacity relies on operationalizing nascent methodological innovations at scale and is dependent on making them cost-effective, risk-reward favourable, and tailored to the challenges faced by the specific environmental conditions of different reefs. The adaptive strategies available to the different coral holobiont entities and how the underlying mechanisms might be employed or manipulated to increase stress resilience at large are summarized with a focus on thermal tolerance. Subsequently, a blueprint for coral survival guided by scientific insight utilizing emerging methods and technologies and how they can be implemented and scaled to real-world application is outlined, emphasizing that feasibility needs to be weighed against scalability, practicality, and regional setting to provide tailored and scaled solutions.

Adaptive strategies of coral hosts

Like all animals, corals respond to changes in their environment via acclimation and adaptation. In the contemporary literature, adaptation does not sensu stricto refer to evolutionary change through positive selection, but is more broadly used to denote adjusting to prevailing environmental conditions by various means46. Here, the term environmental adaptation is used in this broad sense, whereas evolutionary adaptation denotes the specific process of natural selection.

The extent to which corals can acclimate to alleviate environmental stress is currently unclear, although some corals do appear to demonstrate a large capacity for acclimation. For example, colonies (genotypes) of some species can survive for hundreds, if not thousands, of years and experience dramatic environmental changes during their lifetime57,58. In American Samoa, Acropora hyacinthus coral fragments that were transplanted between adjacent pools with different thermal environments demonstrated acquisition of heat tolerance levels by means of acclimation that would be expected from adaptation through natural selection over multiple generations59. In Hawaii, naturally heat-resistant coral transplants acclimated to new environmental regimes on the scale of months, maintaining their thermal tolerance60.

Notably, acclimation capacity differs amongst coral species and appears inherently linked to the ability to mount rapid and lasting widespread transcriptomic changes61,62,63,64 or reprogramming epigenetic marks65,66,67. In addition to acclimation within the lifetime of an animal, transgenerational plasticity might enable corals to acclimate to prevailing environmental conditions48. Such acclimation has been observed in experiments comparing the performance of offspring from parents raised in different environments where acquired tolerances are passed on to the next generation68,69,70, potentially linking transgenerational acclimation to DNA methylation51.

Evolutionary adaptation through natural selection usually requires multiple generations, as the prevalence of selected alleles underlying the beneficial trait needs to increase and become a common trait of the population or species. Therefore, this process depends on several variables, such as the amount of genetic variation present in the population, the population size, the generation time, and the strength of selection. The standing genetic diversity of corals is presumably large71,72,73,74, suggesting a capacity to recover from reductions in population size under suitable conditions, at least for some species73. Corals could also have the capacity to adapt via heritable somatic mutations75,76. The ability to rapidly adapt (years to decades) to changing environments is further supported by the presence and frequency of thermotolerance alleles and the modeling of population trajectories under different climate change scenarios72,77. Indeed, natural populations might already be adapting to increasing sea surface temperatures78,79,80 or have previously adapted to extreme environmental conditions81,82,83.

The ability of at least some coral species to exhibit substantial acclimation capacity presents the possibility to harness this capacity for reef restoration through a process termed environmental hardening (Table 1). For example, preconditioned coral fragments show increased resilience compared with naive coral fragments in some species62,84. These effects might even be passed on to the next generation68,69,70,85. Although the molecular mechanisms underlying these effects are not yet fully understood, epigenetic modifications such as DNA methylation and histone modification, amongst others, might be involved48. DNA methylation changes have been found in response to stress treatments65 or transplantation86 and were not only predictive of phenotypic responses, but also showed higher correlation than changes in gene expression. More importantly, corals (in contrast to other metazoans) appear to biparentally pass on their DNA methylation patterns to their offspring, thereby providing a molecular mechanism for transgenerational inheritance of acclimation responses51. If such mechanisms indeed exist, they could be exploited by growing corals in land-based nurseries that allow controlled exposure to increased temperature or other stressors to induce favourable acclimation responses87.

Table 1 Approaches to manipulate and harvest the adaptive response of the coral holobiont

The extent to which resilience can be improved through environmental hardening and transgenerational acclimation is unclear. For example, there is still little understanding of which mechanisms promote this effect, the extent to which resilience can be increased, or how long the preconditioning effects are maintained. By comparison, assessments on the potential of selective breeding as a means to achieve coral adaptation have provided promising insights to improve restoration approaches through human intervention56. Similarly, breeding experiments reveal that genetic adaptations to higher temperatures can be passed on within a single generation, with coral larvae from parents of warmer regions producing offspring with up to ten times higher chances of survival under heat stress88. Importantly, the survival odds still increased by up to fivefold if only one of the parents came from a warmer region, providing evidence for the increasing thermotolerance of corals via assisted evolution36.

Assisted evolution interventions follow the premise that ‘nature does it best’. Such approaches are generally less extreme than targeted genetic modification approaches; they rely on naturally occurring genotypes and natural selection to counter any drastic genetic alterations that would affect the remainder of the coral holobiont and its genetic constituents. Several interventions are proposed, such as the relocation of thermotolerant colonies (genotypes) to cooler regions to introduce adaptive genetic variants into these populations or selective breeding using thermotolerant colonies36,39,89. Both methods attempt to mimic natural processes by increasing the frequency of beneficial alleles in the local population, providing a foundation for selection, while retaining both genetic diversity and the local genetic adaptations required for the success of corals at the specific location. Importantly, both methods rely on the identification and selection of thermotolerant genotypes (such as those from particularly warmer environments, for example, lagoonal pools). This identification requires the development of large-scale phenotyping platforms and knowledge of the natural distribution range of coral species under study. Selecting more stress-tolerant and resilient genotypes of the same species across locations is a non-trivial task given the challenges associated with coral taxonomy90,91.

Platforms for screening large numbers of individuals for increased thermotolerance have been developed in the form of standardized, mobile, and inexpensive acute heat stress assays, such as the Coral Bleaching Automated Stress System (CBASS)41,44,49,92,93. The underlying premise is that corals that exhibit increased thermal tolerance in acute assays are also more resistant and/or resilient during natural heat stress events41,44. Indeed, considerable variation in thermotolerance can be found and resolved among coral colonies from the same and disparate sites using such short-term heat stress assays41,43,64. The genetic factors underlying such differences in stress tolerance are, however, not fully understood or identified43. Newly available CRISPR technology has been shown to work in corals and could be used to help understand the genetic basis of thermotolerance differences, in addition to offering the potential for engineering tolerant corals in the future, provided all safety requirements are satisfied94,95. Nevertheless, genetic alteration of single coral genotypes and their subsequent outplanting would rely on successful sexual reproduction with conspecifics and positive selection for the beneficial allele(s) to spread. Further, the genetic factors underpinning stress tolerance in corals are complex: it is a polygenic trait with potentially hundreds of genes involved, making genetic engineering challenging, although a subset of conserved genes exist that could form suitable targets for exploration and/or manipulation43,63,96,97.

Colonies from warmer and often geographically distinct regions could provide higher gains in thermotolerance when considered for relocation or selective breeding, but there are associated risks, including potential dilution of local gene pools. Local environments exert selection pressures across a multitude of environmental parameters (so-called environmental mosaics), of which temperature is only one. The translocation of colonies across large geographic distances is therefore problematic as transplanted corals might face a foreign environment, potentially resulting in reduced fitness, reduced competitiveness and, ultimately, reduced survival98,99. In addition, the lack of clarity around coral taxonomy and the inherent plastic morphology raises concerns regarding crosses of colonies assigned to the same species from disparate locations.

Substantial differences in thermal tolerance can already be found at smaller geographic scales (for example at the reef scale), as coral reefs provide many microhabitats that select for more thermotolerant genotypes, resulting in large phenotypic variation within local populations available for exploitation41,81,100. Although this variation might not extend to the greatest extremes of tolerance possible for a given species, it avoids the risks associated with the introduction of foreign genotypes into local populations. Consequently, the identification of locally adapted colonies with high thermotolerance for selective breeding approaches could be the most prudent approach to follow, at least in the case of broadcast spawning corals101. Selected colonies from different microenvironments could be maintained in local land-based nurseries, allowing for controlled conditions and crosses, as well as the rearing of larvae to the pre-settlement stage to increase survivorship102. Unwanted domestication effects such as a growth advantage for corals that do better under aquaria conditions, however, could make it challenging to maintain coral genotypes that ‘thrive’ under environmental extremes in the wild34. Thus, the use of pre-settlement larvae screened for increased thermotolerance for deployment in local reefs and subsequent environmental selection of suitable genotypes might be the most promising approach103.

Adaptive strategies of Symbiodiniaceae

Symbiodiniaceae are the primary photosymbionts of shallow-water tropical coral species104. These microalgae reside within the cells of their coral host and provide photosynthates that broadly cover the energy needs of the coral in return for a light-rich, sheltered environment, and the provisioning of CO2 and other micronutrients105,106,107. Modern corals and Symbiodiniaceae co-diversified in the Jurassic Period (about 160 million years ago), linking the success of reef ecosystems to this symbiosis104. The Symbiodiniaceae family likely comprises hundreds of species104,108,109, with comparative genomic data revealing extensive divergence among and within genera104,110,111. The substantial diversification of the family is explained by the high level of host specialization and fidelity, even under environmental extremes112,113,114.

The coral–Symbiodiniaceae endosymbiosis is particularly sensitive to heat and light stress, which together can cause coral bleaching and subsequent mortality12,15. Although shifts in the dominant Symbiodiniaceae towards more thermotolerant species are observed115, most novel associations do not persist112,116. Thus, considerable effort has been placed on understanding stress tolerance limits among Symbiodiniaceae and how these factors influence coral holobiont performance117,118,119. As a result, there is a growing appreciation for the diverse mechanisms that Symbiodiniaceae use to acclimate and adapt to changing environments on their own as well as in concert with their hosts109,118,120,121. For example, cultured Symbiodiniaceae cells are highly plastic with short-term acclimatory responses in growth, motility, gene expression, and photochemistry observed in response to changes in temperature, light, pH, salinity, and nutrient content122,123,124,125. Similar responses have been recorded in algal communities on coral reefs43,126.

Symbiodiniaceae also possess many traits that favour rapid evolutionary adaptation, including short generation times, both sexual and asexual reproductive modes, and genomic adaptive precursors, such as extensive functional enrichments, mobile elements, and RNA editing110,125,127,128. Interactions with corals and the loss or gain of a symbiotic lifestyle are also predicted to drive evolutionary change111. Even in the absence of their coral hosts, experimental evolution protocols over several years have induced major genetic and phenotypic changes in cultured Symbiodiniaceae129. In nature, Symbiodiniaceae typically exhibit a more pronounced population structure than corals130, signifying geographic isolation, local selection, and opportunities for local adaptation41,43,113,114,130,131,132.

Variation in the extent of symbiont specificity among coral life stages is important for predicting the potential for different coral species to change their symbiont communities through acclimatory processes such as switching or shuffling, which involve reorganizing the symbiont community to favour dominance of heat-tolerant taxa133,134,135. Coral larvae and juveniles are more plastic in their association with different Symbiodiniaceae compared with adult colonies136,137,138 and these could be the critical life stages for focused manipulative experiments (Fig. 2; Table 1). Indeed, manipulation of host–symbiont pairings might be a critical component of both natural and artificial adaptive strategies. However, there is limited evidence for successful long-term manipulation50,139. Short-term manipulation of the coral–algal symbiosis can be experimentally achieved at early life stages via symbiont seeding from the environmental pool or by providing new symbiosis opportunities (for example, by sourcing conspecific symbionts from geographically distant environments, or novel symbionts from distinct host species)140,141,142,143,144. Further approaches include the stress-hardening of adult corals with more invasive methods, including implanting cores of coral tissue containing heat-tolerant symbionts139 or via direct genetic engineering of the symbionts themselves145. However, Symbiodiniaceae seem intractable to such manipulation at present146.

Fig. 2: Adaptive processes in the coral holobiont and their utilization in adaptive interventions.
figure2

Interventions are meant to harness or extend the adaptive capacity of coral holobionts to increase their resilience. Note that all adaptive processes, except for evolutionary adaptation, can happen within the lifetime of the coral holobiont. In the readiness category, the flask represents successful implementation in laboratory trials and the coral represents successful implementation in field trials, with brackets denoting approaches that work in principle but for which either standardized or upscaling protocols are needed.

