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Community assembly and coexistence in communities of arbuscular mycorrhizal fungi

Abstract

Arbuscular mycorrhizal fungi are asexual, obligately symbiotic fungi with unique morphology and genomic structure, which occupy a dual niche, that is, the soil and the host root. Consequently, the direct adoption of models for community assembly developed for other organism groups is not evident. In this paper we adapted modern coexistence and assembly theory to arbuscular mycorrhizal fungi. We review research on the elements of community assembly and coexistence of arbuscular mycorrhizal fungi, highlighting recent studies using molecular methods. By addressing several points from the individual to the community level where the application of modern community ecology terms runs into problems when arbuscular mycorrhizal fungi are concerned, we aim to account for these special circumstances from a mycocentric point of view. We suggest that hierarchical spatial structure of arbuscular mycorrhizal fungal communities should be explicitly taken into account in future studies. The conceptual framework we develop here for arbuscular mycorrhizal fungi is also adaptable for other host-associated microbial communities.

Introduction: applying models of community assembly and contemporary coexistence theory to communities of arbuscular mycorrhizal fungi: knowledge gaps and difficulties

How communities assemble and which species can coexist in the same locale has been a central question of ecology. The recent advancement of high-throughput molecular barcoding methods has enabled researchers to obtain information on the composition and structure of natural microbial communities more easily than ever. This is especially important for organisms that are difficult to culture, such as arbuscular mycorrhizal (AM) fungi, which are obligate symbionts of plants where they form multispecies symbiont communities in the same root. Given the growing number of molecular studies in the field of AM fungal community research, it is timely to review the progress on understanding the processes that underlie AM fungal community assembly, and highlight the knowledge gaps.

The theoretical framework of community assembly and coexistence (HilleRisLambers et al., 2012) combines a classic filter model of community assembly with modern coexistence theory (Chesson, 2000). The filter model describes a regional pool of species from which the members of local communities are selected by passing through environmental and biotic filters. Modern coexistence theory (Chesson, 2000) addresses interactions on the local scale, which arise from niche differences and fitness similarities. The combined approach therefore acknowledges factors on a wide spatiotemporal scale. Regional and local processes are connected by the neutral process of dispersal. The filter model is further nuanced by taking into account feedbacks, when organisms are not only influenced by but also have an impact on their environmental and biotic filters (Figure 1).

Figure 1
figure1

Applying the combination of a filter model of community assembly and neutral processes for AM fungi. The regional pool of AM fungi consists of species present in the soil and in the roots of the host community. Through local or long-distance dispersal and chance, species reach local habitats. The environmental filter prevents species whose environmental tolerances do not overlap with local conditions from entering the community. The host filter allows colonization only for compatible fungal partners, thus further removing species. The local community reflects the cumulative effects of these processes, and in turn influences them through feedbacks. Horizontal interactions within the symbiotic community and with other non-host species also affect local communities. Local communities in turn contribute to the regional species pools with autochtonous propagule input. The capital letters refer to different AM fungal species. Ellipses with different lines depict different root system communities. Details of the depicted community assembly and coexistence model elements can be found in the section 'Factors affecting AM fungal community assembly: review of the elements of the proposed model' in the main text.

AM fungi are a monophyletic group (phylum Glomeromycota) of asexual, obligately symbiotic fungi with a unique combination of traits regarding morphology, genomic structure and ecology. Within their coenocytic mycelia and spores, multiple, potentially genetically divergent nuclei coexist, making it difficult to delineate an individual even with molecular methods (Table 1). Through intraradical and extraradical mycelia, they occupy a dual niche, the plant root and soil. Both the soil environment and plant root can be described according to a simple filter model as species filters preventing certain AM fungal species from entering the local community. However, the simple filter analogy ends when taking into account that host plants and soil do not remain unchanged during community assembly: AM fungi interact with their hosts through hormonal crosstalk and actively shape soil as ecosystem engineers (See section: 'Feedbacks: AM fungi as ecosystem engineers'). Taking into account these developmental, genetic and ecological angles, the direct adoption of models for community assembly developed for other organism groups is not evident. There are several points from the individual to the community level where the application of modern community ecology terms runs into problems when AM fungi are concerned (Table 1). Especially in the area of coexistence, even for the definitions of such fundamental concepts as ‘fitness’ further research and discussion are needed (Table 2).

