Mutualisms weaken the latitudinal diversity gradient among oceanic islands.

The latitudinal diversity gradient (LDG) dominates global patterns of diversity1,2, but the factors that underlie the LDG remain elusive. Here we use a unique global dataset3 to show that vascular plants on oceanic islands exhibit a weakened LDG and explore potential mechanisms for this effect. Our results show that traditional physical drivers of island biogeography4-namely area and isolation-contribute to the difference between island and mainland diversity at a given latitude (that is, the island species deficit), as smaller and more distant islands experience reduced colonization. However, plant species with mutualists are underrepresented on islands, and we find that this plant mutualism filter explains more variation in the island species deficit than abiotic factors. In particular, plant species that require animal pollinators or microbial mutualists such as arbuscular mycorrhizal fungi contribute disproportionately to the island species deficit near the Equator, with contributions decreasing with distance from the Equator. Plant mutualist filters on species richness are particularly strong at low absolute latitudes where mainland richness is highest, weakening the LDG of oceanic islands. These results provide empirical evidence that mutualisms, habitat heterogeneity and dispersal are key to the maintenance of high tropical plant diversity and mediate the biogeographic patterns of plant diversity on Earth.

Plant productivity response to inter- and intra-symbiont diversity: Mechanisms, manifestations and meta-analyses.

Symbiont diversity can have large effects on plant growth but the mechanisms generating this relationship remain opaque. We identify three potential mechanisms underlying symbiont diversity-plant productivity relationships: provisioning with complementary resources, differential impact of symbionts of varying quality and interference between symbionts. We connect these mechanisms to descriptive representations of plant responses to symbiont diversity, develop analytical tests differentiating these patterns and test them using meta-analysis. We find generally positive symbiont diversity-plant productivity relationships, with relationship strength varying with symbiont type. Inoculation with symbionts from different guilds (e.g. mycorrhizal fungi and rhizobia) yields strongly positive relationships, consistent with complementary benefits from functionally distinct symbionts. In contrast, inoculation with symbionts from the same guild yields weak relationships, with co-inoculation not consistently generating greater growth than the best individual symbiont, consistent with sampling effects. The statistical approaches we outline, along with our conceptual framework, can be used to further explore plant productivity and community responses to symbiont diversity, and we identify critical needs for additional research to explore context dependency in these relationships.

Spatial Structure within Root Systems Moderates Stability of Arbuscular Mycorrhizal Mutualism and Plant-Soil Feedbacks.

AbstractThe persistence of mutualisms is paradoxical, as there are fitness incentives for exploitation. This is particularly true for plant-microbe mutualisms like arbuscular mycorrhizae (AM), which are promiscuously horizontally transmitted. Preferential allocation by hosts to the best mutualist can stabilize horizontal mutualisms; however, preferential allocation is imperfect, with its fidelity likely depending on the spatial structure of symbionts in plant roots. In this study we tested AM mutualisms' dependence on two dimensions of spatial structure-the initial spatial association of fungi and the ease of fungal dispersal-through three complementary experiments. We found that fitness of the beneficial AM fungus increased when fungi were initially separate, while initial spatial mixing benefited the fitness of the nonbeneficial fungus. These effects were strongest when dispersal was limited and hosts could discriminate. Additionally, we found that changes in AM fungal proportional abundance induced by spatial structure in roots of a preferentially allocating host produced positive feedbacks on plant growth, showing that interactions between spatial structure and host choice can determine the direction of plant-soil feedbacks. Our results suggest that symbiont spatial structure within plant roots may act as an important modifier of plant preferential allocation and the dynamics of mycorrhizal mutualisms, with potentially cascading effects on plant-plant interactions.

Introducing desirable patches to initiate ecosystem transitions and accelerate ecosystem restoration.