Ultimately, the utility of symbiont community manipulations is dependent on whether such alterations are heritable147,148. If induced changes do not persist across coral generations, they will only function as temporary stopgaps. Although there is evidence to suggest that a component of altered Symbiodiniaceae community composition is heritable148, in the vast majority of cases examined, associations appear to be highly specific104,112,113,114. Thus, any symbiont shuffling that takes place naturally or artificially after thermal bleaching or exposure during larval or juvenile stages does not persist across generations. Instead, the original symbiont composition is restored when environmental conditions return to normal, or after juveniles develop mature immune systems149,150,151,152.

The exception to the rule of reversion to the original community is evident when stressful conditions persist for extended periods or recur with high frequency115. In such cases, the balance shifts such that stress-tolerant Symbiodiniaceae are favoured over metabolically optimized symbionts, and novel species can remain as the numerically dominant partner. With the frequency and intensity of bleaching events increasing, it has been argued that environmental conditions on reefs could soon favour thermally tolerant, novel symbionts139. Such replacement seems to be underway in the Caribbean, with the spread of the heat-tolerant, potentially invasive Durusdinium trenchii115,153. Among Pacific reefs with biannual or annual repeat bleaching, symbiont communities have also already been observed to shift towards dominance of heat-tolerant Symbiodiniaceae154,155, although it is unknown whether such shifts persist across generations. However, even the most resilient symbionts are expected to provide no more than 2 °C of additional thermal tolerance to the coral holobiont, a threshold that will likely be exceeded in the tropics within the next 100 years156. The benefit might increase if coral holobionts evolve to reach greater optima in this period80, although the pace of such evolutionary processes under these conditions is unknown.

Even if altered symbiont communities could persist across generations, there are practical limits to artificially manipulating associations on a large scale. The inoculation and/or manipulation of individual coral adults might only provide single-colony scale resolution due to labour-intensive methods (Table 1). The most promising, scalable approach is to introduce coral larvae or juveniles to alternative algal symbionts while rearing large batches as part of ongoing restoration projects. However, mortality at these early life stages is high (up to >99% for larvae), although the numbers are improving with technological advances102,157. Such efforts might be able to seed struggling reefs with thermally tolerant coral individuals in the future. Currently, the most efficient means of manipulating symbiont communities at scale remains — ironically — anthropogenic climate change.

Adaptive strategies of prokaryotes

Prokaryotes (bacteria and archaea) have a crucial role in the health, fitness, and environmental adaptation of metaorganisms46,158,159,160,161. The coral microbiome (the community of bacteria and archaea) is influenced by the surrounding environmental conditions, host species, age, and size of colonies162,163,164,165. These community diversity patterns reflect the dynamic relationship between prokaryotes and environmental conditions, which are hypothesized to select for the most advantageous coral holobiont composition under a given setting, termed the coral probiotic hypothesis166. The concept of microbiome flexibility46 extends the coral probiotic hypothesis and acknowledges that the capacity for microbial change differs among coral species, with some coral species showing large microbiome changes across adverse environmental regimes, whereas others exhibit highly conserved bacterial assemblages49,165,167. Despite such flexibility, numerous taxonomic groups are found consistently associated with corals, such as Endozoicomonas168,169. Some of these taxa correlate with health, such as Roseobacter spp.170,171 or Pseudoalteromonas spp.170,172, and others with disease, such as Vibrio spp.173,174 or Rhodobacter spp.175, although the role or function for the majority of prokaryotes is unknown.

Manipulative studies employing reciprocal coral transplants or microbial manipulations that correlate changes with increased coral stress tolerance49,55,165,172,176 highlight that microbiome alteration could provide an alternate route to environmental adaptation, facilitating rapid responses of corals to changing environments46,49,55. Microbiome flexibility to adapt to adverse environmental conditions underlies the concept of Beneficial Microorganisms for Corals (BMCs) that centres around the identification of microbes that promote coral health and their subsequent utilization as coral probiotics38,177. Manipulating the coral microbiome is less about the mitigation of a specific impact, but focuses on increasing overall health, based on the premise that a healthier organism is more resilient when subjected to stress54,178. Such health improvements could mitigate an array of impacts that include thermal stress, pathogen challenge, and poor water quality54. Accordingly, BMCs help to reboot an altered and dysbiotic microbiome caused by environmental stress165,179, with the intention to outcompete opportunistic and detrimental microbes to restore or rehabilitate the altered microbiome and its microbial-mediated functions to the coral holobiont38,165 (Fig. 2; Table 1).

Several proof-of-concept studies now demonstrate that exposure of corals to BMCs can improve coral health through potentially mitigating stress and toxic compounds or controlling pathogens, although the underlying molecular mechanisms remain to be determined54,180,181. For instance, BMCs were successfully applied to ameliorate impacts caused by pathogens182 or toxic compounds180,181. Bacterial BMCs to mitigate coral thermal stress have been genomically and biochemically screened for beneficial functions including pathogen-targeted antimicrobial activity, reactive oxygen species (ROS) mitigation, dimethylsulfoniopropionate (DMSP) breakdown, and nitrogen cycling172,183. BMCs can even promote coral bleaching recovery and prevent coral mortality through mitigating post-heat stress disorder (PHSD) syndrome, possibly through bacterial ROS scavenging, coral host transcriptional reprogramming, and provision of alternate nutrition sources to boost coral energetics183.

BMC treatments appear to be most successful when applied during the stress exposure. However, BMCs are not retained for long periods of time, therefore likely requiring to be readministered at times of stress54,183, although retention might differ by life stage162. The application of coral prebiotics could also assist corals in the selection and retention of BMCs. Prebiotic application with or without administered BMCs during bleaching events could promote active enrichment of the coral microbiome as well as facilitate association with beneficial microbes (Fig. 2; Table 1). In addition, the development of strategies to scale up BMC delivery is required. Such upscaling might be achieved through immobilization of microbial cells and/or slowing their temporal release through attachment to biocompatible carriers, as well as bioencapsulation in prey or uptake through heterotrophic feeding54,184. Although existing genetic engineering techniques are easily applied to bacterial isolates derived from corals, they should be restricted to a laboratory context, as the effects that such altered genetic variants could exhibit in the highly complex and diverse coral reef environment (for example, interaction with pathogens) are unknown185,186,187. Accordingly, coral microbiome manipulative approaches at reef sites should focus on utilization of microbes (bacteria) from the native environment.

Adaptive strategies of viruses

Viruses can contribute to the evolution of their hosts and are critically important for the functioning of marine ecosystems188. A mechanistic understanding of the direct role of viruses in holobiont acclimation or adaptation is lacking, but there is evidence that viruses have a role in coral health, disease, or stress (thermal) tolerance189,190,191,192. One explanation could lie in bacteriophages — the most abundant members of the coral metaorganism — controlling the abundance of specific bacterial strains through lysis, thereby shaping the structure of the microbiome and its functional landscape186,193.

In humans and mice, viral predation of bacteria selects the bacterial strains that are able to colonize an animal host upon invasion194,195. When the lytic removal of bacterial strains is selective against pathogens, the viral predation effectively creates a form of immunity that is extremely plastic196,197. Evidence suggests that in a similar way, coral-associated viruses prey on detrimental bacteria that grow when stimulated by competitor turf algae198. Selective viral predation of bacterial strains causes viral–host co-evolution that could be a strong force shaping the coral microbiome, thereby affecting coral holobiont adaptability46. Yet the specific mechanisms underpinning these interactions are unknown, as well as how common such patterns are.

Another way in which bacterial viruses can shape the microbiome, and by extension the genetic and genomic make-up of the coral holobiont, is through lateral gene transfer199. Two main modes of viral-based genetic transfer occur, one when random fragments of bacterial DNA are packed into viral particles and the other when specific regions of bacterial chromosomes that flank integrated phage sequences are transferred. In both cases, lateral gene transfer can bring benefits analogous to sexual reproduction, such as increasing fitness and compensating for detrimental mutations in populations that replicate exclusively clonally200. Therefore, a viral-mediated increase in genetic exchange is expected to facilitate bacterial, and by extension microbiome, adaptation to changing conditions. However, coral reef phages could also transfer bacterial virulence genes that enable pathogen invasion of coral tissues and cause disease201,202. Indeed, transitions in viral community composition have been associated with numerous coral diseases192,203. However, little is known about the factors that determine how frequently coral-associated viruses transfer genes with beneficial or pathogenic effects to the coral host. The coral virome also contains abundant and diverse eukaryotic viruses199, which become more abundant during bleaching190, although cause versus consequence is unknown. Specifically, viruses infecting Symbiodiniaceae could have a direct effect on coral thermal sensitivity, potentially by increasing rates of predation at high temperatures189,204,205.

The application of viruses for coral acclimation and adaptation could take two main (but not exclusive) routes (Fig. 2; Table 1). First, viral therapy could help boost stress tolerance189, pending the successful isolation and culturing of such viral associates. Similarly, phage therapy could be used to control coral diseases when a bacterial pathogen can be identified. Second, phages could be employed to improve the efficacy of BMCs across a suite of applications (for example, to mitigate thermal stress, disease, or oil spill impacts). The application of viruses with BMCs in a ‘dual benefit approach’ to target specific pathogens and improve coral holobiont health is probably the most realistic near-future application. In principle, phages could be used as a tool to transfer desirable genes to members of the BMC consortia (or other entities of the coral holobiont), making them more efficient in colonizing the coral holobiont or stabilizing associations. However, this method would involve adding genetically modified organisms (GMOs) to natural ecosystems, an approach less likely to gain support. Alternatively, native coral-associated viruses could have their abundances manipulated, increasing their natural rates of predation or gene transfer, depending on the desired effect on the bacterial community. This approach relies on a better understanding of the functions of each microbiome and virome member193.

Phage therapy, in particular, is a promising tool for restoration or rehabilitation processes because it addresses the problem of scaling — through their high replication rates and population expansion, phages presumably would distribute even at the reef scale206,207. For example, phage therapy has successfully prevented bacterial-induced photosystem inhibition in Symbiodiniaceae208 and inhibited white plague disease progression in Favia favus in aquaria and in the field209,210. However, the possibilities for applying phage therapy on corals in the wild are very limited because of unanticipated off-target effects and the potential of uncontrolled expansion. The application of phage therapy to treat coral diseases is also constrained because, for most coral diseases, the causative pathogens have not been identified and many diseases might not be caused by a single distinct pathogen211,212,213,214.

There are several essential questions that need to be answered if viruses are to be applied in coral restoration efforts. Perhaps the most pressing need is the reconstruction of virus–host infection networks of coral species targeted for manipulation215. Most of the viruses identified in coral microbiomes have not been matched with a host, prokaryotic or eukaryotic, although available data suggest that many perceived viral–host associations need to be re-evaluated190,199,203. For instance, Hepadnaviridae are typically ascribed to be vertebrate-specific but have been found associated with coral genera199. This lack of knowledge about virus–host relationships prevents the identification of viruses that are potentially beneficial for coral, either through modulating the associated microbiome and its genetic pathways, affecting the response to stress (including Symbiodiniaceae), or encoding genes that improve microbiome function. The reconstruction of phage–bacteria infection networks will also contribute to constraining the possibility of off-target infections and recombination in phage therapy. By knowing how similar an introduced phage is to the resident phages, the risk of moving unwanted genetic material through lateral gene transfer can be reduced216. Such risk reduction is especially important because many resident phages encode bacterial virulence genes, which must not be accessible to bacteria that are strong colonizers of coral mucus and tissues199,202,217. Applying native phages that originate from the same or similar coral reef and coral holobiont that will be treated reduces the risk of off-target effects.

An adaptive intervention framework

Societal need to retain healthy coral reefs under climate change is driving a new era of innovation in reef science, evidenced by global multidisciplinary exploration of approaches to enhance coral resilience30,89,218. From a pragmatic point of view, restoration — trying to recreate reefs as they once were — is largely unachievable, but also would likely not provide future resilience as climate stressors persist and intensify219. Rather, enhancing current functional and/or genetic diversity through environmental rehabilitation to allow reefs to thrive under the new set of conditions should be aimed for. Embedding this central philosophy is critical as reef conditions are likely to worsen before they improve, even if the Paris Agreement goals are achieved30,32,220. Intervention measures aimed at increasing coral resilience will hopefully retain enough functional coral reefs to assist in long-term recovery. The following sections outline how such intervention measures could look, how they complement and can be integrated with existing practices, and how their efficacy can be monitored in the wild.