Table 1 Fundamental questions in defining levels of biological organization for AM fungi
Table 2 Problems and solution attempts in applying community ecology terms to AM fungi

Here we introduce the elements of a community assembly and coexistence model by highlighting recent research on AM fungal communities. As examples for each element, we included studies that used DNA-based methods (preferentially, high-throughput sequencing approaches) to investigate AM fungal communities.

Factors affecting AM fungal community assembly: review of the elements of the proposed model

Regional pool

AM fungi have species pools with distinct composition according to paleocontinents, although endemic species are rare (Kivlin et al., 2011; Davison et al., 2015). Regionally, observed AM fungal communities are spatially heterogenous, but temporally stable, suggesting a fairly constant soil species pool from which mycorrhizae form during the season (Davison et al., 2012).

Dispersal and chance (neutral processes)

Propagules and vectors of dispersal in AM fungi

AM fungi disperse by autochthonous (local mycelium spread) and allochthonous propagules (spores and other inoculum, such as hyphal fragments or colonized root fragments from outside), with the allochthonous propagules being less important locally (Jumpponen and Egerton-Warburton, 2005). AM fungi often have large spores, and many species are distributed by zoochory (for example, through the guts of rats (Janos et al., 1995), earthworms (Shapiro et al., 1993) and collembolans (Klironomos and Moutoglis, 1999) or on the hooves of bison (Lekberg et al., 2011)) as opposed to wind, where their spores are detected rarely (Egan et al., 2014). Thus, AM fungal species are mostly limited to short-distance dispersal. However, over long timespans, these limited dispersal capabilities allow for a surprisingly efficient spread of taxa (Davison et al., 2015).

Spatial community structure, dispersal limitation and other stochastic processes

AM fungal communities are spatially structured, patchily distributed even in relatively homogenous local environments (Rosendahl and Stukenbrock, 2004; Mummey and Rillig, 2008), which suggests that there are other processes beyond environmental filtering that contribute to the structure of AM fungal communities, for example, dispersal limitation. The relative importance of dispersal to environmental filtering is scale-dependent and varies (soil type and dispersal ability, Lekberg et al., 2007; soil pH, C/N ratio, phosphorus and dispersal, Dumbrell et al., 2010a; soil temperature, plant biomes and dispersal, Kivlin et al., 2011). Dispersal and other neutral processes thus exhibit an effect size spectrum that can be completely masked by extreme environmental heterogeneity or anthropogenic disturbance, resulting in communities more dissimilar than expected under the assumptions of neutral theory. On the other hand, stochastic effects are also limited under very homogeneous environmental conditions because of niche effects (Caruso et al., 2012a).

Environmental filter

Niche partitioning along environmental gradients

The assembly process and the coexistence of AM fungi are influenced by various soil environmental variables, such as pH, soil type, soil chemistry and nutrient availability. As nutrient transport is a function of AM fungi, the effect of nutrient availability is well studied (reviewed in Johnson, 2010). The filtering role of the environment, when some species from the regional pool are not present under certain soil conditions, was shown in fertilizer addition experiments: AM fungal phylotype diversity decreased with increasing N and P availability and some AM fungi were only found in specific soil nutrient conditions (for example, Liu et al., 2012; Camenzind et al., 2014; Liu et al., 2015).

Seasonality

AM fungi show temporal niche partitioning over the course of the year. Previously rare types might replace the dominant species (Husband et al., 2002). As possible explanations for this shift, both changing environment, for example, changes in temperature and sunshine hours (which influence the soil carbon pool, Dumbrell et al., 2011), and the seasonal cycle of the plant community and phenology were suggested.