Meeting restoration targets may require active strategies to accelerate natural regeneration rates or overcome the resilience associated with degraded ecosystem states. Introducing desired ecosystem patches in degraded landscapes constitutes a promising active restoration strategy, with various mechanisms potentially causing these patches to become foci from which desired species can re-establish throughout the landscape. This study considers three mechanisms previously identified as potential drivers of introduced patch dynamics: autocatalytic nucleation, directed dispersal, and resource concentration. These mechanisms reflect qualitatively different positive feedbacks. We developed an ecological model framework that compared how the occurrence of each mechanism was reflected in spatio-temporal patch dynamics. We then analyzed the implications of these relationships for optimal restoration design. We found that patch expansion accelerated over time when driven by the autocatalytic nucleation mechanism, while patch expansion driven by the directed dispersal or resource concentration mechanisms decelerated over time. Additionally, when driven by autocatalytic nucleation, patch expansion was independent of patch position in the landscape. However, the proximity of other patches affected patch expansion either positively or negatively when driven by directed dispersal or resource concentration. For autocatalytic nucleation, introducing many small patches was a favorable strategy, provided that each individual patch exceeded a critical patch size. Introducing a single patch or a few large patches was the most effective restoration strategy to initiate the directed dispersal mechanism. Introducing many small patches was the most effective strategy for reaching restored ecosystem states driven by a resource concentration mechanism. Our model results suggest that introducing desirable patches can substantially accelerate ecosystem restoration, or even induce a critical transition from an otherwise stable degraded state toward a desired ecosystem state. However, the potential of this type of restoration strategy for a particular ecosystem may strongly depend on the mechanism driving patch dynamics. In turn, which mechanism drives patch dynamics may affect the optimal spatial design of an active restoration strategy. Each of the three mechanisms considered reflects distinct spatio-temporal patch dynamics, providing novel opportunities for empirically identifying key mechanisms, and restoration designs that introduce desired patches in degraded landscapes according to these patch dynamics.

Preferential Allocation of Benefits and Resource Competition among Recipients Allows Coexistence of Symbionts within Hosts.

AbstractFunctionally variable symbionts commonly co-occur including within the roots of individual plants, in spite of arguments from simple models of the stability of mutualism that predict competitive exclusion among symbionts. We explore this paradox by evaluating the dynamics generated by symbiont competition for plant resources and the plant's preferential allocation to the most beneficial symbiont using a system of differential equations representing the densities of mutualistic and nonmutualistic symbionts and the level of preferentially allocated and nonpreferentially allocated resources for which the symbionts compete. We find that host preferential allocation and costs of mutualism generate resource specialization that makes the coexistence of beneficial and nonbeneficial symbionts possible. Furthermore, coexistence becomes likely because of negative physiological feedbacks in host preferential allocation. We find that biologically realistic models of plant physiology and symbiont competition predict that the coexistence of beneficial and nonbeneficial symbionts should be common in root symbioses and that the density and relative abundance of mutualists should increase in proportion to the needs of the host.

Perennial, but not annual legumes synergistically benefit from infection with arbuscular mycorrhizal fungi and rhizobia: a meta-analysis.

Many plant species simultaneously interact with multiple symbionts, which can, but do not always, generate synergistic benefits for their host. We ask if plant life history (i.e. annual vs perennial) can play an important role in the outcomes of the tripartite symbiosis of legumes, arbuscular mycorrhizal fungi (AMF), and rhizobia. We performed a meta-analysis of 88 studies examining outcomes of legume-AMF-rhizobia interactions on plant and microbial growth. Perennial legumes associating with AMF and rhizobia grew larger than expected based on their response to either symbiont alone (i.e. their response to co-inoculation was synergistic). By contrast, annual legume growth with co-inoculation did not differ from additive expectations. AMF and rhizobia differentially increased phosphorus (P) and nitrogen (N) tissue concentration. Rhizobium nodulation increased with mycorrhizal fungi inoculation, but mycorrhizal fungi colonization did not increase with rhizobium inoculation. Microbial responses to co-infection were significantly correlated with synergisms in plant growth. Our work supports a balanced plant stoichiometry mechanism for synergistic benefits. We find that synergisms are in part driven by reinvestment in complementary symbionts, and that time-lags in realizing benefits of reinvestment may limit synergisms in annuals. Optimization of microbiome composition to maximize synergisms may be critical to productivity, particularly for perennial legumes.

Microbial mediators of plant community response to long-term N and P fertilization: Evidence of a role of plant responsiveness to mycorrhizal fungi.