Extending the coral holobiont natural adaptive capacity

Intervention approaches have the greatest potential, feasibility, and readiness if harnessing the natural adaptive capacity of corals, thereby employing naturally evolved solutions that are tried and tested in reef ecosystems. They also avoid many of the concerns associated with genetic and/or technological engineering, and therefore governance and social licence. Risks will vary depending on the intervention approach, with, for example, environmental hardening possessing less risk although with limited longer-term resilience gains than selective breeding approaches, which directly interfere with coral population structures. Risks associated with the use of probiotics or other means of microbiome manipulation can be reduced if native microbiome partners are used, although how long these treatments persist or whether these approaches need repeated application requires investigation. It is essential to assess their longer-term benefits to determine their efficacy, applicability, and the best way to combine or integrate them with other techniques (Fig. 2; Table 1). Nature-based solutions still entail manipulation of biological interactions amongst holobiont partners, albeit avoiding any use of GMOs. Gaining a better understanding of the interactions between holobiont member species is necessary to identify and maximize synergistic effects through targeted combinations of different intervention methods, whereby all combinations are theoretically possible (Fig. 3). Selective breeding, for instance, can provide substantial increases in temperature resilience and could be further boosted through environmental hardening and/or the provisioning of probiotics and alternative algal symbiont strains.

Fig. 3: A scaled adaptive intervention framework.
figure3

Development and implementation of systematic health state surveys can provide a decision framework with standardized diagnostics, and, in turn, a suite of indicated intervention measures under consideration of the diverse reef, environmental, and ecological conditions. Diagnosis of endangered reefs, for instance, could detail several levels of degradation, where ecological traits such as coral cover, reproductive potential, and thermal tolerance are differentially affected. Accordingly, degraded reefs could be defined by predominant presence of bleached and/or diseased colonies that outnumber the prevalence of healthy colonies. In the scaled adaptive intervention framework, healthy reefs can help elucidate the role of coral holobiont entities as targets for adaptive intervention, whereas endangered and degraded reefs can be targets for a range of manipulative techniques pending the level of threat and traits to be restored.

The combination of different approaches does not rely on additional infrastructure beyond what is required for their independent implementation. Given the differences in practicality, scalability, and the time required for the interventions to take effect, it might be most efficient to combine technologies at different levels. Although selectively bred corals likely have the highest potential for resilience gains and scalability in the long run, their production is costly and scaling up is mostly achieved through propagation in the wild139,221,222. Implementation will therefore require natural populations to persist to provide enough coral cover for efficient natural reproduction and the preservation of ecosystem services. Initially, more scalable methods such as probiotics and Symbiodiniaceae manipulations could be used to increase resilience of the natural populations, ensuring sufficient coral cover to maintain coral reef function and providing enough colonies for efficient sexual reproduction and sufficient genetic diversity until beneficial alleles reach critical densities in the populations (Figs 3 and 4). Currently, however, it is unknown to what degree interventions centred around the coral holobiont translate into observable reef-level effects or the time that is required for holobiont-targeted interventions to manifest at the reef level. Addressing this gap in knowledge between holobiont-centred interventions to meet reef ecological scale goals is a key priority for global restoration efforts.

Fig. 4: Research road map for extending the adaptive capacity of the coral holobiont.
figure4

Emerging approaches (upper half) can inform and integrate with coral restoration measures (blue arrows). For instance, the thermal stress response of many colonies can be assessed using a standardized approach (such as the Coral Bleaching Automated Stress System (CBASS)) to identify coral colonies for selective breeding or environmental hardening. In addition, the success of restoration and/or rehabilitation and probiotic approaches can be monitored with this system. Likewise, information on genetic diversity can be incorporated into propagation approaches to enhance thermal resilience and maintain genetic diversity, and ex situ spawning can increase the input of larval supply for coral restoration through propagation. Alongside the characterization of further holobiont member species with beneficial effects, the study of corals from extreme environments can inform on and provide a source of adaptive alleles, adaptive mechanisms, and powerful probiotics underlying coral resilience (lower half). To improve success and inform adaptive intervention decision frameworks, it is essential to expand and integrate knowledge from real-world case studies. Increasing standardization and coordination of efforts can be leveraged through construction of a global database to provide a long-term defined and coordinated strategy, enable comparative (meta-)analyses and track success to catalyse and hasten effective coral reef conservation. Standardized, coordinated data recording can serve as a foundation for building predictive models and analytical frameworks that incorporate ecological, physiological, and molecular dimensions. Images courtesy of A. Roik and J. Craggs.

A scaled adaptive intervention framework

Coral propagation provides the fundamental practical framework needed to accelerate reef restoration, where the goal is to deliver coral functional diversity (in the form of taxonomic diversity that covers the different functions provided by reef-building corals) at a scale that exceeds natural recovery (as well as mortality) rates. Most coral restoration practices worldwide, however, still rely on asexual fragmentation-based propagation of individual genetic (or phenotypic) lines, and therefore, do not address restoration of functional genetic diversity40. Asexual fragmentation is a method utilized to boost living coral tissue within degraded reef areas quickly. It can also be implemented in situ by non-specialist groups, in particular through innovations enabling scalability of nursery-based propagation and outplanting rates223,224,225. Propagation and outplanting success is generally high (>75–90%)40,225,226, but survivorship can decline precipitously over time226,227, especially where other factors — such as disproportionately high corallivore rates — are not simultaneously mitigated. Success is further confounded where practices often operate without knowledge of the inherent genetic and functional diversity, and hence, do not increase the resilience of corals produced and even run the risk of adaptive bottlenecking in the long term42,221. Consequently, effective repopulation rests on capturing sufficient genetic and functional diversity to resist stochastic environmental change224,228,229. As such, sexual propagation techniques to maximize genetic recombination of parents — and hence adaptive potential — through either controlled (such as selective breeding amongst genotypes) or uncontrolled (such as mass larval-based seeding of outplant structures) approaches88,140,221,230 represent an essential and necessary pipeline, not only for coral reef restoration, but for rehabilitation.

Coral propagation approaches are now becoming tuned towards adaptive capacity. New diagnostic tools can be deployed to identify within-species diversity for more informed propagation decision-making41,42, and ex situ spawning aquarium systems can be employed to overcome limited larval supply imposed by annual coral spawning events231 (Fig. 4). Efforts in the Indo-Pacific have demonstrated how propagating within-species genetic diversity is important to ensuring efforts against transient heat waves44. This work suggests that new tools capable of high-throughput diagnostics of tolerance to different stressors, such as CBASS assays41, could become critical components in scaling coral restoration effectiveness and informing targeted breeding approaches (Fig. 4). Resolving the extent of local coral holobiont diversity — and how it is interdispersed amongst sites via connectivity and reproduction patterns232,233 — provides a logical basis for ensuring that active propagation efforts exploit the maximum available range of genetic diversity and coral functional performance (Fig. 4). Efforts are rapidly gearing towards overcoming technical and methodological constraints for selective breeding approaches based on large-scale sexual propagation221.

Alongside these efforts to enhance coral resilience, it is still important to mitigate the impact of environmental parameters, such as water quality, that are broadly linked to reef resilience and directly implicated in coral bleaching and disease susceptibility24,25,26,165. Interventions to enhance the stress tolerance of corals are unlikely to succeed without addressing local environmental conditions. Moreover, the technology to grow more resilient coral colonies is available (Fig. 2), but colony and reef growth will not naturally speed up. Better integration of current reef management practices and scaled adaptive approaches are required (Fig. 3). Local stressors, such as water quality and overfishing, act synergistically with climate change and represent important targets for intervention measures to counter some of the effects of global climate change24,25,27. Measures to improve water quality or reduce overfishing, alongside the management of other environmental drivers of reef decline, should be prioritized alongside the more manipulative coral holobiont-centric intervention measures presented here.

Standardization and monitoring success

Despite the prospect of combining emergent technologies with tried and tested approaches, standardized protocols must be developed and made available for broad application, which should become more available in the coming years, or are already in place221 (Figs 2 and 4). Restoration and/or rehabilitation will likely benefit from operational frameworks that can adopt ‘best of both worlds’ practices: more specialized, manipulative (and likely costly) solutions to be applied when reefs are severely endangered or degraded, in balance with broader scale measures that aim to maintain reef health and do not require sophisticated instrumentation or knowledge to be implemented (such as monitoring water quality) (Fig. 3). In addition, not all intervention measures are needed everywhere and all of the time. Rather, standardized surveys to determine the reef state, for example through measurements of coral cover, reproductive potential, and thermal tolerance, can provide a list of indicated actions (Fig. 3). In all likelihood, no unified approach exists that could be used globally because local conditions can either amplify or reduce climate change impacts and therefore must be considered27.

Continuous monitoring to determine success and identify potential risks or side effects of applied approaches is also critically important. Although survival following bleaching events will ultimately determine how successful the applied intervention measures were in increasing resilience, the identification of potential risks will require more active efforts. For instance, when using selectively bred corals, the coral population structure should be monitored to determine how frequencies of beneficial alleles increase over time or whether outbreeding depression can be observed. Similarly, the application of coral probiotics requires regular monitoring to assess any changes in the microbial community assemblage and potential reapplication of the treatment.

Summary and future perspectives

Coral reefs globally are rapidly degrading, requiring the development and implementation of novel intervention strategies to mitigate the impacts of ongoing climate change and environmental degradation. Research activities are attempting to extend the adaptive capacity of reef-forming corals through integration of novel tools, methods, and environments that are studied to increase the survival of corals under more extreme or variable conditions. A particular emphasis on the coral holobiont as the functional biological unit provides a more complete and better understanding of coral functioning while opening the door for novel strategies and targets to harness and maximize the adaptive capacity of corals and the reefs they build to survive climate change. These emerging approaches need to consider and be tailored towards the different reef, environmental, and ecological conditions. Implementing an adaptive intervention framework tailored around nature-based solutions requires standardized methodology, safety assessments, and analytical routines for consistent and most effective utilization and global coordination.

Work on the following four areas could accelerate implementation of the framework described here, starting with increasing understanding of the role of other coral holobiont entities as targets of adaptive intervention. For instance, endolithic algae (such as Ostreobium) can translocate fixed carbon to the coral during coral bleaching, potentially providing resilience to thermal stress by offering alternate energy provision to sustain coral function234,235. Similarly, corallicolids (Apicomplexa) live inside coral tissues and are only second in abundance to Symbiodiniaceae, but their ecology is still unclear236. Second, extreme environments should be utilized as sources of discovery regarding adaptive mechanisms, powerful probiotics and the biological, ecological and physico-chemical characteristics underlying coral reef refuges81,237,238,239. Third, knowledge from real-world case studies must be expanded: it is currently unknown how much ‘manipulation’ within a given population is ideal ecologically or acceptable from a management perspective. In other words, the relative contribution of selectively bred versus randomly bred coral colonies must be investigated, along with the amount of manipulation needed to exert a measurable effect at the reef level. This knowledge is likely to be highly variable for reefs from different localities37. Similar considerations apply for assisted gene flow or seeding coral larvae approaches.

Last, the application of manipulative approaches will be most effective through standardization and coordination of efforts, which will also allow assessment of feasibility, efficacy, and associated risks in a much quicker and more coherent way41,108,240. Predictions of coral survival are imperfect. All reefs and corals are subject to changing environments, and it is not clear whether the best predictor of future coral colony survival is their past survival. We need to derive standardized analytical and decision frameworks that are accurate, easy to implement, and reliable at predicting measures that provide corals and reefs with the highest chance of survival. Such standardization will be reliant on a global data and knowledge base to enable comparative (meta-)analyses and provide a long-term defined and coordinated strategy to catalyse and ensure effective coral reef conservation.

References

  1. 1.

    Fisher, R. et al. Species richness on coral reefs and the pursuit of convergent global estimates. Curr. Biol. 25, 500–505 (2015).

    Article  Google Scholar 

  2. 2.

    Costanza, R. et al. Changes in the global value of ecosystem services. Glob. Environ. Change 26, 152–158 (2014).

    Article  Google Scholar 

  3. 3.

    Moberg, F. & Folke, C. Ecological goods and services of coral reef ecosystems. Ecol. Econ. 29, 215–233 (1999).

    Article  Google Scholar 

  4. 4.

    Wilkinson, C. Status of Coral Reefs of the World: 2008 (Global Coral Reef Monitoring Network, 2008).

  5. 5.

    Spalding, M. et al. Mapping the global value and distribution of coral reef tourism. Mar. Policy 82, 104–113 (2017).

    Article  Google Scholar 

  6. 6.