Disturbance

Increasing agricultural land-use intensity selectively removes rare AM fungal species from the local community (Helgason et al., 1998; Verbruggen et al., 2012). Heavy anthropogenic disturbance, such as plowing, tillage and fungicide treatment, can lower the number of AM fungal species, abundance and root colonization while favoring generalist species (Helgason et al., 1998; Hijri et al., 2006; Helgason et al., 2007; Schnoor et al., 2011). However, disturbance does not always shift communities in a predictable way (Lekberg et al., 2012) probably because of the dominance of stochastic effects (Caruso et al., 2012a).

Host filter

One of the particular features of AM fungal community assembly is the importance of the host filter compared with free-living or facultatively symbiotic organisms. Plants restrict AM fungal diversity in roots (Johnson et al., 2004) and they also differentially influence sporulation (Eom et al., 2000). Given the obligatory symbiotic AM fungal lifestyle, the existence of host effects could be obvious. The non-evident detail in the host–AM fungal relationship is the apparent lack of species-level specificity (there are many fewer AM fungal species than plant species, even though most land plants are mycorrhizal). As an explanation, it was proposed that being able to colonize and to be colonized by a wider range of partners has an evolutionary benefit, and that environmental conditions affect the ability of plants to differentially reward their symbionts (reviewed in Walder and van der Heijden, 2015). In the field, different plant species, and even plants of the same species at different growth stages, associate with different fungal communities from the same soil (Gollotte et al., 2004; Sýkorová et al., 2007; Gosling et al., 2013) and some AM fungi do not colonize certain plants (Helgason et al., 2002). AM fungi differ regarding how beneficial they are for hosts (Helgason et al., 2007), and plants are able to reward better fungal partners with photosynthates (Bever et al., 2009; Kiers et al., 2011). The solution might be that host specificity does not happen at the species level, but on an ecological level, where generalist AM fungi interact with generalist plants while specialists tend to occur in the roots of specialist plants (Öpik et al., 2010; Davison et al., 2011). Furthermore, pairings of hosts and symbionts with similar life history strategies (competitive, stress tolerant, ruderal, as described for AM fungi in Chagnon et al., 2013) are likely more beneficial. The functional traits defining these strategies are often conserved at a higher taxonomic level (Maherali and Klironomos, 2007; Chagnon et al., 2013). Not only the host itself but also neighboring plants (Hausmann and Hawkes, 2009) and plant species richness (Burrows and Pfleger, 2002; Engelmoer and Kiers, 2015) influence fungal communities. In addition, AM fungal preference regarding hosts also exists (Davison et al., 2011).

Non-host biotic interactions and feedbacks

Horizontal interactions between members of local AM fungal communities

Past work has found intense competition for root space (Cano and Bago, 2005; Engelmoer et al., 2014) and even competitive exclusion (Hepper et al., 1988). As opposed to root colonization, the ability of AM fungal species to colonize soil did not influence coexistence (Maherali and Klironomos, 2012). Phylogenetic overdispersion promotes coexistence: communities of more distantly related and functionally different species showed higher realized species richness (Maherali and Klironomos, 2007). Conserved differences in other functional traits, such as timing of spore production and hyphal growth rate, metabolism of photosynthates, P and N uptake, might alleviate competition as well.

Despite the potential importance for commercial use of fungal inocula, the effect of arrival order in AM fungi is not well understood. Priority effects were shown (Mummey et al., 2009); however, it was recently observed that the resident AM fungi did not suffer from reduced growth despite being invaded, which makes competition for space an unlikely explanation, and suggesting downregulation by the host instead (Werner and Kiers, 2015).

Interactions with other non-host organisms

Negative interactions with consumers (fungal grazers), pathogens and parasites could reduce competition between AM fungi. However, collembola feeding on AM fungi had no effect on the community composition (Gange, 2000), and parasitism has not yet been conclusively shown to exist in AM fungi (Purin and Rillig, 2008). Either these interactions are really not important for AM fungal communities or we are limited by data.