Climate changes and anthropogenic nutrient enrichment widely threaten plant diversity and ecosystem functions. Understanding the mechanisms governing plant species turnover across nutrient gradients is crucial to developing successful management and restoration strategies. We tested whether and how soil microbes, particularly arbuscular mycorrhizal fungi (AMF), could mediate plant community response to a 15 years long-term N (0, 4, 8, and 16 g N m-2  year-1 ) and P (0 and 8 g N m-2  year-1 ) enrichment in a grassland system. We found N and P enrichment resulted in plant community diversity decrease and composition change, in which perennial C4  graminoids were dramatically reduced while annuals and perennial forbs increased. Metabarcoding analysis of soil fungal community showed that N and P changed fungal diversity and composition, of which only a cluster of AMF identified by the co-occurrence networks analysis was highly sensitive to P treatments and was negatively correlated with shifts in percentage cover of perennial C4  graminoids. Moreover, by estimating the mycorrhizal responsiveness (MR) of 41 plant species in the field experiment from 264 independent tests, we found that the community weighted mean MR of the plant community was substantially reduced with nutrient enrichment and was positively correlated with C4  graminoids percentage cover. Both analyses of covariance and structural equation modeling indicated that the shift in MR rather than AMF composition change was the primary predictor of the decline in perennial C4  graminoids, suggesting that the energy cost invested by C4 plants on those sensitive AMF might drive the inferior competitive abilities compared with other groups. Our results suggest that shifts in the competitive ability of mycorrhizal responsive plants can drive plant community change to anthropogenic eutrophication, suggesting a functional benefit of mycorrhizal mutualism in ecological restoration following climatic or anthropogenic degradation of soil communities.

Environmental identification of arbuscular mycorrhizal fungi using the LSU rDNA gene region: an expanded database and improved pipeline.

Arbuscular mycorrhizal fungi (AMF; Glomeromycota) are difficult to culture; therefore, establishing a robust amplicon-based approach to taxa identification is imperative to describe AMF diversity. Further, due to low and biased sampling of AMF taxa, molecular databases do not represent the breadth of AMF diversity, making database matching approaches suboptimal. Therefore, a full description of AMF diversity requires a tool to determine sequence-based placement in the Glomeromycota clade. Nonetheless, commonly used gene regions, including the SSU and ITS, do not enable reliable phylogenetic placement. Here, we present an improved database and pipeline for the phylogenetic determination of AMF using amplicons from the large subunit (LSU) rRNA gene. We improve our database and backbone tree by including additional outgroup sequences. We also improve an existing bioinformatics pipeline by aligning forward and reverse reads separately, using a universal alignment for all tree building, and implementing a BLAST screening prior to tree building to remove non-homologous sequences. Finally, we present a script to extract AMF belonging to 11 major families as well as an amplicon sequencing variant (ASV) version of our pipeline. We test the utility of the pipeline by testing the placement of known AMF, known non-AMF, and Acaulospora sp. spore sequences. This work represents the most comprehensive database and pipeline for phylogenetic placement of AMF LSU amplicon sequences within the Glomeromycota clade.

Microbiome influence on host community dynamics: Conceptual integration of microbiome feedback with classical host-microbe theory.

Microbiomes have profound effects on host fitness, yet we struggle to understand the implications for host ecology. Microbiome influence on host ecology has been investigated using two independent frameworks. Classical ecological theory powerfully represents mechanistic interactions predicting environmental dependence of microbiome effects on host ecology, but these models are notoriously difficult to evaluate empirically. Alternatively, host-microbiome feedback theory represents impacts of microbiome dynamics on host fitness as simple net effects that are easily amenable to experimental evaluation. The feedback framework enabled rapid progress in understanding microbiomes' impacts on plant ecology, and can also be applied to animal hosts. We conceptually integrate these two frameworks by deriving expressions for net feedback in terms of mechanistic model parameters. This generates a precise mapping between net feedback theory and classic population modelling, thereby merging mechanistic understanding with experimental tractability, a necessary step for building a predictive understanding of microbiome influence on host ecology.

Celebrating INVAM: 35 years of the largest living culture collection of arbuscular mycorrhizal fungi.