    Hoegh-Guldberg, O. Climate change, coral bleaching and the future of the world’s coral reefs. Mar. Freshw. Res. 50, 839–866 (1999). This paper projects loss and degradation of coral reefs on a global scale before it became common knowledge.

    Google Scholar 

  7. 7.

    Hughes, T. P. et al. Global warming transforms coral reef assemblages. Nature 556, 492–496 (2018).

    Article  Google Scholar 

  8. 8.

    Porter, J. W. & Meier, O. W. Quantification of loss and change in Floridian reef coral populations. Am. Zool. 32, 625–640 (1992).

    Article  Google Scholar 

  9. 9.

    Ruzicka, R. R. et al. Temporal changes in benthic assemblages on Florida Keys reefs 11 years after the 1997/1998 El Niño. Mar. Ecol. Prog. Ser. 489, 125–141 (2013).

    Article  Google Scholar 

  10. 10.

    Somerfield, P. J. et al. Changes in coral reef communities among the Florida Keys, 1996–2003. Coral Reefs 27, 951–965 (2008).

    Article  Google Scholar 

  11. 11.

    Lapointe, B. E., Brewton, R. A., Herren, L. W., Porter, J. W. & Hu, C. Nitrogen enrichment, altered stoichiometry, and coral reef decline at Looe Key, Florida Keys, USA: a 3-decade study. Mar. Biol. 166, 108 (2019).

    Article  Google Scholar 

  12. 12.

    Suggett, D. J. & Smith, D. J. Coral bleaching patterns are the outcome of complex biological and environmental networking. Global Change Biol. https://doi.org/10.1111/gcb.14871 (2019).

    Article  Google Scholar 

  13. 13.

    Hughes, T. P. et al. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359, 80–83 (2018).

    Article  Google Scholar 

  14. 14.

    Lesser, M. P. in Coral Reefs: An Ecosystem in Transition (eds Dubinsky, Z. & Stambler, N.) 405–419 (Springer, 2011).

  15. 15.

    Rädecker, N. et al. Heat stress destabilizes symbiotic nutrient cycling in corals. Proc. Natl Acad. Sci. USA 118, e2022653118 (2021). This paper demonstrates that algal symbionts cease photosynthate transfer to coral hosts under heat stress long before visual signs of bleaching (symbiont loss) become evident.

    Article  Google Scholar 

  16. 16.

    Allen, M. R. et al. in Sustainable Development, and Efforts to Eradicate Poverty (eds Masson-Delmotte, V. et al.) 41–91 (IPCC, 2018).

  17. 17.

    Gattuso, J.-P. et al. Contrasting futures for ocean and society from different anthropogenic CO2 emissions scenarios. Science 349, aac4722 (2015).

    Article  Google Scholar 

  18. 18.

    Hughes, D. J. et al. Coral reef survival under accelerating ocean deoxygenation. Nat. Clim. Chang. 10, 296–307 (2020).

    Article  Google Scholar 

  19. 19.

    Durack, P.J., Wijffels, S.E. & Matear, R.J. Ocean salinities reveal strong global water cycle intensification during 1950 to 2000. Science 336, 455-458 (2012).

    Article  Google Scholar 

  20. 20.

    Morris, L. A., Voolstra, C. R., Quigley, K. M., Bourne, D. G. & Bay, L. K. Nutrient availability and metabolism affect the stability of coral–Symbiodiniaceae symbioses. Trends Microbiol. 27, 678–689 (2019).

    Article  Google Scholar 

  21. 21.

    Muller, E. M., Sartor, C., Alcaraz, N. I. & van Woesik, R. Spatial Epidemiology of the Stony-Coral-Tissue-Loss Disease in Florida. Front. Mar. Sci. 7, 163 (2020).

    Article  Google Scholar 

  22. 22.

    Hughes, T. P. et al. Climate change, human impacts, and the resilience of coral reefs. Science 301, 929–933 (2003).

    Article  Google Scholar 

  23. 23.

    Nyström, M., Folke, C. & Moberg, F. Coral reef disturbance and resilience in a human-dominated environment. Trends Ecol. Evol. 15, 413–417 (2000).

    Article  Google Scholar 

  24. 24.

    Wiedenmann, J. et al. Nutrient enrichment can increase the susceptibility of reef corals to bleaching. Nat. Clim. Chang. 3, 160–164 (2012).

    Article  Google Scholar 

  25. 25.

    D’Angelo, C. & Wiedenmann, J. Impacts of nutrient enrichment on coral reefs: new perspectives and implications for coastal management and reef survival. Curr. Opin. Environ. Sust. 7, 82–93 (2014).

    Article  Google Scholar 

  26. 26.

    Thurber, R. L. V. et al. Chronic nutrient enrichment increases prevalence and severity of coral disease and bleaching. Glob. Change Biol. 20, 544–554 (2014).

    Article  Google Scholar 

  27. 27.

    Donovan, M. K. et al. Local conditions magnify coral loss after marine heatwaves. Science 372, 977–980 (2021).

    Article  Google Scholar 

  28. 28.

    Climate change widespread, rapid, and intensifying. IPCC (9 August 2021); https://www.ipcc.ch/2021/08/09/ar6-wg1-20210809-pr.

  29. 29.

    Radchuk, V. et al. Adaptive responses of animals to climate change are most likely insufficient. Nat. Commun. 10, 3109 (2019).

    Article  Google Scholar 

  30. 30.

    Kleypas, J. et al. Designing a blueprint for coral reef survival. Biol. Conserv. 257, 109107 (2021).

    Article  Google Scholar 

  31. 31.

    Gattuso, J.-P. et al. Ocean solutions to address climate change and Its effects on marine ecosystems. Front. Mar. Sci. 5, 337 (2018).

    Article  Google Scholar 

  32. 32.

    Knowlton, N. et al. Rebuilding Coral Reefs: A Decadal Grand Challenge (International Coral Reef Society and Future Earth Coasts, 2021) https://doi.org/10.53642/NRKY9386.

  33. 33.

    Hoegh-Guldberg, O., Kennedy, E. V., Beyer, H. L., McClennen, C. & Possingham, H. P. Securing a long-term future for coral reefs. Trends Ecol. Evol. 33, 936–944 (2018).

    Article  Google Scholar 

  34. 34.

    Zoccola, D. et al. The World Coral Conservatory (WCC): a Noah’s ark for corals to support survival of reef ecosystems. PLoS Biol. 18, e3000823 (2020).

    Article  Google Scholar 

  35. 35.

    Kleinhaus, K. et al. Science, diplomacy, and the Red Sea’s unique coral reef: it’s time for action. Front. Mar. Sci. 7, 90 (2020).

    Article  Google Scholar 

  36. 36.

    van Oppen, M. J. H., Oliver, J. K., Putnam, H. M. & Gates, R. D. Building coral reef resilience through assisted evolution. Proc. Natl Acad. Sci. USA 112, 2307–2313 (2015).

    Article  Google Scholar 

  37. 37.

    Baums, I. B. et al. Considerations for maximizing the adaptive potential of restored coral populations in the western Atlantic. Ecol. Appl. 29, e01978 (2019).

    Article  Google Scholar 

  38. 38.

    Peixoto, R. S., Sweet, M. & Bourne, D. G. Customized medicine for corals. Front. Mar. Sci. 6, 686 (2019).

    Article  Google Scholar 

  39. 39.

    Rinkevich, B. The active reef restoration toolbox is a vehicle for coral resilience and adaptation in a changing world. J. Mar. Sci. Eng. 7, 201 (2019).

    Article  Google Scholar 

  40. 40.

    Boström-Einarsson, L. et al. Coral restoration — a systematic review of current methods, successes, failures and future directions. PLoS ONE 15, e0226631 (2020).

    Article  Google Scholar 

  41. 41.

    Voolstra, C. R. et al. Standardized short-term acute heat stress assays resolve historical differences in coral thermotolerance across microhabitat reef sites. Glob. Chang. Biol. 26, 4328–4343 (2020). This paper highlights the potential of mobile acute heat stress assays to resolve fine-scale differences in coral thermotolerance, suitable for large-scale identification of resilient genotypes/reefs for conservation and restoration approaches.

    Article  Google Scholar 

  42. 42.

    Parkinson, J. E. et al. Molecular tools for coral reef restoration: beyond biomarker discovery. Conserv. Lett. 13, e12687 (2020).

    Article  Google Scholar 

  43. 43.

    Voolstra, C. R. et al. Contrasting heat stress response patterns of coral holobionts across the Red Sea suggest distinct mechanisms of thermal tolerance. Mol. Ecol. https://doi.org/10.1111/mec.16064 (2021).

    Article  Google Scholar 

  44. 44.

    Morikawa, M. K. & Palumbi, S. R. Using naturally occurring climate resilient corals to construct bleaching-resistant nurseries. Proc. Natl Acad. Sci. USA 116, 10586–10591 (2019).

    Article  Google Scholar 

  45. 45.

    Sweet, M. & Brown, B. in Oceanography and Marine Biology — An Annual Review (eds Hughes R.N. et al.) 271–314 (CRC, 2016).

  46. 46.

    Voolstra, C. R. & Ziegler, M. Adapting with microbial help: microbiome flexibility facilitates rapid responses to environmental change. Bioessays 42, e2000004 (2020). This paper proposes microbiome flexibility as a mechanism to aid adaptation to environmental change and posits that capacity for dynamic restructuring of the microbiome is host specific.

    Article  Google Scholar 

  47. 47.

    Jaspers, C. et al. Resolving structure and function of metaorganisms through a holistic framework combining reductionist and integrative approaches. Zoology 133, 81–87 (2019).

    Article  Google Scholar 

  48. 48.

    Torda, G. et al. Rapid adaptive responses to climate change in corals. Nat. Clim. Chang. 7, 627–636 (2017).

    Article  Google Scholar 

  49. 49.

    Ziegler, M., Seneca, F. O., Yum, L. K., Palumbi, S. R. & Voolstra, C. R. Bacterial community dynamics are linked to patterns of coral heat tolerance. Nat. Commun. 8, 14213 (2017). This paper provides the first putative link between bacterial community composition and coral heat tolerance.

    Article  Google Scholar 

  50. 50.

    Morgans, C. A., Hung, J. Y., Bourne, D. G. & Quigley, K. M. Symbiodiniaceae probiotics for use in bleaching recovery. Restor. Ecol. 28, 282–288 (2020).

    Article  Google Scholar 

  51. 51.

    Liew, Y. J. et al. Intergenerational epigenetic inheritance in reef-building corals. Nat. Clim. Chang. 10, 254–259 (2020).

    Article  Google Scholar 

  52. 52.

    Craggs, J. et al. Inducing broadcast coral spawning ex situ: closed system mesocosm design and husbandry protocol. Ecol. Evol. 7, 11066–11078 (2017).

    Article  Google Scholar 

  53. 53.

    Camp, E. F., Schoepf, V. & Suggett, D. J. How can “super corals” facilitate global coral reef survival under rapid environmental and climatic change? Glob. Chang. Biol. 24, 2755–2757 (2018).

    Article  Google Scholar 

  54. 54.

    Peixoto, R. S. et al. Coral probiotics: premise, promise, prospects. Annu. Rev. Anim. Biosci. 9, 265–288 (2021). This paper reviews coral probiotics and critical assessment of applicability.

    Article  Google Scholar 

  55. 55.

    Doering, T. et al. Towards enhancing coral heat tolerance: a “microbiome transplantation” treatment using inoculations of homogenized coral tissues. Microbiome 9, 102 (2021).

    Article  Google Scholar 

  56. 56.

    Howells, E. J. et al. Enhancing the heat tolerance of reef-building corals to future warming. Sci. Adv. 7 (2021).

  57. 57.

    Devlin-Durante, M. K., Miller, M. W., Caribbean Acropora Research Group, Precht, W. F. & Baums, I. B. How old are you? Genet age estimates in a clonal animal. Mol. Ecol. 25, 5628–5646 (2016).

    Article  Google Scholar 

  58. 58.

    Irwin, A. et al. Age and intraspecific diversity of resilient Acropora communities in Belize. Coral Reefs 36, 1111–1120 (2017).

    Article  Google Scholar 

  59. 59.

    Palumbi, S. R., Barshis, D. J., Traylor-Knowles, N. & Bay, R. A. Mechanisms of reef coral resistance to future climate change. Science 344, 895–898 (2014). This paper demonstrates that acclimation and adaptation contribute to coral thermal tolerance and climate resistance at about equal contribution.

