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Immunity and the coral crisis

Communications Biologyvolume 1, Article number: 91 (2018) | Download Citation

Abstract

Climate change is killing coral at an unprecedented rate. As immune systems promote homeostasis and survival of adverse conditions I propose we explore coral health in the context of holobiont immunity.

Immunity, purveyor of health

Immune systems are the purveyors of homeostasis and orchestrators of relationships among hosts, mutualists, commensals and pathogens of multipartite organisms, termed holobionts. Immunity underpins the health and survival of these holobionts—withstanding disruption and re-establishing homeostasis in the face of biotic and abiotic perturbations. Physiological trade-offs operating under evolved constraints drive distinct manifestations of immunity and underpin resistance. Variation in immunity therefore likely has a strong influence over coral survivorship under climate-change pressures.

Traditionally, innate immunity was recognized as the system used by invertebrates as a non-specific response to non-self1. But non-specificity and non-self may be out-dated concepts; innate immune systems have targeted responses and memory2,3, and many organisms are not discrete ‘self’ entities with borders to defend4. Corals are complex mutualisms among multicellular partners and associated microbiota, which influence coral physiology sensu latu5,6. Corals and their plethora of mutualists, including the light-harvesting and energy-providing algae Symbiodinium spp. that live inside coral cells, enable all associates to thrive in often nutrient-poor tropical warm waters and build complex reef structures7. Homeostasis of these coral holobionts8 therefore hinges on the immune system accepting mutualists and being vigilant of imposters while managing the housekeeping: clearing dead cells and selecting and maintaining an appropriate commensal microbiota9.

With climate change impacting the entire global marine ecosystem, as well as millions of people, biologists are racing to develop novel approaches to better conserve, restore and manage coral reefs10, which have endured significant impacts since the early 1980s11. To be effective, we need to fully explore, and embrace, the intricacies and complexities of coral holobiont health12. This will require understanding the role of immunity in maintaining and degrading homeostasis, inclusive of mutualisms and under environmental change13,14.

Understanding the dynamics and limitations of coral holobiont immunity is essential for accurately interpreting stress experiments and for elucidating appropriate target genes for assisted evolution of more resilient corals. To stimulate research, I challenge the dogma of coral bleaching as a general stress response distinct from immunity. I also propose the Damage Threshold Hypothesis of Coral Holobiont Susceptibility, a related concept to that described previously for insects15, to conceptualize immune-dynamics under homeostasis and with perturbations.

Homeostasis of self

Immunity is generally treated as an activated response—being switched on from an off state16 during an invasion. However, heightened immune activity is just one of various modalities in which an immune system operates. Immune systems can be viewed as ecosystems of receptors, cells, pathways, chemical mediators, mutualists, invaders, and more. These immune ecosystems therefore maintain homeostasis of health by being constantly active, assessing, checking and making adjustments through continual, normal, immune activity—termed constituent immunity—like our circulating white blood cells and the turn-over of our skin cells16,17. A lack of heightened immune activity in the presence of normally-associated microbiota indicates a tolerance of them, rather than an inactive immune system. This normal conglomerate of organisms, the coral holobiont8, arguably delimits immune self16.

The coral holobiont immune self can be viewed as comparable to the vertebrate or plant with its mitochondria and plastids, though at a much earlier stage of co-evolution. Similar to plants, coevolution of the coral holobiont has occurred under inescapable daily and seasonal fluctuations in abiotic conditions. For plants, this sedentary existence has ensured the necessary development of a finely tuned, integrated and responsive system for maintaining health in the presence of multiple stresses, both biotic and abiotic18. Similarly, the coral holobiont, like those of other organisms19,20, is likely to be maintained in dynamic equilibrium by an interconnected immune system that promotes health and protects partnerships for optimal function, moderates commensals, removes over-abundant, degraded or malfunctioning mutualists21 and embraces new ones14,22 when circumstances warrant. However, the limits of coral holobiont immune systems are being tested as accelerating climate change shifts baseline abiotic conditions and fosters extremes.

