Marcel G. A. van der Heijden

Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity

The functioning and stability of terrestrial ecosystems are determined by plant biodiversity and species composition. However, the ecological mechanisms by which plant biodiversity and species composition are regulated and maintained are not well understood. These mechanisms need to be identified to ensure successful management for conservation and restoration of diverse natural ecosystems. Here we show, by using two independent, but complementary, ecological experiments, that below-ground diversity of arbuscular mycorrhizal fungi (AMF) is a major factor contributing to the maintenance of plant biodiversity and to ecosystem functioning. At low AMF diversity, the plant species composition and overall structure of microcosms that simulate European calcareous grassland fluctuate greatly when the AMF taxa that are present are changed. Plant biodiversity, nutrient capture and productivity in macrocosms that simulate North American old-fields increase significantly with increasing AMF-species richness. These results emphasize the need to protect AMF and to consider these fungi in future management practices in order to maintain diverse ecosystems. Our results also show that microbial interactions can drive ecosystem functions such as plant biodiversity, productivity and variability.

DIFFERENT ARBUSCULAR MYCORRHIZAL FUNGAL SPECIES ARE POTENTIAL DETERMINANTS OF PLANT COMMUNITY STRUCTURE

Almost all natural plant communities contain arbuscular mycorrhizal fungi (AMF). We hypothesized that the species composition of AMF communities could have the potential to determine plant community structure if the growth response to different AMF species or to communities of AMF species varies among plant species. To test the existence of such a differential response we conducted a pot experiment where each of three plant species, Hieracium pilosella, Bromus erectus, and Festuca ovina were inoculated with each of four AMF species, or with a mixture of these four AMF species, or were uninoculated. The AMF species originated from a calcareous grassland in which the three plant species also coexisted. We obtained three pieces of evidence suggesting that AMF have the potential to de- termine plant community structure. First, plant species differed in their dependency on AMF, thus varying in degree of benefit received. Second, specific AMF species and a mixture of these AMF species had significantly different effects on several plant growth variables, and these effects were not the same on each plant species. Third, the amount of variation in the growth response of a plant species to four AMF species and to the mixture of AMF species differed among the plant species. Hieracium differed greatly in its growth response to several AMF species while Bromus did not exhibit much variation in its response to different AMF species. The varying mycorrhizal dependency of different plant species has previously been proposed as a mechanism determining plant community structure. However, we found that the mycorrhizal dependency of a plant species can vary greatly because of differential growth responses to specific AMF species compared to the growth of the uninoculated plants. Consequently mycorrhizal dependency, as a measure indicating how much a plant depends on AMF for its growth, is not necessarily a fixed value and therefore cannot be used as a definitive term. In addition, those plant species with highly variable responses to single AMF species or to combinations of AMF species (AMF communities) will be strongly affected by the specific species of AMF that occupy their roots, in contrast to plant species that do not respond differently to different AMF species. We conclude that, through their differential effects on plant growth, AMF species that co-occur as natural AMF communities have the potential to determine plant community structure, and that future studies on plant population and community structure need to consider the strength of their role as a determinant.

Mycorrhizal ecology and evolution: the past, the present, and the future

Almost all land plants form symbiotic associations with mycorrhizal fungi. These below-ground fungi play a key role in terrestrial ecosystems as they regulate nutrient and carbon cycles, and influence soil structure and ecosystem multifunctionality. Up to 80% of plant N and P is provided by mycorrhizal fungi and many plant species depend on these symbionts for growth and survival. Estimates suggest that there are c. 50 000 fungal species that form mycorrhizal associations with c. 250 000 plant species. The development of high-throughput molecular tools has helped us to better understand the biology, evolution, and biodiversity of mycorrhizal associations. Nuclear genome assemblies and gene annotations of 33 mycorrhizal fungal species are now available providing fascinating opportunities to deepen our understanding of the mycorrhizal lifestyle, the metabolic capabilities of these plant symbionts, the molecular dialogue between symbionts, and evolutionary adaptations across a range of mycorrhizal associations. Large-scale molecular surveys have provided novel insights into the diversity, spatial and temporal dynamics of mycorrhizal fungal communities. At the ecological level, network theory makes it possible to analyze interactions between plant-fungal partners as complex underground multi-species networks. Our analysis suggests that nestedness, modularity and specificity of mycorrhizal networks vary and depend on mycorrhizal type. Mechanistic models explaining partner choice, resource exchange, and coevolution in mycorrhizal associations have been developed and are being tested. This review ends with major frontiers for further research.