    Article  Google Scholar 

  60. 60.

    Barott, K. L. et al. Coral bleaching response is unaltered following acclimatization to reefs with distinct environmental conditions. Proc. Natl Acad. Sci. USA 118, e2025435118 (2021).

    Article  Google Scholar 

  61. 61.

    Thomas, L., López, E. H., Morikawa, M. K. & Palumbi, S. R. Transcriptomic resilience, symbiont shuffling, and vulnerability to recurrent bleaching in reef-building corals. Mol. Ecol. 28, 3371–3382 (2019).

    Article  Google Scholar 

  62. 62.

    Bellantuono, A. J., Granados-Cifuentes, C., Miller, D. J., Hoegh-Guldberg, O. & Rodriguez-Lanetty, M. Coral thermal tolerance: tuning gene expression to resist thermal stress. PLoS ONE 7, e50685 (2012).

    Article  Google Scholar 

  63. 63.

    Barshis, D. J. et al. Genomic basis for coral resilience to climate change. Proc. Natl Acad. Sci. USA 110, 1387–1392 (2013).

    Article  Google Scholar 

  64. 64.

    Savary, R. et al. Fast and pervasive transcriptomic resilience and acclimation of extremely heat-tolerant coral holobionts from the northern Red Sea. Proc. Natl Acad. Sci. USA 118, e2023298118 (2021).

    Article  Google Scholar 

  65. 65.

    Liew, Y. J. et al. Epigenome-associated phenotypic acclimatization to ocean acidification in a reef-building coral. Sci. Adv. 4, eaar8028 (2018).

    Article  Google Scholar 

  66. 66.

    Durante, M. K., Baums, I. B., Williams, D. E., Vohsen, S. & Kemp, D. W. What drives phenotypic divergence among coral clonemates of Acropora palmata? Mol. Ecol. 28, 3208–3224 (2019).

    Article  Google Scholar 

  67. 67.

    Rodríguez-Casariego, J. A. et al. Genome-Wide DNA Methylation Analysis Reveals a Conserved Epigenetic Response to Seasonal Environmental Variation in the Staghorn Coral Acropora cervicornis. Front. Mar. Sci. 7, 822 https://doi.org/10.3389/fmars.2020.560424 (2020).

  68. 68.

    Putnam, H. M. & Gates, R. D. Preconditioning in the reef-building coral Pocillopora damicornis and the potential for trans-generational acclimatization in coral larvae under future climate change conditions. J. Exp. Biol. 218, 2365–2372 (2015).

    Article  Google Scholar 

  69. 69.

    Putnam, H. M., Davidson, J. M. & Gates, R. D. Ocean acidification influences host DNA methylation and phenotypic plasticity in environmentally susceptible corals. Evol. Appl. 9, 1165–1178 (2016).

    Article  Google Scholar 

  70. 70.

    Putnam, H. M., Ritson-Williams, R., Cruz, J. A., Davidson, J. M. & Gates, R. D. Environmentally-induced parental or developmental conditioning influences coral offspring ecological performance. Sci. Rep. 10, 13664 (2020).

    Article  Google Scholar 

  71. 71.

    Drury, C. et al. Genomic variation among populations of threatened coral: Acropora cervicornis. BMC Genomics 17, 286 (2016).

    Article  Google Scholar 

  72. 72.

    Bay, R. A., Rose, N. H., Logan, C. A. & Palumbi, S. R. Genomic models predict successful coral adaptation if future ocean warming rates are reduced. Sci. Adv. 3, e1701413 (2017).

    Article  Google Scholar 

  73. 73.

    Prada, C. et al. Empty niches after extinctions increase population sizes of modern corals. Curr. Biol. 26, 3190–3194 (2016).

    Article  Google Scholar 

  74. 74.

    Robitzch, V., Banguera-Hinestroza, E., Sawall, Y., Al-Sofyani, A. and Voolstra, C.R., 2015. Absence of genetic differentiation in the coral Pocillopora verrucosa along environmental gradients of the Saudi Arabian Red Sea. Front. Mar. Sci. 2, 5 (2015).

    Article  Google Scholar 

  75. 75.

    Van Oppen, M. J. H., Souter, P., Howells, E. J., Heyward, A. & Berkelmans, R. Novel genetic diversity through somatic mutations: fuel for adaptation of reef corals? Diversity 3, 405–423 (2011).

    Article  Google Scholar 

  76. 76.

    Vasquez Kuntz, K. L. et al. Juvenile corals inherit mutations acquired during the parent’s lifespan. Preprint at bioRxiv https://doi.org/10.1101/2020.10.19.345538 (2020).

    Article  Google Scholar 

  77. 77.

    Matz, M. V., Treml, E. A., Aglyamova, G. V. & Bay, L. K. Potential and limits for rapid genetic adaptation to warming in a Great Barrier Reef coral. PLoS Genet. 14, e1007220 (2018).

    Article  Google Scholar 

  78. 78.

    Guest, J. R. et al. Contrasting patterns of coral bleaching susceptibility in 2010 suggest an adaptive response to thermal stress. PLoS ONE 7, e33353 (2012).

    Article  Google Scholar 

  79. 79.

    Coles, S. L. et al. Evidence of acclimatization or adaptation in Hawaiian corals to higher ocean temperatures. PeerJ 6, e5347 (2018).

    Article  Google Scholar 

  80. 80.

    Sully, S., Burkepile, D. E., Donovan, M. K., Hodgson, G. & van Woesik, R. A global analysis of coral bleaching over the past two decades. Nat. Commun. 10, 1264 (2019).

    Article  Google Scholar 

  81. 81.

    Camp, E. F. et al. The future of coral reefs subject to rapid climate change: lessons from natural extreme environments. Front. Mar. Sci. 5, 4 (2018).

    Article  Google Scholar 

  82. 82.

    Oliver, T. A. & Palumbi, S. R. Do fluctuating temperature environments elevate coral thermal tolerance? Coral Reefs 30, 429–440 (2011).

    Article  Google Scholar 

  83. 83.

    Morgan, K. M., Perry, C. T., Smithers, S. G., Johnson, J. A. & Daniell, J. J. Evidence of extensive reef development and high coral cover in nearshore environments: implications for understanding coral adaptation in turbid settings. Sci. Rep. 6, 29616 (2016).

    Article  Google Scholar 

  84. 84.

    Middlebrook, R., Hoegh-Guldberg, O. & Leggat, W. The effect of thermal history on the susceptibility of reef-building corals to thermal stress. J. Exp. Biol. 211, 1050–1056 (2008).

    Article  Google Scholar 

  85. 85.

    Brown, B. E., Dunne, R. P., Edwards, A. J., Sweet, M. J. & Phongsuwan, N. Decadal environmental ‘memory’ in a reef coral? Mar. Biol. 162, 479–483 (2015).

    Article  Google Scholar 

  86. 86.

    Dixon, G., Liao, Y., Bay, L. K. & Matz, M. V. Role of gene body methylation in acclimatization and adaptation in a basal metazoan. Proc. Natl Acad. Sci. USA 115, 13342–13346 (2018).

    Article  Google Scholar 

  87. 87.

    Humanes, A. et al. An experimental framework for selectively breeding corals for assisted evolution. Front. Mar. Sci. 8, 626 (2021).

    Article  Google Scholar 

  88. 88.

    Dixon, G. B. et al. Genomic determinants of coral heat tolerance across latitudes. Science 348, 1460–1462 (2015). This paper demonstrates applicability of assisted evolution via selective breeding.

    Article  Google Scholar 

  89. 89.

    van Oppen, M. J. H. et al. Shifting paradigms in restoration of the world’s coral reefs. Glob. Chang. Biol. 23, 3437–3448 (2017).

    Article  Google Scholar 

  90. 90.

    Fukami, H. et al. Conventional taxonomy obscures deep divergence between Pacific and Atlantic corals. Nature 427, 832–835 (2004).

    Article  Google Scholar 

  91. 91.

    Voolstra, C. R. et al. Consensus guidelines for advancing coral holobiont genome and specimen voucher deposition. Front. Mar. Sci. 8, 1029 (2021).

    Article  Google Scholar 

  92. 92.

    Seneca, F. O. & Palumbi, S. R. The role of transcriptome resilience in resistance of corals to bleaching. Mol. Ecol. 24, 1467–1484 (2015).

    Article  Google Scholar 

  93. 93.

    Evensen, N. R., Fine, M., Perna, G., Voolstra, C. R. & Barshis, D. J. Remarkably high and consistent tolerance of a Red Sea coral to acute and chronic thermal stress exposures. Limnol. Oceanogr. https://doi.org/10.1002/lno.11715 (2021).

    Article  Google Scholar 

  94. 94.

    Cleves, P. A., Strader, M. E., Bay, L. K., Pringle, J. R. & Matz, M. V. CRISPR/Cas9-mediated genome editing in a reef-building coral. Proc. Natl Acad. Sci. USA 115, 5235–5240 (2018).

    Article  Google Scholar 

  95. 95.

    Cleves, P. A. et al. Reduced thermal tolerance in a coral carrying CRISPR-induced mutations in the gene for a heat-shock transcription factor. Proc. Natl Acad. Sci. USA 117, 28899–28905 (2020).

    Article  Google Scholar 

  96. 96.

    Fuller, Z. L. et al. Population genetics of the coral Acropora millepora: toward genomic prediction of bleaching. Science 369, eaba4674 (2020).

    Article  Google Scholar 

  97. 97.

    Yetsko, K. et al. Genetic differences in thermal tolerance among colonies of threatened coral Acropora cervicornis: potential for adaptation to increasing temperature. Mar. Ecol. Prog. Ser. 646, 45–68 (2020).

    Article  Google Scholar 

  98. 98.

    Kenkel, C. D., Almanza, A. T. & Matz, M. V. Fine-scale environmental specialization of reef-building corals might be limiting reef recovery in the Florida Keys. Ecology 96, 3197–3212 (2015).

    Article  Google Scholar 

  99. 99.

    D’Angelo, C. et al. Local adaptation constrains the distribution potential of heat-tolerant Symbiodinium from the Persian/Arabian Gulf. ISME J. 9, 2551–2560 (2015).

    Article  Google Scholar 

  100. 100.

    Safaie, A. et al. High frequency temperature variability reduces the risk of coral bleaching. Nat. Commun. 9, 1671 (2018).

    Article  Google Scholar 

  101. 101.

    Quigley, K. M., Bay, L. K. & van Oppen, M. J. H. Genome-wide SNP analysis reveals an increase in adaptive genetic variation through selective breeding of coral. Mol. Ecol. 29, 2176–2188 (2020).

    Article  Google Scholar 

  102. 102.

    Craggs, J., Guest, J., Bulling, M. & Sweet, M. Ex situ co culturing of the sea urchin, Mespilia globulus and the coral Acropora millepora enhances early post-settlement survivorship. Sci. Rep. 9, 12984 (2019).

    Article  Google Scholar 

  103. 103.

    Quigley, K. M. et al. Variability in fitness trade-offs amongst coral juveniles with mixed genetic backgrounds held in the wild. Front. Mar. Sci. 8, 161 (2021).

    Article  Google Scholar 

  104. 104.

    LaJeunesse, T. C. et al. Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr. Biol. 28, 2570–2580.e6 (2018). This paper provides a revised coral symbiont taxonomy and shows that Symbiodiniaceae diversification coincides with the radiation of reef-building corals.

    Article  Google Scholar 

  105. 105.

    Muscatine, L. The role of symbiotic algae in carbon and energy flux in reef corals. Coral Reefs 25, 75–87 (1990).

    Google Scholar 

  106. 106.

    Trench, R. K. Microalgal–invertebrate symbiosis, a review. Endocytobiosis Cell Res. 9, 135–175 (1993).

    Google Scholar 

  107. 107.

    Pogoreutz, C. et al. in Cellular Dialogues in the Holobiont (eds Bosch, T. C. G. & Hadfield, M. G.) 91–118 (CRC, 2020). https://doi.org/10.1201/9780429277375-7.

  108. 108.

    Hume, B. C. C. et al. SymPortal: a novel analytical framework and platform for coral algal symbiont next-generation sequencing ITS2 profiling. Mol. Ecol. Resour. 19, 1063–1080 (2019).

    Article  Google Scholar 

  109. 109.

    Decelle, J. et al. Worldwide occurrence and activity of the reef-building coral symbiont Symbiodinium in the open ocean. Curr. Biol. 28, 3625–3633.e3 (2018).

