Miranda M. Hart

Reciprocal Rewards Stabilize Cooperation in the Mycorrhizal Symbiosis

Plants and their associated fungi reward partners that offer the best resources to sustain mutualism in complex systems. Plants and their arbuscular mycorrhizal fungal symbionts interact in complex underground networks involving multiple partners. This increases the potential for exploitation and defection by individuals, raising the question of how partners maintain a fair, two-way transfer of resources. We manipulated cooperation in plants and fungal partners to show that plants can detect, discriminate, and reward the best fungal partners with more carbohydrates. In turn, their fungal partners enforce cooperation by increasing nutrient transfer only to those roots providing more carbohydrates. On the basis of these observations we conclude that, unlike many other mutualisms, the symbiont cannot be “enslaved.” Rather, the mutualism is evolutionarily stable because control is bidirectional, and partners offering the best rate of exchange are rewarded.

Plant coexistence mediated by arbuscular mycorrhizal fungi

Recent research has indicated the importance of arbuscular mycorrhizal fungi (AMF) in mediating plant coexistence. Coarse-scale studies compare the effects of the presence versus absence of AMF on plant coexistence, a phenomenon that is most relevant in early successional ecosystems where AMF are patchily distributed. By contrast, fine-scale studies investigate interactions that might occur once AMF have developed more fully within ecosystems, and most plants come into contact with AMF. Whereas coarse-scale effects are well understood, our understanding of fine-scale factors is just developing, as a result of investigations into AMF‐ plant specificity, AMF species richness, shared mycelial networks, and plant‐AMF feedback effects. Further research into these areas will provide a better understanding of factors that mediate plant species co-existence and, ultimately, the maintenance of biodiversity within plant communities. The term ‘coexistence’ has been used by ecologists to describe a balanced mixture of species in a biotic community. Such coexistence is a biological riddle, because the tendency towards competitive exclusion should favour a monoculture. Theories attempting to explain plant coexistence have focused on either interactions among species, such as competitive balance [1–3], or the avoidance of interaction among species [4,5]. Non-interaction theories have traditionally examined the role of spatial segregation and disturbance in promoting or suppressing plant coexistence. Agent-mediated coexistence is a non-interaction theory proposed as a mechanism for maintaining multi-species assemblages in plant communities [6,7]. When the ‘agent’ is a pathogen or a predator, it can reduce the ability of a plant to compete for resources if the tissues affected are involved in resource gathering (root or leaf). Often, the effects of pathogens and predators can be density dependent, in that the most abundant host plant species loses more tissue than do less abundant plant species. As a result, less abundant plant species experience reduced competition, lessening their chance of competitive exclusion, and thus promoting species coexistence within plant communities.

Phylogenetic trait conservatism and the evolution of functional trade-offs in arbuscular mycorrhizal fungi

The diversity of functional and life-history traits of organisms depends on adaptation as well as the legacy of shared ancestry. Although the evolution of traits in macro-organisms is well studied, relatively little is known about character evolution in micro-organisms. Here, we surveyed an ancient and ecologically important group of microbial plant symbionts, the arbuscular mycorrhizal (AM) fungi, and tested hypotheses about the evolution of functional and life-history traits. Variation in the extent of root and soil colonization by AM fungi is constrained to a few nodes basal to the most diverse groups within the phylum, with relatively little variation associated with recent divergences. We found no evidence for a trade-off in biomass allocated to root versus soil colonization in three published glasshouse experiments; rather these traits were positively correlated. Partial support was observed for correlated evolution between fungal colonization strategies and functional benefits of the symbiosis to host plants. The evolution of increased soil colonization was positively correlated with total plant biomass and shoot phosphorus content. Although the effect of AM fungi on infection by root pathogens was phylogenetically conserved, there was no evidence for correlated evolution between the extent of AM fungal root colonization and pathogen infection. Variability in colonization strategies evolved early in the diversification of AM fungi, and we propose that these strategies were influenced by functional interactions with host plants, resulting in an evolutionary stasis resembling trait conservatism.