Soil biodiversity and soil community composition determine ecosystem multifunctionality

Significance Biological diversity is the foundation for the maintenance of ecosystems. Consequently it is thought that anthropogenic activities that reduce the diversity in ecosystems threaten ecosystem performance. A large proportion of the biodiversity within terrestrial ecosystems is hidden below ground in soils, and the impact of altering its diversity and composition on the performance of ecosystems is still poorly understood. Using a novel experimental system to alter levels of soil biodiversity and community composition, we found that reductions in the abundance and presence of soil organisms results in the decline of multiple ecosystem functions, including plant diversity and nutrient cycling and retention. This suggests that below-ground biodiversity is a key resource for maintaining the functioning of ecosystems. Biodiversity loss has become a global concern as evidence accumulates that it will negatively affect ecosystem services on which society depends. So far, most studies have focused on the ecological consequences of above-ground biodiversity loss; yet a large part of Earth’s biodiversity is literally hidden below ground. Whether reductions of biodiversity in soil communities below ground have consequences for the overall performance of an ecosystem remains unresolved. It is important to investigate this in view of recent observations that soil biodiversity is declining and that soil communities are changing upon land use intensification. We established soil communities differing in composition and diversity and tested their impact on eight ecosystem functions in model grassland communities. We show that soil biodiversity loss and simplification of soil community composition impair multiple ecosystem functions, including plant diversity, decomposition, nutrient retention, and nutrient cycling. The average response of all measured ecosystem functions (ecosystem multifunctionality) exhibited a strong positive linear relationship to indicators of soil biodiversity, suggesting that soil community composition is a key factor in regulating ecosystem functioning. Our results indicate that changes in soil communities and the loss of soil biodiversity threaten ecosystem multifunctionality and sustainability.

Climate change effects on beneficial plant–microorganism interactions

It is well known that beneficial plant-associated microorganisms may stimulate plant growth and enhance resistance to disease and abiotic stresses. The effects of climate change factors such as elevated CO(2), drought and warming on beneficial plant-microorganism interactions are increasingly being explored. This now makes it possible to test whether some general patterns occur and whether different groups of plant-associated microorganisms respond differently or in the same way to climate change. Here, we review the results of 135 studies investigating the effects of climate change factors on beneficial microorganisms and their interaction with host plants. The majority of studies showed that elevated CO(2) had a positive influence on the abundance of arbuscular and ectomycorrhizal fungi, whereas the effects on plant growth-promoting bacteria and endophytic fungi were more variable. In most cases, plant-associated microorganisms had a beneficial effect on plants under elevated CO(2). The effects of increased temperature on beneficial plant-associated microorganisms were more variable, positive and neutral, and negative effects were equally common and varied considerably with the study system and the temperature range investigated. Moreover, numerous studies indicated that plant growth-promoting microorganisms (both bacteria and fungi) positively affected plants subjected to drought stress. Overall, this review shows that plant-associated microorganisms are an important factor influencing the response of plants to climate change.

Nonlegumes, Legumes, and Root Nodules Harbor Different Arbuscular Mycorrhizal Fungal Communities

ABSTRACT Legumes are an important plant functional group since they can form a tripartite symbiosis with nitrogen-fixing Rhizobium bacteria and phosphorus-acquiring arbuscular mycorrhizal fungi (AMF). However, not much is known about AMF community composition in legumes and their root nodules. In this study, we analyzed the AMF community composition in the roots of three nonlegumes and in the roots and root nodules of three legumes growing in a natural dune grassland. We amplified a portion of the small-subunit ribosomal DNA and analyzed it by using restriction fragment length polymorphism and direct sequencing. We found differences in AMF communities between legumes and nonlegumes and between legume roots and root nodules. Different plant species also contained different AMF communities, with different AMF diversity. One AMF sequence type was much more abundant in legumes than in nonlegumes (39 and 13%, respectively). Root nodules contained characteristic AMF communities that were different from those in legume roots, even though the communities were similar in nodules from different legume species. One AMF sequence type was found almost exclusively in root nodules. Legumes and root nodules have relatively high nitrogen concentrations and high phosphorus demands. Accordingly, the presence of legume- and nodule-related AMF can be explained by the specific nutritional requirements of legumes or by host-specific interactions among legumes, root nodules, and AMF. In summary, we found that AMF communities vary between plant functional groups (legumes and nonlegumes), between plant species, and between parts of a root system (roots and root nodules).