    Article  Google Scholar 

  110. 110.

    Aranda, M. et al. Genomes of coral dinoflagellate symbionts highlight evolutionary adaptations conducive to a symbiotic lifestyle. Sci. Rep. 6, 39734 (2016).

    Article  Google Scholar 

  111. 111.

    González-Pech, R. A., Bhattacharya, D., Ragan, M. A. & Chan, C. X. Genome evolution of coral reef symbionts as intracellular residents. Trends Ecol. Evol. 34, 799–806 (2019).

    Article  Google Scholar 

  112. 112.

    Hume, B. C. C., Mejia-Restrepo, A., Voolstra, C. R. & Berumen, M. L. Fine-scale delineation of Symbiodiniaceae genotypes on a previously bleached central Red Sea reef system demonstrates a prevalence of coral host-specific associations. Coral Reefs 39, 583–601 (2020).

    Article  Google Scholar 

  113. 113.

    Howells, E. J. et al. Corals in the hottest reefs in the world exhibit symbiont fidelity not flexibility. Mol. Ecol. 29, 899–911 (2020).

    Article  Google Scholar 

  114. 114.

    Turnham, K. E., Wham, D. C., Sampayo, E. & LaJeunesse, T. C. Mutualistic microalgae co-diversify with reef corals that acquire symbionts during egg development. ISME J. https://doi.org/10.1038/s41396-021-01007-8 (2021).

    Article  Google Scholar 

  115. 115.

    Grottoli, A. G. et al. The cumulative impact of annual coral bleaching can turn some coral species winners into losers. Glob. Chang. Biol. 20, 3823–3833 (2014).

    Article  Google Scholar 

  116. 116.

    LaJeunesse, T. C., Smith, R. T., Finney, J. & Oxenford, H. Outbreak and persistence of opportunistic symbiotic dinoflagellates during the 2005 Caribbean mass coral ‘bleaching’ event. Proc. R. Soc. B Biol. Sci. 276, 4139–4148 (2009).

    Article  Google Scholar 

  117. 117.

    Grégoire, V., Schmacka, F., Coffroth, M. A. & Karsten, U. Photophysiological and thermal tolerance of various genotypes of the coral endosymbiont Symbiodinium sp. (Dinophyceae). J. Appl. Phycol. 29, 1893–1905 (2017).

    Article  Google Scholar 

  118. 118.

    Quigley, K. M., Baker, A. C., Coffroth, M. A., Willis, B. L. & van Oppen, M. J. H. in Coral Bleaching: Patterns, Processes, Causes and Consequences (eds van Oppen, M. J. H. & Lough, J. M.) 111–151 (Springer International, 2018).

  119. 119.

    Ziegler, M., Arif, C. & Voolstra, C. R. in Coral Reefs of the Red Sea (eds Voolstra, C. R. & Berumen, M. L.) 69–89 (Springer International, 2019).

  120. 120.

    Suggett, D. J., Warner, M. E. & Leggat, W. Symbiotic dinoflagellate functional diversity mediates coral survival under ecological crisis. Trends Ecol. Evol. 32, 735–745 (2017).

    Article  Google Scholar 

  121. 121.

    Hume, B. C. C. et al. Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change. Proc. Natl Acad. Sci. USA 113, 4416–4421 (2016).

    Article  Google Scholar 

  122. 122.

    Ochsenkühn, M. A., Röthig, T., D’Angelo, C., Wiedenmann, J. & Voolstra, C. R. The role of floridoside in osmoadaptation of coral-associated algal endosymbionts to high-salinity conditions. Sci. Adv. 3, e1602047 (2017).

    Article  Google Scholar 

  123. 123.

    Baumgarten, S. et al. Integrating microRNA and mRNA expression profiling in Symbiodinium microadriaticum, a dinoflagellate symbiont of reef-building corals. BMC Genomics 14, 704 (2013).

    Article  Google Scholar 

  124. 124.

    Klein, S. G. et al. Symbiodinium mitigate the combined effects of hypoxia and acidification on a noncalcifying cnidarian. Glob. Chang. Biol. 23, 3690–3703 (2017).

    Article  Google Scholar 

  125. 125.

    Liew, Y. J., Li, Y., Baumgarten, S., Voolstra, C. R. & Aranda, M. Condition-specific RNA editing in the coral symbiont Symbiodinium microadriaticum. PLoS Genet. 13, e1006619 (2017).

    Article  Google Scholar 

  126. 126.

    Warner, M. E. & Suggett, D. J. in The Cnidaria, Past, Present and Future: The World of Medusa and Her Sisters (eds Goffredo, S. & Dubinsky, Z.) 489–509 (Springer International, 2016).

  127. 127.

    Levin, R. A. et al. Sex, scavengers, and chaperones: transcriptome secrets of divergent symbiodinium thermal tolerances. Mol. Biol. Evol. 33, 3032 (2016).

    Article  Google Scholar 

  128. 128.

    Nand, A. et al. Genetic and spatial organization of the unusual chromosomes of the dinoflagellate Symbiodinium microadriaticum. Nat. Genet. 53, 618–629 (2021).

    Article  Google Scholar 

  129. 129.

    Buerger, P. et al. Heat-evolved microalgal symbionts increase coral bleaching tolerance. Sci. Adv. 6, eaba2498 (2020).

    Article  Google Scholar 

  130. 130.

    Thornhill, D. J., Howells, E. J., Wham, D. C., Steury, T. D. & Santos, S. R. Population genetics of reef coral endosymbionts (Symbiodinium, Dinophyceae). Mol. Ecol. 26, 2640–2659 (2017).

    Article  Google Scholar 

  131. 131.

    LaJeunesse, T. C. et al. Long-standing environmental conditions, geographic isolation and host–symbiont specificity influence the relative ecological dominance and genetic diversification of coral endosymbionts in the genus Symbiodinium. J. Biogeogr. 37, 785–800 (2010).

    Article  Google Scholar 

  132. 132.

    Parkinson, J. E. et al. Gene expression variation resolves species and individual strains among coral-associated dinoflagellates within the genus Symbiodinium. Genome Biol. Evol. 8, 665–680 (2016).

    Article  Google Scholar 

  133. 133.

    Baker, A. C. Flexibility and specificity in coral–algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu. Rev. Ecol. Evol. Syst. 34, 661–689 (2003).

    Article  Google Scholar 

  134. 134.

    Boulotte, N. M. et al. Exploring the Symbiodinium rare biosphere provides evidence for symbiont switching in reef-building corals. ISME J. 10, 2693–2701 (2016).

    Article  Google Scholar 

  135. 135.

    Ziegler, M., Eguíluz, V. M., Duarte, C. M. & Voolstra, C. R. Rare symbionts may contribute to the resilience of coral–algal assemblages. ISME J. 12, 161–172 (2018).

    Article  Google Scholar 

  136. 136.

    Mies, M., Sumida, P. Y. G., Rädecker, N. & Voolstra, C. R. Marine Invertebrate Larvae Associated with Symbiodinium: A Mutualism from the Start? Front. Ecol. Evol. 5, 56 https://www.frontiersin.org/article/10.3389/fevo.2017.00056 (2017).

  137. 137.

    Cumbo, V. R., Baird, A. H. & van Oppen, M. J. H. The promiscuous larvae: flexibility in the establishment of symbiosis in corals. Coral Reefs 32, 111–120 (2013).

    Article  Google Scholar 

  138. 138.

    Quigley, K. M., Willis, B. L. & Bay, L. K. Heritability of the Symbiodinium community in vertically- and horizontally-transmitting broadcast spawning corals. Sci. Rep. 7, 8219 (2017).

    Article  Google Scholar 

  139. 139.

    National Academies of Sciences, Engineering, and Medicine. A Research Review of Interventions to Increase the Persistence and Resilience of Coral Reefs (National Academies Press, 2019). This book reviews restoration interventions, detailing latest emerging technologies and approaches.

  140. 140.

    Quigley, K. M., Randall, C. J., van Oppen, M. J. H. & Bay, L. K. Assessing the role of historical temperature regime and algal symbionts on the heat tolerance of coral juveniles. Biol. Open 9, bio047316 (2020).

    Article  Google Scholar 

  141. 141.

    McIlroy, S. E. et al. The effects of Symbiodinium (Pyrrhophyta) identity on growth, survivorship, and thermal tolerance of newly settled coral recruits. J. Phycol. 52, 1114–1124 (2016).

    Article  Google Scholar 

  142. 142.

    Thornhill, D. J., Daniel, M. W., LaJeunesse, T. C., Schmidt, G. W. & Fitt, W. K. Natural infections of aposymbiotic Cassiopea xamachana scyphistomae from environmental pools of Symbiodinium. J. Exp. Mar. Bio. Ecol. 338, 50–56 (2006).

    Article  Google Scholar 

  143. 143.

    Coffroth, M. A., Lewis, C. F., Santos, S. R. & Weaver, J. L. Environmental populations of symbiotic dinoflagellates in the genus Symbiodinium can initiate symbioses with reef cnidarians. Curr. Biol. 16, R985–R987 (2006).

    Article  Google Scholar 

  144. 144.

    Fujise, L. et al. Unlocking the phylogenetic diversity, primary habitats, and abundances of free-living Symbiodiniaceae on a coral reef. Mol. Ecol. 30, 343–360 (2021).

    Article  Google Scholar 

  145. 145.

    Levin, R. A. et al. Engineering strategies to decode and enhance the genomes of coral symbionts. Front. Microbiol. 8, 1220 (2017).

    Article  Google Scholar 

  146. 146.

    Chen, J. E., Barbrook, A. C., Cui, G., Howe, C. J. & Aranda, M. The genetic intractability of Symbiodinium microadriaticum to standard algal transformation methods. PLoS ONE 14, e0211936 (2019).

    Article  Google Scholar 

  147. 147.

    Sheykhali, S. et al. Robustness to extinction and plasticity derived from mutualistic bipartite ecological networks. Sci. Rep. 10, 9783 (2020).

    Article  Google Scholar 

  148. 148.

    Quigley, K. M., Bay, L. K. & Willis, B. L. Leveraging new knowledge of Symbiodinium community regulation in corals for conservation and reef restoration. Mar. Ecol. Prog. Ser. 600, 245–253 (2018).

    Article  Google Scholar 

  149. 149.

    LaJeunesse, T. C. et al. Host–symbiont recombination versus natural selection in the response of coral–dinoflagellate symbioses to environmental disturbance. Proc. R. Soc. B: Biol. Sci. 277, 2925–2934 (2010).

    Article  Google Scholar 

  150. 150.

    Poland, D. M. & Coffroth, M. A. Trans-generational specificity within a cnidarian–algal symbiosis. Coral Reefs 36, 119–129 (2017).

    Article  Google Scholar 

  151. 151.

    Sampayo, E. M. et al. Coral symbioses under prolonged environmental change: living near tolerance range limits. Sci. Rep. 6, 36271 (2016).

    Article  Google Scholar 

  152. 152.

    Abrego, D., van Oppen, M. J. H. & Willis, B. L. Onset of algal endosymbiont specificity varies among closely related species of Acropora corals during early ontogeny. Mol. Ecol. 18, 3532–3543 (2009).

    Article  Google Scholar 

  153. 153.

    Pettay, D. T., Wham, D. C., Smith, R. T., Iglesias-Prieto, R. & LaJeunesse, T. C. Microbial invasion of the Caribbean by an Indo-Pacific coral zooxanthella. Proc. Natl Acad. Sci. USA 112, 7513–7518 (2015).

    Article  Google Scholar 

  154. 154.

    Qin, Z. et al. Diversity of Symbiodiniaceae in 15 coral species from the Southern South China Sea: potential relationship with coral thermal adaptability. Front. Microbiol. 10, 2343 (2019).

    Article  Google Scholar 

  155. 155.

    Claar, D. C. et al. Dynamic symbioses reveal pathways to coral survival through prolonged heatwaves. Nat. Commun. 11, 6097 (2020).

    Article  Google Scholar 

  156. 156.

    Lim, E.-P. et al. Continuation of tropical Pacific Ocean temperature trend may weaken extreme El Niño and its linkage to the Southern Annular Mode. Sci. Rep. 9, 17044 (2019).

    Article  Google Scholar 

  157. 157.

    Pollock, F. J. et al. Coral larvae for restoration and research: a large-scale method for rearing Acropora millepora larvae, inducing settlement, and establishing symbiosis. PeerJ 5, e3732 (2017).