The dynamics of immunity

The manifestation of an immune system—including both constituent immunity and immune responses—is variable among and within organisms. This is largely because it requires resources that may otherwise go to other functions23 at both ecological and evolutionary scales24. In this respect, at any given moment, an organism’s immune strategy is the consequence of circumstance-dependent, and phenotypically plastic, physiological trade-offs, occurring within the predetermined constraints of evolutionary trade-offs, as per Life History Theory23. Physiological costs, determining plasticity, can be incurred during both the maintenance and implementation of immunity, and include energy expenditure and potential self-harm (autoimmunity)24. For many organisms, including coral25, such physiological costs may be expressed as a temporary reduction in fecundity or growth, as resources are reallocated, and/or damaged by the immune response24. Coral holobiont homeostasis, as maintained by immunity, is therefore likely directly related to energy availability and the ability to compensate for costs—such as through increased heterotrophy. For organisms, likely including corals, the varying timescales and difficult-to-measure variables, plus potentially hidden compensations24, make the costs of immunity difficult to quantify26. However, the variability in cost allocation is likely responsible for the great variation in both constituent immunity and immune responses observed among and within corals13,27.

Danger model challenges the coral general stress response dogma

Since coral bleaching—the breakdown in mutualism between coral holobiont and Symbiodinium—was first described28, it has largely become synonymous with generic terms including general stress response, stress response or thermal stress response29,30,31,32. Used in reference to coral responses ranging in scale from the gene33 to ecosystem32,34, such terms likely came into common use because of the plethora of stressors that induce coral bleaching29,35. Coral bleaching, and the assumed general stress response, has been a dominant focus of coral health biology for decades, due to its high impact on reefs globally29,33,36,37,38,39. Easy to use and encompassing a wide variety of biological contexts, meanings and mechanisms, coral ‘stress responses’ are often investigated and discussed with little to no reference to immunity, or as a completely separate biological process33,39,40. The continued segregation of stress responses and immunity in the coral literature33,40, or omission of immunity in reference to resilience6,10, has the effect that they are generally treated as distinct. In reality, stress responses and immunity are intrinsically linked and, particularly in the context of the holobiont, are more likely one and the same14,21,41.

In general biology, a stress response typically refers to a hormone-mediated fight or flight reaction42, but can also refer to the integrated stress response (ISR)—a conserved, context-dependent cellular pathway that promotes survival43. ISR, or cellular stress response, is often characterized by a pathogen-killing oxidative burst44 that can lead to damaging oxidative stress45. Since oxidative stress has been reported as a driver of coral-algal mutualism breakdown14,35,46, components of the ISR pathway, including reactive species (e.g., nitric oxide), and antioxidants have been extensively detected in coral holobionts as stress responses to adverse conditions (such as warmer water30,47,48) and with infection31. Consequently, components of the ISR pathway have been proposed as potential gene expression biomarkers (GEB) of thermal stress in the coral holobiont40. However, such so-called stress components may be described as immune modulators49.

Immune responses are triggered upon the detection of danger and/or by a disruption in the structure or function of cells, tissues or mutualisms, to a level that perturbs holobiont homeostasis and affects fitness. Disruptors of homeostasis and elicitors of immunity, may be biotic, abiotic or a combination of both20. They may also be exogenous, such as pathogenic infection, or endogenous such as tumorous growth or cellular instability50. The mechanism of immune signaling to abiotic stress is conserved from plants51 to humans49, and occurs with the extracellular release or leakage of endogenous cell constituents or components45. Such components are considered key to stress responses of cells45. In the Danger Model of immune activity49 cellular ‘danger’ molecules, including heat shock proteins, uric acid and reactive molecules, signal damage and are essential in modulating an effective immune response to various perturbations49,51,52. The coral general stress response, and resultant bleaching, is therefore a component of holobiont immunity14,21. The continued use of terms such as ‘general stress response’, in the absence of reference to immune activity will likely continue to polarize coral health research and handicap our understanding of the acclimation and adaptation potential of corals—something that is being actively investigated53,54.