Colonization of roots by arbuscular mycorrhizal fungi using different sources of inoculum.

Abstract. Arbuscular mycorrhizal fungi (AMF) form a number of different infective propagules that are used to form new mycorrhizal associations. These are spores, extraradical hyphae and infected roots. However, not all fungi are equally capable of colonizing roots with all of the above-mentioned propagules and there is conflicting evidence of major differences in colonization strategy between members of the Glomineae and Gigasporineae. In this study, we tested the abilities of eight fungal species from four different genera to colonize roots using three different types of inoculum. Glomus and Acaulospora isolates colonized from all inoculum types, whereas Gigaspora and Scutellospora isolates colonized mainly from spores and to a limited degree from root fragments. Extraradical hyphae were not suitable propagules for the species of Gigaspora and Scutellospora tested. This indicates that AMF have different colonization strategies and that this is largely differentiated at the suborder level. It is unclear why there is such a difference among the fungi in inoculum types. Future research should examine differences in the anatomy and physiology to discern a mechanism for such differences in life-history strategies.

Food-web dynamics. Animal nitrogen swap for plant carbon.

Predatory plants are typically found in discrete groups living under conditions of extreme nutrient stress. But we show here how a common species of boreal tree can act indirectly as a predator of arthropods living in the soil by virtue of a fungal symbiont that supplies it with animal nitrogen in exchange for the plants carbon. If the way in which this partnership operates proves to be widespread, ideas about nutrient cycling and food-web dynamics in temperate forests may have to be modified.

Diversity of Arbuscular Mycorrhizal Fungi and Ecosystem Functioning

In this chapter, we review recent literature pertaining to the debate linking biodiversity and ecosystem functioning, highlighting the role of arbuscular mycorrhizae. We suggest that the arbuscular mycorrhizal symbiosis should be a vital component of studies designed to elucidate a mechanistic basis linking biodiversity and terrestrial ecosystem function. Most importantly, it is important to consider the role of the mycorrhizal networks, functional specificity among glomalean fungi, and differential effects on host species, all of which can influence plant community dynamics. Finally, we suggest a new direction for mycorrhizal research that includes developing fundamental ecological theory for this group of fungi. Eventually, such theory will allow researchers to include arbuscular mycorrhizal fungi into community and ecosystem models.

Plant-soil feedbacks and mycorrhizal type influence temperate forest population dynamics

Soil biota and plant diversity Soil biota, including symbionts such as mycorrhizal fungi and nitrogen-fixing bacteria, as well as fungal and bacterial pathogens, affect terrestrial plant diversity and growth patterns (see the Perspective by van der Putten). Teste et al. monitored growth and survival in Australian shrubland plant species paired with soil biota from plants of the same species and from other plants that use different nutrient acquisition strategies. Plant-soil feedbacks appear to drive local plant diversity through interactions between the different types of plants and their associated soil biota. Bennett et al. studied plant-soil feedbacks in soil and seeds from 550 populations of 55 species of North American trees. Feedbacks ranged from positive to negative, depending on the type of mycorrhizal association, and were related to how densely the same species occurred in natural populations. Science, this issue p. 134, p. 173; see also p. 181 A large-scale study of North American trees reveals how different soil-associated fungi can either help or hinder tree growth. Feedback with soil biota is an important determinant of terrestrial plant diversity. However, the factors regulating plant-soil feedback, which varies from positive to negative among plant species, remain uncertain. In a large-scale study involving 55 species and 550 populations of North American trees, the type of mycorrhizal association explained much of the variation in plant-soil feedbacks. In soil collected beneath conspecifics, arbuscular mycorrhizal trees experienced negative feedback, whereas ectomycorrhizal trees displayed positive feedback. Additionally, arbuscular mycorrhizal trees exhibited strong conspecific inhibition at multiple spatial scales, whereas ectomycorrhizal trees exhibited conspecific facilitation locally and less severe conspecific inhibition regionally. These results suggest that mycorrhizal type, through effects on plant-soil feedbacks, could be an important contributor to population regulation and community structure in temperate forests.