    Article  Google Scholar 

  158. 158.

    McFall-Ngai, M. et al. Animals in a bacterial world, a new imperative for the life sciences. Proc. Natl Acad. Sci. USA 110, 3229–3236 (2013).

    Article  Google Scholar 

  159. 159.

    Bosch, T. C. G. & McFall-Ngai, M. J. Metaorganisms as the new frontier. Zoology 114, 185–190 (2011).

    Article  Google Scholar 

  160. 160.

    Robbins, S. J. et al. A genomic view of the reef-building coral Porites lutea and its microbial symbionts. Nat. Microbiol. 4, 2090–2100 (2019).

    Article  Google Scholar 

  161. 161.

    Bang, C. et al. Metaorganisms in extreme environments: do microbes play a role in organismal adaptation? Zoology 127, 1–19 (2018).

    Article  Google Scholar 

  162. 162.

    Williams, A. D., Brown, B. E., Putchim, L. & Sweet, M. J. Age-related shifts in bacterial diversity in a reef coral. PLoS ONE 10, e0144902 (2015).

    Article  Google Scholar 

  163. 163.

    Roder, C., Bayer, T., Aranda, M., Kruse, M. & Voolstra, C. R. Microbiome structure of the fungid coral Ctenactis echinata aligns with environmental differences. Mol. Ecol. 24, 3501–3511 (2015).

    Article  Google Scholar 

  164. 164.

    Sweet, M. J., Brown, B. E., Dunne, R. P., Singleton, I. & Bulling, M. Evidence for rapid, tide-related shifts in the microbiome of the coral Coelastrea aspera. Coral Reefs 36, 815–828 (2017).

    Article  Google Scholar 

  165. 165.

    Ziegler, M. et al. Coral bacterial community structure responds to environmental change in a host-specific manner. Nat. Commun. 10, 3092 (2019).

    Article  Google Scholar 

  166. 166.

    Reshef, L., Koren, O., Loya, Y., Zilber-Rosenberg, I. & Rosenberg, E. The coral probiotic hypothesis. Environ. Microbiol. 8, 2068–2073 (2006).

    Article  Google Scholar 

  167. 167.

    Pogoreutz, C. et al. Dominance of Endozoicomonas bacteria throughout coral bleaching and mortality suggests structural inflexibility of the Pocillopora verrucosa microbiome. Ecol. Evol. 8, 2240–2252 (2018).

    Article  Google Scholar 

  168. 168.

    Neave, M. J. et al. Differential specificity between closely related corals and abundant Endozoicomonas endosymbionts across global scales. ISME J. 11, 186–200 (2017).

    Article  Google Scholar 

  169. 169.

    Neave, M. J., Apprill, A., Ferrier-Pagès, C. & Voolstra, C. R. Diversity and function of prevalent symbiotic marine bacteria in the genus. Endozoicomonas. Appl. Microbiol. Biotechnol. 100, 8315–8324 (2016).

    Article  Google Scholar 

  170. 170.

    Nissimov, J., Rosenberg, E. & Munn, C. B. Antimicrobial properties of resident coral mucus bacteria of Oculina patagonica. FEMS Microbiol. Lett. 292, 210–215 (2009).

    Article  Google Scholar 

  171. 171.

    Sharp, K. H., Sneed, J. M., Ritchie, K. B., Mcdaniel, L. & Paul, V. J. Induction of larval settlement in the reef coral Porites astreoides by a cultivated marine roseobacter strain. Biol. Bull. 228, 98–107 (2015).

    Article  Google Scholar 

  172. 172.

    Rosado, P. M. et al. Marine probiotics: increasing coral resistance to bleaching through microbiome manipulation. ISME J. 13, 921–936 (2019).

    Article  Google Scholar 

  173. 173.

    Sunagawa, S. et al. Bacterial diversity and white plague disease-associated community changes in the Caribbean coral Montastraea faveolata. ISME J. 3, 512–521 (2009).

    Article  Google Scholar 

  174. 174.

    Ushijima, B., Smith, A., Aeby, G. S. & Callahan, S. M. Vibrio owensii induces the tissue loss disease Montipora white syndrome in the Hawaiian reef coral Montipora capitata. PLoS ONE 7, e46717 (2012).

    Article  Google Scholar 

  175. 175.

    Mouchka, M. E., Hewson, I. & Harvell, C. D. Coral-associated bacterial assemblages: current knowledge and the potential for climate-driven impacts. Integr. Comp. Biol. 50, 662–674 (2010).

    Article  Google Scholar 

  176. 176.

    Glasl, B., Herndl, G. J. & Frade, P. R. The microbiome of coral surface mucus has a key role in mediating holobiont health and survival upon disturbance. ISME J. 10, 2280–2292 (2016).

    Article  Google Scholar 

  177. 177.

    Peixoto, R. S. et al. Beneficial Microorganisms for Corals (BMC): proposed mechanisms for coral health and resilience. Front. Microbiol. 8, 341 (2017).

    Article  Google Scholar 

  178. 178.

    Mueller, E. A., Wisnoski, N. I., Peralta, A. L. & Lennon, J. T. Microbial rescue effects: how microbiomes can save hosts from extinction. Funct. Ecol. 34, 2055–2064 (2020).

    Article  Google Scholar 

  179. 179.

    Leite, D. C. A. et al. Coral bacterial-core abundance and network complexity as proxies for anthropogenic pollution. Front. Microbiol. 9, 833 (2018).

    Article  Google Scholar 

  180. 180.

    Fragoso Ados Santos, H. et al. Impact of oil spills on coral reefs can be reduced by bioremediation using probiotic microbiota. Sci. Rep. 5, 18268 (2015).

    Article  Google Scholar 

  181. 181.

    Silva, D. P. et al. Multi-domain probiotic consortium as an alternative to chemical remediation of oil spills at coral reefs and adjacent sites. Microbiome 9, 118 (2021).

    Article  Google Scholar 

  182. 182.

    Welsh, R. M. et al. Alien vs. predator: bacterial challenge alters coral microbiomes unless controlled by Halobacteriovorax predators. PeerJ 5, e3315 (2017).

    Article  Google Scholar 

  183. 183.

    Santoro, E. P. et al. Coral microbiome manipulation elicits metabolic and genetic restructuring to mitigate heat stress and evade mortality. Sci. Adv. 7, eabg3088 (2021).

    Article  Google Scholar 

  184. 184.

    Assis, J. M. et al. Delivering Beneficial Microorganisms for Corals: rotifers as carriers of probiotic bacteria. Front. Microbiol. 11, 608506 (2020).

    Article  Google Scholar 

  185. 185.

    Damjanovic, K., Blackall, L. L., Webster, N. S. & van Oppen, M. J. H. The contribution of microbial biotechnology to mitigating coral reef degradation. Microb. Biotechnol. 10, 1236–1243 (2017).

    Article  Google Scholar 

  186. 186.

    van Oppen, M. J. H. & Blackall, L. L. Coral microbiome dynamics, functions and design in a changing world. Nat. Rev. Microbiol. 17, 557–567 (2019).

    Article  Google Scholar 

  187. 187.

    Sweet, M. et al. Insights into the cultured bacterial fraction of corals. mSystems 6, e0124920 (2021).

    Article  Google Scholar 

  188. 188.

    Brussaard, C. P. D., Baudoux, A.-C. & Rodríguez-Valera, F. in The Marine Microbiome: An Untapped Source of Biodiversity and Biotechnological Potential (eds Stal, L. J. & Cretoiu, M. S.) 155–183 (Springer International, 2016).

  189. 189.

    Levin, R. A., Voolstra, C. R., Weynberg, K. D. & van Oppen, M. J. H. Evidence for a role of viruses in the thermal sensitivity of coral photosymbionts. ISME J. 11, 808–812 (2017).

    Article  Google Scholar 

  190. 190.

    Messyasz, A. et al. Coral bleaching phenotypes associated with differential abundances of nucleocytoplasmic large DNA viruses. Front. Mar. Sci. https://doi.org/10.3389/fmars.2020.555474 (2020).

    Article  Google Scholar 

  191. 191.

    Thurber, R. L. V. et al. Metagenomic analysis indicates that stressors induce production of herpes-like viruses in the coral Porites compressa. Proc. Natl Acad. Sci. USA 105, 18413–18418 (2008).

    Article  Google Scholar 

  192. 192.

    Sweet, M. & Bythell, J. The role of viruses in coral health and disease. J. Invertebr. Pathol. 147, 136–144 (2017).

    Article  Google Scholar 

  193. 193.

    Thurber, R. V., Payet, J. P., Thurber, A. R. & Correa, A. M. S. Virus–host interactions and their roles in coral reef health and disease. Nat. Rev. Microbiol. 15, 205–216 (2017). This paper reviews the role of viruses in coral holobiont biology.

    Article  Google Scholar 

  194. 194.

    Frazão, N., Sousa, A., Lässig, M. & Gordo, I. Horizontal gene transfer overrides mutation in Escherichia coli colonizing the mammalian gut. Proc. Natl Acad. Sci. USA 116, 17906–17915 (2019).

    Article  Google Scholar 

  195. 195.

    Lepage, P. et al. Dysbiosis in inflammatory bowel disease: a role for bacteriophages? Gut 57, 424–425 (2008).

    Article  Google Scholar 

  196. 196.

    Barr, J. J. et al. Bacteriophage adhering to mucus provide a non-host-derived immunity. Proc. Natl Acad. Sci. USA 110, 10771–10776 (2013).

    Article  Google Scholar 

  197. 197.

    Silveira, C. B. & Rohwer, F. L. Piggyback-the-winner in host-associated microbial communities. NPJ Biofilms Microbiomes 2, 16010 (2016).

    Article  Google Scholar 

  198. 198.

    Roach, T. N. F. et al. A multiomic analysis of in situ coral–turf algal interactions. Proc. Natl Acad. Sci. USA 117, 13588–13595 (2020).

    Article  Google Scholar 

  199. 199.

    Cárdenas, A. et al. Coral-associated viral assemblages from the central Red Sea align with host species and contribute to holobiont genetic diversity. Front. Microbiol. 11, 572534 (2020).

    Article  Google Scholar 

  200. 200.

    Bondy-Denomy, J. & Davidson, A. R. When a virus is not a parasite: the beneficial effects of prophages on bacterial fitness. J. Microbiol. 52, 235–242 (2014).

    Article  Google Scholar 

  201. 201.

    Weynberg, K. D., Voolstra, C. R., Neave, M. J., Buerger, P. & van Oppen, M. J. H. From cholera to corals: viruses as drivers of virulence in a major coral bacterial pathogen. Sci. Rep. 5, 17889 (2015).

    Article  Google Scholar 

  202. 202.

    Silveira, C. B. et al. Genomic and ecological attributes of marine bacteriophages encoding bacterial virulence genes. BMC Genomics 21, 126 (2020).

    Article  Google Scholar 

  203. 203.

    Soffer, N., Brandt, M. E., Correa, A. M. S., Smith, T. B. & Thurber, R. V. Potential role of viruses in white plague coral disease. ISME J. 8, 271–283 (2014).

    Article  Google Scholar 

  204. 204.

    Weynberg, K. D. et al. Prevalent and persistent viral infection in cultures of the coral algal endosymbiont Symbiodinium. Coral Reefs 36, 773–784 (2017).

    Article  Google Scholar 

  205. 205.

    Brüwer, J. D., Agrawal, S., Liew, Y. J., Aranda, M. & Voolstra, C. R. Association of coral algal symbionts with a diverse viral community responsive to heat shock. BMC Microbiol. 17, 174 (2017).

    Article  Google Scholar 

  206. 206.

    Jacquemot, L. et al. Therapeutic potential of a new jumbo phage that infects Vibrio coralliilyticus, a widespread coral pathogen. Front. Microbiol. 9, 2501 (2018).

    Article  Google Scholar 

  207. 207.

    Efrony, R., Loya, Y., Bacharach, E. & Rosenberg, E. Phage therapy of coral disease. Coral Reefs 26, 7–13 (2007).

    Article  Google Scholar 

  208. 208.

    Cohen, Y., Joseph Pollock, F., Rosenberg, E. & Bourne, D. G. Phage therapy treatment of the coral pathogen Vibrio coralliilyticus. Microbiologyopen 2, 64–74 (2013).

    Article  Google Scholar 

  209. 209.

    Efrony, R., Atad, I. & Rosenberg, E. Phage therapy of coral white plague disease: properties of phage BA3. Curr. Microbiol. 58, 139–145 (2009).