Combining Self/non-self and Danger theories of immunity

Self/non-self theory, involving suites of pattern recognition receptors that recognize conserved pathogens motifs, was largely accepted to explain pathogen detection and the induction of immune responses55,56. Corals possess many pattern recognition receptors, such as Toll-like receptors, Toll/interleukin-1 receptors and Lectins, which are able to detect microbe-associated molecular patters (MAMPs) and activate signaling pathways so as to produce immune responses (reviewed in Mydlarz, et al.41). However, MAMP detection with subsequent microbe killing by the holobiont immune system confounds the presence of specific mutualist and commensal interactions20. Equally conflicting is that immune responses may occur in the absence of a pathogen, such as with sterile wounding49,57, and disruption may not occur in the presence of non-self (e.g., coral chimeras58). These discrepancies, as well as the extensive crosstalk among pathways triggered by both biotic and abiotic perturbations within coral33,41,59,60,61, plants18,62 and vertebrates alike63, support the suggestion that Self/Non-self Theory alone does not fully represent the dynamics of immune activity. Combining two theories of immune activation, Self/Non-self Theory and the Danger Hypothesis, may hold the key to understanding coral holobiont immune dynamics (Fig. 1)20,64.

Fig. 1
Fig. 1

MAMP detection, danger signaling and available resources determine immune response to disruption. The total disruption of homeostasis is the combination of a challenge with environmental conditions, which can be detected as danger, MAMPs or both. The elicitors detected, including mutualist-derived danger signals, and the available resources determine the type and magnitude of the immune response, which is also traded off against other factors including potential autoimmunity20

Coral immune activity, like that of insects20 and similar to that of plants18 and vertebrates65, is likely a balanced consequence of both MAMP1,56 and danger/damage signal (DAMP—danger associated molecular patterns) detection by pattern recognition receptors49,66 (Fig. 1). Depending on the combination of signals, their intensity and the current condition of the holobiont, an immune response may or may not be induced (Fig. 1)20. Viewing the coral holobiont immune system in this regard gives rise to the potential for context-dependent immune responses and microbiome modulation, which in turn addresses how corals are able to fight pathogens while maintaining their microbiota67. For example, under homeostatic conditions, commensal and mutualistic microbes are detected through pattern recognition receptors of MAMPs, but, in the absence of a danger signal (DAMP), do not elicit an immune response to eliminate them20 (Fig. 1). Furthermore, as a change in abiotic factors can induce the release of danger molecules from mutualists45, including coral endo-mutualists Symbiodinium spp.14,48,68,69, this combination of theories poses a mechanism by which mutualists, and even commensals, may be detected as foe (Fig. 1). However, the immune response elicited may be directly dependent on the physiological context, such as energetic reserves needed to mount an effective response and compensate for autoimmune damage. As such, we can overlay genetic and plastic variation in susceptibility to threats (e.g., disease and adverse environmental conditions13,70), and the observations that different holobionts are able to tolerate or resist a variable amount of challenge to homeostasis, dependant on current physiological constraints24.