The International Culture Collection of (Vesicular-) Arbuscular Mycorrhizal Fungi-INVAM-the largest living culture collection of arbuscular mycorrhizal fungi (AMF) celebrated its 35th year in 2020. The authors record here the mission and goals of INVAM, its contribution as a living culture collection, some historical aspects of INVAM, and describe the advances in mycorrhizology and AMF systematics after INVAM moved to West Virginia University. This commentary emphasizes the importance of a living culture collection to preserve germplasm and to educate and assist researchers in mycorrhizal science.

Pathogens and Mutualists as Joint Drivers of Host Species Coexistence and Turnover: Implications for Plant Competition and Succession.

The potential for either pathogens or mutualists to alter the outcome of interactions between host species has been clearly demonstrated experimentally, but our understanding of their joint influence remains limited. Individually, pathogens and mutualists can each stabilize (via negative feedback) or destabilize (via positive feedback) host-host interactions. When pathogens and mutualists are both present, the potential for simultaneous positive and negative feedbacks can generate a wide range of possible effects on host species coexistence and turnover. Extending existing theoretical frameworks, we explore the range of dynamics generated by simultaneous interactions with pathogens and mutualists and identify the conditions for pathogen or mutualist mediation of host coexistence. We then explore the potential role of microbial mutualists and pathogens in plant species turnover during succession. We show how a combination of positive and negative plant-microbe feedbacks can generate a coexistence state that is part of a set of alternative stable states. This result implies that the outcomes of coexistence from classical plant-soil feedback experiments may be susceptible to disturbances and that empirical investigations of microbially mediated coexistence would benefit from consideration of interactive effects of feedbacks generated from different distinct components of the plant microbiome.

Local adaptation of mycorrhizae communities changes plant community composition and increases aboveground productivity.

Soil microbial communities can have an important role in the adaptation of plants to their local abiotic soil conditions and in mediating plant responses to environmental stress. This has been clearly demonstrated for individual plant species, but it is unknown how locally adapted microbes may affect plant communities. It is possible that the adaptation of microbial communities to local conditions can shape plant community composition. Additionally, it is possible that the effects of locally adapted microorganisms on individual plant species could be altered by co-occurring plant species. We tested these possibilities in plant community mesocosms with soils and mycorrhizal fungi (AMF) from three locations. We found that plant community biomass responded positively to local adaptation of AMF to soil conditions. Plant community composition also changed in response to local adaptation of AMF. Unexpectedly, the strongest benefits of locally adapted AMF went to early successional plant species that have the highest relative growth rates and the lowest responsiveness to the presence of AMF. Late successional plants that responded positively overall to the presence of AMF were often suppressed in communities with local AMF, perhaps because of strong competition from fast growing plant species. These results show that local adaptation of soil microbial communities can shape plant community composition, and the benefits that plants derive from locally adapted microorganisms can be reshaped by the competitive context in which these associations occur.

Soil microbiome mediates positive plant diversity-productivity relationships in late successional grassland species.

Which processes drive the productivity benefits of biodiversity remain a critical, but unanswered question in ecology. We tested whether the soil microbiome mediates the diversity-productivity relationships among late successional plant species. We found that productivity increased with plant richness in diverse soil communities, but not with low-diversity mixtures of arbuscular mycorrhizal fungi or in pasteurised soils. Diversity-interaction modelling revealed that pairwise interactions among species best explained the positive diversity-productivity relationships, and that transgressive overyielding resulting from positive complementarity was only observed with the late successional soil microbiome, which was both the most diverse and exhibited the strongest community differentiation among plant species. We found evidence that both dilution/suppression from host-specific pathogens and microbiome-mediated resource partitioning contributed to positive diversity-productivity relationships and overyielding. Our results suggest that re-establishment of a diverse, late successional soil microbiome may be critical to the restoration of the functional benefits of plant diversity following anthropogenic disturbance.

When and where plant-soil feedback may promote plant coexistence: a meta-analysis.