    Article  Google Scholar 

  210. 210.

    Atad, I., Zvuloni, A., Loya, Y. & Rosenberg, E. Phage therapy of the white plague-like disease of Favia favus in the Red Sea. Coral Reefs 31, 665–670 (2012).

    Article  Google Scholar 

  211. 211.

    Sweet, M. J. & Bulling, M. T. On the importance of the microbiome and pathobiome in coral health and disease. Front. Mar. Sci. 4, 9 (2017).

    Article  Google Scholar 

  212. 212.

    Pollock, F. J., Morris, P. J., Willis, B. L. & Bourne, D. G. The urgent need for robust coral disease diagnostics. PLoS Pathog. 7, e1002183 (2011).

    Article  Google Scholar 

  213. 213.

    Lesser, M. P., Bythell, J. C., Gates, R. D., Johnstone, R. W. & Hoegh-Guldberg, O. Are infectious diseases really killing corals? Alternative interpretations of the experimental and ecological data. J. Exp. Mar. Bio. Ecol. 346, 36–44 (2007).

    Article  Google Scholar 

  214. 214.

    Roder, C., Arif, C., Daniels, C., Weil, E. & Voolstra, C. R. Bacterial profiling of white plague disease across corals and oceans indicates a conserved and distinct disease microbiome. Mol. Ecol. 23, 965–974 (2014).

    Article  Google Scholar 

  215. 215.

    Soffer, N., Zaneveld, J. & Vega Thurber, R. Phage–bacteria network analysis and its implication for the understanding of coral disease. Environ. Microbiol. 17, 1203–1218 (2015).

    Article  Google Scholar 

  216. 216.

    Ubeda, C. et al. Antibiotic-induced SOS response promotes horizontal dissemination of pathogenicity island-encoded virulence factors in staphylococci. Mol. Microbiol. 56, 836–844 (2005).

    Article  Google Scholar 

  217. 217.

    Cárdenas, A. et al. Excess labile carbon promotes the expression of virulence factors in coral reef bacterioplankton. ISME J. 12, 59–76 (2018).

    Article  Google Scholar 

  218. 218.

    Anthony, K. et al. New interventions are needed to save coral reefs. Nat. Ecol. Evol. 1, 1420–1422 (2017).

    Article  Google Scholar 

  219. 219.

    Allard, S. M. et al. Introducing the mangrove microbiome initiative: identifying microbial research priorities and approaches to better understand, protect, and rehabilitate mangrove ecosystems. mSystems https://doi.org/10.1128/mSystems.00658-20 (2020).

    Article  Google Scholar 

  220. 220.

    Zickfeld, K. et al. Long-term climate change commitment and reversibility: An EMIC intercomparison. J. Clim. 26, 5782–5809 (2013).

    Article  Google Scholar 

  221. 221.

    Humanes, A. et al. A framework for selectively breeding corals for assisted evolution. Preprint at bioRxiv https://doi.org/10.1101/2021.02.23.432469 (2021).

    Article  Google Scholar 

  222. 222.

    National Academies of Sciences, Engineering, and Medicine. A Decision Framework for Interventions to Increase the Persistence and Resilience of Coral Reefs (National Academies Press, 2019).

  223. 223.

    Page, C. A., Muller, E. M. & Vaughan, D. E. Microfragmenting for the successful restoration of slow growing massive corals. Ecol. Eng. 123, 86–94 (2018).

    Article  Google Scholar 

  224. 224.

    Schopmeyer, S. A. et al. Regional restoration benchmarks for Acropora cervicornis. Coral Reefs 36, 1047–1057 (2017).

    Article  Google Scholar 

  225. 225.

    Suggett, D. J., Edmondson, J., Howlett, L. & Camp, E. F. Coralclip®: a low-cost solution for rapid and targeted out-planting of coral at scale. Restor. Ecol. 28, 289–296 (2020).

    Article  Google Scholar 

  226. 226.

    Woesik, R. et al. Differential survival of nursery-reared Acropora cervicornis outplants along the Florida reef tract. Restor. Ecol. 29, e13302 (2021).

    Article  Google Scholar 

  227. 227.

    Ware, M. et al. Survivorship and growth in staghorn coral (Acropora cervicornis) outplanting projects in the Florida Keys National Marine Sanctuary. PLoS ONE 15, e0231817 (2020).

    Article  Google Scholar 

  228. 228.

    Ladd, M. C., Shantz, A. A., Bartels, E. & Burkepile, D. E. Thermal stress reveals a genotype-specific tradeoff between growth and tissue loss in restored Acropora cervicornis. Mar. Ecol. Prog. Ser. 572, 129–139 (2017).

    Article  Google Scholar 

  229. 229.

    Goergen, E. A. & Gilliam, D. S. Outplanting technique, host genotype, and site affect the initial success of outplanted Acropora cervicornis. PeerJ 6, e4433 (2018).

    Article  Google Scholar 

  230. 230.

    Chamberland, V. F. et al. New seeding approach reduces costs and time to outplant sexually propagated corals for reef restoration. Sci. Rep. 7, 18076 (2017).

    Article  Google Scholar 

  231. 231.

    Craggs, J., Guest, J., Davis, M. & Sweet, M. Completing the life cycle of a broadcast spawning coral in a closed mesocosm. Invertebr. Reprod. Dev. 64, 244–247 (2020).

    Article  Google Scholar 

  232. 232.

    Hock, K. et al. Connectivity and systemic resilience of the Great Barrier Reef. PLoS Biol. 15, e2003355 (2017).

    Article  Google Scholar 

  233. 233.

    Quigley, K. M., Bay, L. K. & van Oppen, M. J. H. The active spread of adaptive variation for reef resilience. Ecol. Evol. 9, 11122–11135 (2019).

    Article  Google Scholar 

  234. 234.

    Sangsawang, L. et al. 13C and 15N assimilation and organic matter translocation by the endolithic community in the massive coral Porites lutea. R. Soc. Open Sci. 4, 171201 (2017).

    Article  Google Scholar 

  235. 235.

    Pernice, M. et al. Down to the bone: the role of overlooked endolithic microbiomes in reef coral health. ISME J. 14, 325–334 (2020).

    Article  Google Scholar 

  236. 236.

    Kwong, W. K., Del Campo, J., Mathur, V., Vermeij, M. J. A. & Keeling, P. J. A widespread coral-infecting apicomplexan with chlorophyll biosynthesis genes. Nature 568, 103–107 (2019).

    Article  Google Scholar 

  237. 237.

    Fine, M., Gildor, H. & Genin, A. A coral reef refuge in the Red Sea. Glob. Chang. Biol. 19, 3640–3647 (2013).

    Article  Google Scholar 

  238. 238.

    Osman, E. O. et al. Thermal refugia against coral bleaching throughout the northern Red Sea. Glob. Chang. Biol. 24, e474–e484 (2018).

    Article  Google Scholar 

  239. 239.

    Camp, E. F. et al. Corals exhibit distinct patterns of microbial reorganisation to thrive in an extreme inshore environment. Coral Reefs 39, 701–716 (2020).

    Article  Google Scholar 

  240. 240.

    Grottoli, A. G. et al. Increasing comparability among coral bleaching experiments. Ecol. Appl. 31, e02262 (2021).

    Article  Google Scholar 

  241. 241.

    Putnam, H. M., Barott, K. L., Ainsworth, T. D. & Gates, R. D. The vulnerability and resilience of reef-building corals. Curr. Biol. 27, R528–R540 (2017).

    Article  Google Scholar 

  242. 242.

    Hagedorn, M. & Spindler, R. The reality, use and potential for cryopreservation of coral reefs. Adv. Exp. Med. Biol. 753, 317–329 (2014).

    Article  Google Scholar 

  243. 243.

    Hagedorn, M. et al. Successful demonstration of assisted gene flow in the threatened coral Acropora palmata across genetically-isolated caribbean populations using cryopreserved sperm. Cold Spring Harb. Lab. https://doi.org/10.1101/492447 (2018).

    Article  Google Scholar 

  244. 244.

    Hagedorn, M., Spindler, R. & Daly, J. Cryopreservation as a tool for reef restoration: 2019. Adv. Exp. Med. Biol. 1200, 489–505 (2019).

    Article  Google Scholar 

  245. 245.

    Daly, J. et al. Successful cryopreservation of coral larvae using vitrification and laser warming. Sci. Rep. 8, 15714 (2018).

    Article  Google Scholar 

  246. 246.

    Chakravarti, L. J., Beltran, V. H. & van Oppen, M. J. H. Rapid thermal adaptation in photosymbionts of reef-building corals. Glob. Chang. Biol. 23, 4675–4688 (2017).

    Article  Google Scholar 

  247. 247.

    Quigley, K. M., Alvarez Roa, C., Torda, G., Bourne, D. G. & Willis, B. L. Co-dynamics of Symbiodiniaceae and bacterial populations during the first year of symbiosis with Acropora tenuis juveniles. Microbiologyopen 9, e959 (2020).

    Article  Google Scholar 

  248. 248.

    Teplitski, M. & Ritchie, K. How feasible is the biological control of coral diseases? Trends Ecol. Evol. 24, 378–385 (2009).

    Article  Google Scholar 

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Acknowledgements

C.R.V. acknowledges funding from the German Research Foundation (DFG) (grants 433042944 and 458901010). R.S.P. acknowledges funding from King Abdullah University of Science and Technology (grant FCC/1/1973-51-01). J.E.P. acknowledges funding from the University of South Florida Research & Innovation Internal Awards Program (grant 0142687). K.M.Q. acknowledges funding from the Australian Institute of Marine Science (AIMS). E.M.M. was supported by the Mote Eminent Scholarship and the National Science Foundation (NSF) (OCE-1452538). M.A. acknowledges funding from King Abdullah University of Science and Technology (grant FCC/1/1973-36-01).

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Researching data for article: C.R.V., R.P., J.E.P., K.M.Q., C.B.S., M.S., M.A.; substantial contribution to discussion of content: C.R.V., D.J.S., R.P., J.E.P., K.M.Q., C.B.S., D.G.B., M.A.; writing: C.R.V., D.J.S., R.P., J.E.P., K.M.Q., C.B.S., D.G.B., M.A.; review/editing manuscript before submission: C.R.V., D.J.S., R.P., J.E.P., K.M.Q., C.B.S., M.S., E.M.M., D.J.B., D.G.B., M.A.

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Correspondence to Christian R. Voolstra.

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Nature Reviews Earth & Environment thanks D. Huang, who co-reviewed with E. Bollati; J. Wiedenmann; S.-L. Tang; and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Glossary

Coral bleaching

Discolouration of coral tissue due to the loss of microalgal symbionts triggered by climate change-induced ocean warming and thermal stress anomalies.

Assisted evolution

Human interventions aimed at speeding up natural evolutionary processes to increase the rate of adaptation of threatened species.

Adaptive capacity

The ability of coral holobionts to respond and adjust to environmental stress.

Acclimation

The physiological process of becoming accustomed to a new condition.

Environmental adaptation

The process of (meta-)organismal change used more broadly to denote adjustment to prevailing environmental conditions, for example in the context of host microbiome changes

Evolutionary adaptation

The process of genetic change through which populations become better attuned to their environment over generations.

Restoration

The action of returning something to a former condition, for instance through reinstatement of the original functional or genetic diversity.

Environmental hardening

The preconditioning of coral colonies to elevated temperatures as a means to increase tolerance to future heat stress events (can also apply to other stressors).

Microhabitats

A small area that differs from the surrounding habitat, with unique conditions that could select for unique genotypes that might not be found in the remainder of the area.

Beneficial Microorganisms for Corals

(BMCs). Umbrella term to define (microbial) symbionts that promote coral health and can be used as probiotics.

Coral probiotics

Live microorganisms to benefit coral host health.

Coral prebiotics

Molecules that modulate bacterial (microbial) association to benefit coral host health.

Lysis

A common outcome of viral infections, whereby cells are actively induced by viruses to release newly assembled viruses that can then infect other cells.

Genetically modified organisms

(GMOs). Organisms whose genomes are engineered to produce specific traits of interest.

Environmental rehabilitation

The action of restoring to an improved condition to allow species and ecosystems to thrive under altered environmental conditions.

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Voolstra, C.R., Suggett, D.J., Peixoto, R.S. et al. Extending the natural adaptive capacity of coral holobionts. Nat Rev Earth Environ (2021). https://doi.org/10.1038/s43017-021-00214-3

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