AM fungi harbor bacteria associated with their spores. These bacteria promote hyphal growth and stimulate nutrient biodynamics. They might facilitate not only the fungus, but the whole mycorrhizal system by contributing to the suppression of soil-borne plant pathogens and by adding nitrogen fixation to the benefits of the plant (Cruz and Ishii, 2011).

Feedbacks: AM fungi as ecosystem engineers

AM fungi significantly modify their habitat both in the soil and in the plant in a way that influences their own communities. In the soil they increase soil aggregation and the water stability of the aggregates by a variety of mechanisms, including hyphal enmeshment (Rillig et al., 2015). Greater particle size and pore space may in turn benefit hyphal growth (Rillig and Steinberg, 2002).

They affect plant diversity and composition by improving the nutrient status of their host plants and by facilitating their hosts, which was shown to induce shifts in plant communities (van der Heijden et al., 1998). To harness this effect, enhancing natural AM fungal communities is suggested as an environmentally friendly weed-control option in agricultural ecosystems (Cameron, 2010). On the other hand, plant community composition also has an effect on AM fungal communities, completing the feedback loop.

Relative importance of different elements: possible explanations for the idiosyncratic response of AM fungi to biotic and abiotic variables

Despite the considerable literature that exists on the host, abiotic environmental and neutral factors influencing AM fungal community composition, there is no consensus on their relative importance. AM fungi have an idiosyncratic response to these variables. We propose two hypotheses to explain this pattern.

‘Law of the minimum’: an idea from plant nutrition

In agricultural science, the ‘law of the minimum’ is an idea that the scarcest essential nutrient (the most limiting factor) is the most important in determining plant growth (Gorban et al., 2011). Similarly, but stepping away from only thinking about resources, the relative importance of assembly factors would depend on the most restrictive component, and the most limiting factor would explain the most variability. Under non-filtering environmental conditions, in an abiotically homogenous sampling area, host effects would be relatively more important. A strong environmental gradient that includes harsh conditions unsuitable for certain species would result in environmental filtering as the dominant structuring force.

Scale dependency: different assembly rules for different spatial scales? An analogy borrowed from parasite communities

Studies on AM fungal communities vary strongly in the spatial scale being addressed. Definitions range from AM fungi found in a root piece through an entire root system to a mixed root sample of an entire site. As different assembly factors act on different scales, explicitly considering the spatial structure of AM fungal communities could lead to a synthesis between contrasting responses to assembly factors (for example, host versus abiotic environmental filter). Parasitology defines a hierarchical, host-based, scale-dependent community system (Figure 2 and Table 1). In infra- and compound communities of fleas, which also have varying levels of host specificity, the relative importance of environmental and host effects depends on the spatial scale (Linardi and Krasnov, 2013; Krasnov et al., 2015). AM fungal communities have a similar host-based hierarchical spatial structure (Figure 2); therefore, it is a compelling idea that the relative importance of assembly factors depends on the spatial scale in AM fungi too. Maherali and Klironomos (2012) hypothesized that subplot-scale interactions (infracommunity) such as competition could determine coexistence, whereas the AM fungal composition of a whole site (compound community) would mostly depend on niche requirements or climate (environmental filter). Consequently, AM fungal communities are found to show phylogenetic clustering within study sites (Kivlin et al., 2011), with sometimes negligible effects of the environment (Horn et al., 2014), which might indicate facilitation between species. At a global scale, the AM fungal community composition was shown to be best predicted by spatial distance, edaphic and climatic factors, and plant community type (Kivlin et al., 2011; Davison et al., 2015). To sum up, the scale dependency of the relative importance of the elements of community assembly and coexistence is well established in many organisms; however, explicit consideration of spatial scale in AM fungal community studies is still rare. An example of how the relative importance of the assembly processes might change with spatial scales is shown in Figure 2.