Plant-soil feedback (PSF) theory provides a powerful framework for understanding plant dynamics by integrating growth assays into predictions of whether soil communities stabilise plant-plant interactions. However, we lack a comprehensive view of the likelihood of feedback-driven coexistence, partly because of a failure to analyse pairwise PSF, the metric directly linked to plant species coexistence. Here, we determine the relative importance of plant evolutionary history, traits, and environmental factors for coexistence through PSF using a meta-analysis of 1038 pairwise PSF measures. Consistent with eco-evolutionary predictions, feedback is more likely to mediate coexistence for pairs of plant species (1) associating with similar guilds of mycorrhizal fungi, (2) of increasing phylogenetic distance, and (3) interacting with native microbes. We also found evidence for a primary role of pathogens in feedback-mediated coexistence. By combining results over several independent studies, our results confirm that PSF may play a key role in plant species coexistence, species invasion, and the phylogenetic diversification of plant communities.

Relative importance of competition and plant-soil feedback, their synergy, context dependency and implications for coexistence.

Plants interact simultaneously with each other and with soil biota, yet the relative importance of competition vs. plant-soil feedback (PSF) on plant performance is poorly understood. Using a meta-analysis of 38 published studies and 150 plant species, we show that effects of interspecific competition (either growing plants with a competitor or singly, or comparing inter- vs. intraspecific competition) and PSF (comparing home vs. away soil, live vs. sterile soil, or control vs. fungicide-treated soil) depended on treatments but were predominantly negative, broadly comparable in magnitude, and additive or synergistic. Stronger competitors experienced more negative PSF than weaker competitors when controlling for density (inter- to intraspecific competition), suggesting that PSF could prevent competitive dominance and promote coexistence. When competition was measured against plants growing singly, the strength of competition overwhelmed PSF, indicating that the relative importance of PSF may depend not only on neighbour identity but also density. We evaluate how competition and PSFs might interact across resource gradients; PSF will likely strengthen competitive interactions in high resource environments and enhance facilitative interactions in low-resource environments. Finally, we provide a framework for filling key knowledge gaps and advancing our understanding of how these biotic interactions influence community structure.

Disturbance reduces the differentiation of mycorrhizal fungal communities in grasslands along a precipitation gradient.

Given that mycorrhizal fungi play key roles in shaping plant communities, greater attention should be focused on factors that determine the composition of mycorrhizal fungal communities and their sensitivity to anthropogenic disturbance. We investigate changes in arbuscular mycorrhizal (AM) fungal community composition across a precipitation gradient in North American grasslands as well as changes occurring with varying degrees of site disturbance that have resulted in invasive plant establishment. We find strong differentiation of AM fungal communities in undisturbed remnant grasslands across the precipitation gradient, whereas communities in disturbed grasslands were more homogeneous. These changes in community differentiation with disturbance are consistent with more stringent environmental filtering of AM fungal communities in undisturbed sites that may also be promoted by more rigid functional constraints imposed on AM fungi by the native plant communities in these areas. The AM fungal communities in eastern grasslands were particularly sensitive to anthropogenic disturbance, with disturbed sites having low numbers of AM fungal operational taxonomic units (OTUs) commonly found in undisturbed sites, and also the proliferation of AM fungal OTUs in disturbed sites. This proliferation of AM fungi in eastern disturbed sites coincided with increased soil phosphorus availability and is consistent with evidence suggesting the fungi represented by these OTUs would provide reduced benefits to native plants. The differentiation of AM fungal communities along the precipitation gradient in undisturbed grasslands but not in disturbed sites is consistent with AM fungi aiding plant adaptation to climate, and suggests they may be especially important targets for conservation and restoration in order to help maintain or re-establish diverse grassland plant communities.

Biogeography of arbuscular mycorrhizal fungi (Glomeromycota): a phylogenetic perspective on species distribution patterns.