Damage threshold hypothesis of coral holobiont susceptibility

Immune systems can use resistance or tolerance strategies to promote fitness in the presence of a perturbation71,72,73,74 (Box 1). The damage threshold hypothesis of insect-pathogen interactions15 proposes that resistance and tolerance are intimately related to the amount of damage/danger signaling an infection incurs, and its effect on fitness. As such, we can expand upon the damage threshold hypothesis15 to form a hypothetical and dynamic framework for how coral holobionts may moderate mutualisms, cohabit with commensals, kill pathogens and manage acute abiotic perturbations (Box 1). While the terms tolerance and resistance, and even resilience are often used interchangeably in coral biology53,54, they represent different immune strategies and outcomes72. Resisting a perturbation incurs high short-term costs, energetically, in rapidly mounting a strong immune response, and in autoimmune damage24. Tolerance, on the other hand, incurs a lower but longer-term cost of continual immune activity that physiologically offsets a damage burden, such as oxidative stress, and possibly more strictly moderates the microbiome15. The damage threshold hypothesis of coral holobiont susceptibility (Box 1, Fig. 2) demonstrates how more tolerant holobionts, with their higher constituent immunity13, may be better able to maintain homeostasis through perturbations (inclusive of a functional microbiome), than holobionts that employ a resistance strategy, which may be more readily overwhelmed. Balancing the trade-offs in immune strategy (Box 1), in the context of life history theory and physiology, may help explain the high variation in susceptibility to perturbations observed among coral holobionts with their dynamic microbiota13,67,75 (Box 1).

Fig. 2
Fig. 2

Damage threshold hypothesis of coral susceptibility. Holobiont with a low susceptibility, tolerance strategy (a) has comparatively high constituent immunity, (b) is intermediate, living closer to the lowered damage threshold (dt) and (c) respresents a highly susceptible holobiont, unable to survive the hypothetical perturbation. a indicates constituent immunity levels, while A and B demonstrate homeostatic tolerance of damage, lowering the burden. C and D represent the magnitude of heightened immunity to a perturbation and D and E indicate resilliance (the time taken to return below the damage threshold) with the shorter duration indicating higher resilience

Coral bleaching and breaching the damage threshold

Under homeostatic conditions, the removal of unwanted algal mutualists from coral tissue is a normal and inconspicuous component of housekeeping by the immune system35. However, more commonly the term coral bleaching is used to refer to an observable paling of part or all of a coral, resulting from the loss of photosynthetic pigments and/or associated Symbiodinium spp.29,35. Coral bleaching, though widely reported as a general stress response, can perhaps more accurately be described as a visually striking immune response to disruption in holobiont homeostasis—one that has exceeded the damage threshold15 (Box 1).

Accelerating global climate change is more frequently pushing tropical water temperatures, and photosynthetically active radiation (PAR) intensities, to and beyond the upper thermal limits of coral holobionts29. The resultant mass coral bleaching events, with their high coral mortality, pose the greatest threat to global coral reef persistence76. Occurring since the 1980s, mass bleaching events are the consequence of many coral holobiont immune systems becoming overwhelmed—pushed, often irreversibly, beyond their damage thresholds—by increasingly extreme environmental conditions. However, there is high variation in coral holobiont susceptibility to such events. Some corals bleach quickly and may die, whereas others take a long time to bleach or may not bleach at all. Such variation in immune tolerance to abiotic stress may be explained using the damage threshold hypothesis of coral holobiont susceptibility (Box 2).

Thermal bleaching events are a relatively recent phenomenon that corals have not necessarily evolved with, and therefore present an unusual perturbation to holobiont homeostasis. Innate immune systems evolved to mitigate acute, short-lived events, such as an infection, with an equally acute immune response, though under daily and seasonal environmental fluctuations. The high short-term investment in immunity is justified by the rapid removal of the threat and limited, or localized, autoimmunity, which can be easily repaired or compensated for once the immediate threat is quelled. A long-term perturbation, such as sustained elevated water temperatures, presents a greater challenge. Holobionts with higher damage thresholds, higher constituent immunity, large energy reserves and/or the ability to compensate for depletions and autoimmune damage (e.g., by feeding and antioxidants), are better able to survive long-term perturbations like bleaching events (Box 2, Fig. 3)30. This raises the question of whether coral holobionts can be trained or modified to increase their damage thresholds and become better able to survive thermal extremes6,77.