Where the wild things are: looking for uncultured Glomeromycota

Our knowledge of Glomeromycotan fungi rests largely on studies of cultured isolates. However, these isolates probably comprise one life-history strategy - ruderal. Consequently, our knowledge of arbuscular mycorrhizal (AM) fungi may be biased towards fungi that occur primarily in disturbed habitats and associate with disturbance-tolerant host plants. We can expect to see a signal for this in DNA-based community surveys: human-impacted habitats and cultivated plants should yield a higher proportion of AM fungal species that have been cultured compared with natural habitats and wild plants. Using the MaarjAM database (a curated open-access database of Glomeromycotan sequences), we performed a meta-analysis on studies that described AM fungal communities from a variety of habitats and host plants. We found a greater proportion of cultured AM fungal taxa in human-impacted habitats. In particular, undisturbed forests and grasslands/savannahs contained significantly fewer cultured taxa than human-impacted sites. We also found that wild plants hosted fewer cultured fungal taxa than cultivated plants. Our data show that natural communities of AM fungi are composed largely of uncultured taxa, and this is particularly pronounced in natural habitats and wild plants. We are better poised to understand the functioning of AM symbioses associated with cultivated plants and human-impacted habitats.

Influence of commercial inoculation with Glomus intraradices on the structure and functioning of an AM fungal community from an agricultural site

The use of commercial arbuscular mycorrhizal (AM) inoculants is growing. However, we know little about how resident AM communities respond to inoculations under different soil management conditions. The objective of this study was to simulate the application of a commercial AM fungal inoculant of Glomus intraradices to soil to determine whether the structure and functioning of that soil’s resident AM community would be affected. The effects of inoculation were investigated over time under disturbed or undisturbed soil conditions. We predicted that the introduction of an infective AM fungus, such as G. intraradices, would have greater consequences in disturbed soil. Using a combination of molecular (terminal restriction length polymorphism analysis based on the large subunit of the rRNA gene) and classical methods (AM fungal root colonization and P nutrition) we found that, contrary to our prediction, adding inoculant to soil containing a resident AM fungal community does not necessarily have an impact on the structure of that community either under disturbed or undisturbed conditions. However, we found evidence of positive effects of inoculation on plant nutrition under disturbed conditions, suggesting that the inoculant interacted, directly or indirectly, with the resident AM fungi. The inoculant significantly improved the P content of the host but only in presence of the resident AM fungal community. In contrast to inoculation, soil disturbance had a significant negative impact on species richness of AM fungi and influenced the AM fungal community composition as well as its functioning. Thus, we conclude that soil disturbance may under certain conditions have greater consequences for the structure of resident AM fungal communities in agricultural soils than commercial AM fungal inoculations with G. intraradices.

Navigating the labyrinth: a guide to sequence‐based, community ecology of arbuscular mycorrhizal fungi

Data generated from next generation sequencing (NGS) will soon comprise the majority of information about arbuscular mycorrhizal fungal (AMF) communities. Although these approaches give deeper insight, analysing NGS data involves decisions that can significantly affect results and conclusions. This is particularly true for AMF community studies, because much remains to be known about their basic biology and genetics. During a workshop in 2013, representatives from seven research groups using NGS for AMF community ecology gathered to discuss common challenges and directions for future research. Our goal was to improve the quality and accessibility of NGS data for the AMF research community. Discussions spanned sampling design, sample preservation, sequencing, bioinformatics and data archiving. With concrete examples we demonstrated how different approaches can significantly alter analysis outcomes. Failure to consider the consequences of these decisions may compound bias introduced at each step along the workflow. The products of these discussions have been summarized in this paper in order to serve as a guide for any researcher undertaking NGS sequencing of AMF communities.