Information on the biogeography of arbuscular mycorrhizal fungi (AMF) is important because this group of obligately symbiotic soil microbes is a ubiquitous and functionally critical component of terrestrial ecosystems. In this paper, we utilize a biogeography database summarizing data on AMF species distribution linked to geographic and environmental conditions to describe global distribution patterns and interpret these patterns within a phylogenetic perspective. The data were obtained from accessions in living culture collections (INVAM, CICG), species descriptions, and other published literature from 1960 to 2012. The database contains 7105 records, 6396 of them from 768 published papers and the remaining 709 from culture accessions. Glomeromycotan species were recorded in all seven continents, 87 countries, 11 biogeographical realms, and 14 biomes. The distribution of families differed among climatic zones and continents, but they, together with all genera, appear to be cosmopolitan. Distribution of AMF species shows a slight decrease from low to high latitudes, but this decrease is steeper in the southern than in the northern hemisphere. A total of 189 species is shared between ancient supercontinents Gondwana and Laurasia and 78 species are common to all climatic zones. Ninety-five species (43% of the total) have known cosmopolitan distribution, including members of all genera except Redeckera. Some species have disjunct distribution and 26% of species have been registered from only one continent. Data on AMF distribution challenge the "Everything is everywhere" hypothesis in favor of the "moderate endemicity model" for species distribution. Data from this study provide a foundation to formulate and test hypotheses of biogeographic patterns and processes in Glomeromycota.

Negative plant-phyllosphere feedbacks in native Asteraceae hosts - a novel extension of the plant-soil feedback framework.

Over the past 25 years, the plant-soil feedback (PSF) framework has catalyzed our understanding of how belowground microbiota impact plant fitness and species coexistence. Here, we apply a novel extension of this framework to microbiota associated with aboveground tissues, termed 'plant-phyllosphere feedback (PPFs)'. In parallel greenhouse experiments, rhizosphere and phyllosphere microbiota of con- and heterospecific hosts from four species were independently manipulated. In a third experiment, we tested the combined effects of soil and phyllosphere feedback under field conditions. We found that three of four species experienced weak negative PSF whereas, in contrast, all four species experienced strong negative PPFs. Field-based feedback estimates were highly negative for all four species, though variable in magnitude. Our results suggest that phyllosphere microbiota, like rhizosphere microbiota, can potentially mediate plant species coexistence via negative feedbacks. Extension of the PSF framework to the phyllosphere is needed to more fully elucidate plant-microbiota interactions.

Dominant mycorrhizal association of trees alters carbon and nutrient cycling by selecting for microbial groups with distinct enzyme function.

While it is well established that plants associating with arbuscular mycorrhizal (AM) and ectomycorrhizal (ECM) fungi cycle carbon (C) and nutrients in distinct ways, we have a limited understanding of whether varying abundance of ECM and AM plants in a stand can provide integrative proxies for key biogeochemical processes. We explored linkages between the relative abundance of AM and ECM trees and microbial functioning in three hardwood forests in southern Indiana, USA. Across each site's 'mycorrhizal gradient', we measured fungal biomass, fungal : bacterial (F : B) ratios, extracellular enzyme activities, soil carbon : nitrogen ratio, and soil pH over a growing season. We show that the percentage of AM or ECM trees in a plot promotes microbial communities that both reflect and determine the C to nutrient balance in soil. Soils dominated by ECM trees had higher F : B ratios and more standing fungal biomass than AM stands. Enzyme stoichiometry in ECM soils shifted to higher investment in extracellular enzymes needed for nitrogen and phosphorus acquisition than in C-acquisition enzymes, relative to AM soils. Our results suggest that knowledge of mycorrhizal dominance at the stand or landscape scale may provide a unifying framework for linking plant and microbial community dynamics, and predicting their effects on ecological function.

Microbial population and community dynamics on plant roots and their feedbacks on plant communities.

The composition of the soil microbial community can be altered dramatically due to association with individual plant species, and these effects on the microbial community can have important feedbacks on plant ecology. Negative plant-soil feedback plays primary roles in maintaining plant community diversity, whereas positive plant-soil feedback may cause community conversion. Host-specific differentiation of the microbial community results from the trade-offs associated with overcoming plant defense and the specific benefits associated with plant rewards. Accumulation of host-specific pathogens likely generates negative feedback on the plant, while changes in the density of microbial mutualists likely generate positive feedback. However, the competitive dynamics among microbes depends on the multidimensional costs of virulence and mutualism, the fine-scale spatial structure within plant roots, and active plant allocation and localized defense. Because of this, incorporating a full view of microbial dynamics is essential to explaining the dynamics of plant-soil feedbacks and therefore plant community ecology.