Fig. 3
Fig. 3

Damage threshold hypothesis (a) during a thermal bleaching event comparing how a tolerant and a suscpetible holobiont may respond, and (b) a potential mechanism for immune memory through mulitple perturbations

Immune memory, acclimatization and adaptation

Immune memory can be broadly defined as increased resistance upon re-exposure and was considered a phenomenon solely of adaptive immunity. However, innate immune systems of organisms including plants and invertebrates also, arguably, demonstrate immune memory, which is sometimes called priming3. In contradiction of innate immune systems being non-specific, typically, immune memory is investigated as a primed response to a specific parasitic infection, which subsides between challenges and provides resistance upon re-infection. Immune memory can also be an acquired resistance or sustained response that protects against a future challenge—an anticipatory response3,78. In addition to immune memory, innate immune systems, such as those of plants, display cross-tolerance, whereby responding to one perturbation increases tolerance or resistance to others18. Considering the coral holobiont immune system responds to both biotic and abiotic stimuli, immune memory with its heritability described for other invertebrates3, is a tantalizing topic in this era of climate change and coral reef crisis79.

Mechanisms of immune memory vary among organisms, but largely remain to be elucidated, including for coral. The ability of corals to acclimate and/or adapt to more extreme conditions77, potentially through immune memory, and/or immune training79, would clearly benefit restoration, conservation and management efforts. In this vein, genes underpinning traits of coral climate resilience are being sought as targets for assisted evolution, with a focus on cellular stress response components10. However, with our limited comprehension of holobiont immune mechanisms—those of the coral host, algal mutualists and the wider microbiome and their interactions—accurately measuring and interpreting factors that promote tolerance is challenging. In this context it seems we have a fair way to go before effective target genes will be identifiable.

The coral research community has high expectations of the more tolerant ‘super corals’ emerging77,80, being sought and being created53,79. But, whether evolved (assisted or otherwise) or physiological, enhanced tolerance (i.e., an increased damage threshold) will inevitably incur costs24. As well as ensuring coral reef persistence through increasing perturbations, such super corals will need to grow complex reef structures and reproduce sufficiently to maintain ecosystem function, while existing within unavoidable limits of life history trade-offs.

Future directions and concluding remarks

Addressing the dramatic global loss of coral reefs is a daunting and bleak task. However, comprehensively approaching coral health under climate change from an immunological perspective will provide greater insight into survival mechanisms. In research efforts towards unraveling components of coral climate resilience it is imperative we use coral holobionts across the susceptibility range. This will avoid skewed, misleading and confounding results, which likely cannot be accurately generalized to other holobionts or locations. We also need awareness that altering one component of the holobiont, such as a Symbiodinium strain or a single gene, will have knock-on effects that we have not begun to explore. To help conceptualize the dynamics of coral holobiont immunity I have presented a simplified model in the hope it can be used to more accurately interpret immune activity of the multipartite organism and firmly build our foundation of knowledge. With awareness that coral holobiont damage thresholds will likely be species- and system-specific, I hope this model can be used as a framework to develop more targeted approaches and more effective monitoring of reef management, conservation and restoration, including genetic engineering.

Dramatically reducing carbon emissions is key to globally conserving coral reefs. While this largely hinges on political agenda, biologists can utilize a combination of immunological information and physiological natural history to better understand drivers of coral health. In doing so, and while pushing for action on climate change, hopefully we can buy enough time to conserve sufficient coral to maintain ecological function.

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Acknowledgements

The author would like to thank Barbara Brown, John Bythell, Robert Puschendorf, Daniel Janzen and Frank Joyce for comments and constructive criticism during the development of this manuscript.

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Affiliations

  1. School of Biological & Marine Sciences, University of Plymouth, Plymouth, Devon, PL48AA, UK

    • Caroline V. Palmer
  2. Guanacaste Dry Forest Conservation Fund, Devon, PL207NA, UK

    • Caroline V. Palmer

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C.V.P. conceived the idea, evolved it and wrote the manuscript.

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The authors declare no competing interests.

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Correspondence to Caroline V. Palmer.

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https://doi.org/10.1038/s42003-018-0097-4

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