Figure 2
figure2

Hierarchical scale-dependent community system in AM fungi. At a given spatial (or temporal) scale, multiple processes influence the assembly of AM fungal communities. Relative importance of assembly processes changes with spatial scale, causing idiosyncrasy in response to different assembly factors, when the hierarchical spatial structure is not explicitly considered.

Conclusion: community ecology from the viewpoint of a microbial symbiont

We presented a conceptual framework of community assembly and coexistence adapted to a microbial symbiont group with a unique combination of characteristics. The importance of factors influencing obligate symbionts differs from those affecting free-living organisms, or even facultative symbionts (Linardi and Krasnov, 2013). The host–AM fungal relationship, similarly to parasites, exhibits a hierarchical spatial structure, which should be explicitly incorporated into future studies, to enable the study of the scale dependency of the relative importance of elements of community assembly. Adapting a symbiont-centered point of view in addition to considering how the host community is affected would help to fill the knowledge gaps of coexistence research, especially in the field of non-host interactions.

Outlook: how further research on AM fungal communities could advance the field of community assembly and coexistence theory

Owing to the advance of high-throughput molecular methods, researchers gained insight into the communities of specialized organisms, for example, the AM fungal communities in plant roots. With the number of AM fungal community studies rising, it is now possible to start to piece together the mechanisms influencing community assembly and coexistence. By considering the unique combination of characteristics in genetic makeup, physiology, niche and dispersal of AM fungi, and highlighting problems in applying community ecology concepts stemming from these, we are getting closer to adapting community assembly and coexistence models to them.

Taking levels of community organization related to the host into account (infracommunities, component communities and compound communities, see Figure 2) can help reconcile contrasting results regarding the relative importance of assembly factors.

In AM fungi, where the effect of the host filter is so significant, non-host biotic interactions, although they might not be able to act as a filter in community assembly, are still influencing community structure, and future studies in this currently neglected field might reveal more interesting relations.

Examining different assembly and coexistence factors in a multitude of specialized microbial groups would help advance the field of community ecology by increasing the external validity of its models and theories. Although it is important to transfer concepts from general ecology, it is critical that these concepts be carefully evaluated before application (Table 1): two examples are the application of metacommunity concepts to symbiotic systems (Veresoglou et al., 2012) and the use of network theory in mycorrhizal ecology (Caruso et al., 2012b); in both cases it is important to verify the validity of assumptions lest analyses be misleading. Emerging concepts in community ecology, like metrics for quantifying intransitive competition (Soliveres et al., 2015) or community coalescence (Rillig et al., 2015), will require similar validation to apply them to specific microbial communities. Doing so can lead to new hypotheses in the AM fungal and broader community ecology, as in applying community phylogenetics (Webb et al., 2002 ; Vamosi et al, 2009) to AM fungi: after carefully proving that AM fungal traits related to spatial niche use are conserved at a higher taxonomic level (Maherali and Klironomos, 2007), this was used to generate hypotheses and a theoretical framework on the coupling of plant and AM fungal life history strategies (Chagnon et al., 2013).

Answers to the questions of community assembly and coexistence in AM fungi are increasingly required in order to more successfully manage AM fungi for application. Community composition influences ecosystem services, which is true also for AM fungi (van der Heijden et al., 1998). Better understanding of AM fungal communities could be a powerful tool in mitigating the effects of global change, for example, in agriculture and habitat restoration.

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Acknowledgements

We thank the editor, two reviewers and W Zheng for their valuable comments. MCR thanks BMBF for funding through the BonaRes initiative (INPLAMINT). SH and KV thank DFG (grant number HE 6183/1-1). UM thanks DRS HONORS Fellowship programme of Freie Universität Berlin.

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Vályi, K., Mardhiah, U., Rillig, M. et al. Community assembly and coexistence in communities of arbuscular mycorrhizal fungi. ISME J 10, 2341–2351 (2016). https://doi.org/10.1038/ismej.2016.46

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