Positive effects of organic farming on below‐ground mutualists: large‐scale comparison of mycorrhizal fungal communities in agricultural soils

*The impact of various agricultural practices on soil biodiversity and, in particular, on arbuscular mycorrhizal fungi (AMF), is still poorly understood, although AMF can provide benefit to plants and ecosystems. Here, we tested whether organic farming enhances AMF diversity and whether AMF communities from organically managed fields are more similar to those of species-rich grasslands or conventionally managed fields. *To address this issue, the AMF community composition was assessed in 26 arable fields (13 pairs of organically and conventionally managed fields) and five semi-natural grasslands, all on sandy soil. Terminal restriction fragment length polymorphism community fingerprinting was used to characterize AMF community composition. *The average number of AMF taxa was highest in grasslands (8.8), intermediate in organically managed fields (6.4) and significantly lower in conventionally managed fields (3.9). Moreover, AMF richness increased significantly with the time since conversion to organic agriculture. AMF communities of organically managed fields were also more similar to those of natural grasslands when compared with those under conventional management, and were less uniform than their conventional counterparts, as expressed by higher beta-diversity (between-site diversity). *We suggest that organic management in agro-ecosystems contributes to the restoration and maintenance of these important below-ground mutualists.

MUTUALISTIC STABILITY IN THE ARBUSCULAR MYCORRHIZAL SYMBIOSIS: EXPLORING HYPOTHESES OF EVOLUTIONARY COOPERATION

The 450-million-year-old symbiosis between the majority of land plants and arbuscular mycorrhizal fungi (AMF) is one of the most ancient, abundant, and ecologically important mutualisms on Earth. Yet, the evolutionary stability of mycorrhizal associations is still poorly understood, as it follows none of the constraints thought to stabilize cooperation in other well-known mutualisms. The capacity of both host and symbiont to simultaneously interact with several partners introduces a unique dilemma; detecting and punishing those exploiting the mutualism becomes increasingly difficult if these individuals can continue to access resources from alternative sources. Here, we explore four hypotheses to explain evolutionary cooperation in the arbuscular mycorrhizal symbiosis: (1) pseudo-vertical transmission and spatial structuring of plant and fungal populations leading to local adaptation of partners; (2) luxury resource exchange in which plants trade surplus carbon for excess fungal nutrients; (3) partner choice allowing partners to associate with better cooperators; and (4) host and symbiont sanctions which actively reward good partners and punish less cooperative ones. We propose that mycorrhizal cooperation is promoted by an exchange of surplus resources between partners and enforced through sanctions by one or both partners. These mechanisms may allow plant and fungal genotypes to discriminate against individuals employing exploitative strategies, promoting patterns of partner choice. Together these selection pressures provide a framework for understanding the stabilization of mycorrhizal cooperation over evolutionary time.

Belowground biodiversity effects of plant symbionts support aboveground productivity

Soil microbes play key roles in ecosystems, yet the impact of their diversity on plant communities is still poorly understood. Here we demonstrate that the diversity of belowground plant-associated soil fungi promotes plant productivity and plant coexistence. Using additive partitioning of biodiversity effects developed in plant biodiversity studies, we demonstrate that this positive relationship can be driven by complementarity effects among soil fungi in one soil type and by a selection effect resulting from the fungal species that stimulated plant productivity the most in another soil type. Selection and complementarity effects among fungal species contributed to improving plant productivity up to 82% and 85%, respectively, above the average of the respective fungal species monocultures depending on the soil in which they were grown. These results also indicate that belowground diversity may act as insurance for maintaining plant productivity under differing environmental conditions.

Mycorrhizal fungal identity and diversity relaxes plant–plant competition

There is a great interest in ecology in understanding the role of soil microbial diversity for plant productivity and coexistence. Recent research has shown increases in species richness of mutualistic soil fungi, the arbuscular mycorrhizal fungi (AMF), to be related to increases in aboveground productivity of plant communities. However, the impact of AMF richness on plant-plant interactions has not been determined. Moreover, it is unknown whether species-rich AMF communities can act as insurance to maintain productivity in a fluctuating environment (e.g., upon changing soil conditions). We tested the impact of four different AMF taxa and of AMF diversity (no AMF, single AMF taxa, and all four together) on competitive interactions between the legume Trifolium pratense and the grass Lolium multiflorum grown under two different soil conditions of low and high sand content. We hypothesized that more diverse mutualistic interactions (e.g., when four AMF taxa are present) can ease competitive effects between plants, increase plant growth, and maintain plant productivity across different soil environments. We used quantitative PCR to verify that AMF taxa inoculated at the beginning of the experiment were still present at the end. The presence of AMF reduced the competitive inequality between the two plant species by reducing the growth suppression of the legume by the grass. High AMF richness enhanced the combined biomass production of the two plant species and the yield of the legume, particularly in the more productive soil with low sand content. In the less productive (high sand content) soil, the single most effective AMF had an equally beneficial effect on plant productivity as the mixture of four AMF. Since contributions of single AMF to plant productivity varied between both soils, higher AMF richness would be required to maintain plant productivity in heterogeneous environments. Overall this work shows that AMF diversity promotes plant productivity and that AMF diversity can act as insurance to sustain plant productivity under changing environmental conditions.