Pierre-Luc Chagnon

A trait-based framework to understand life history of mycorrhizal fungi

Despite the growing appreciation for the functional diversity of arbuscular mycorrhizal (AM) fungi, our understanding of the causes and consequences of this diversity is still poor. In this opinion article, we review published data on AM fungal functional traits and attempt to identify major axes of life history variation. We propose that a life history classification system based on the grouping of functional traits, such as Grimes C-S-R (competitor, stress tolerator, ruderal) framework, can help to explain life history diversification in AM fungi, successional dynamics, and the spatial structure of AM fungal assemblages. Using a common life history classification framework for both plants and AM fungi could also help in predicting probable species associations in natural communities and increase our fundamental understanding of the interaction between land plants and AM fungi.

Using ecological network theory to evaluate the causes and consequences of arbuscular mycorrhizal community structure

Arbuscular mycorrhizal fungi (AMF) are widespread and their symbiotic interactions involve the majority of terrestrial plant species (Wang & Qiu, 2006). These obligate biotrophs generally improve the nutrition and vigor of the host, thereby affecting individual plant traits (van der Heijden et al., 1998) as well as the composition and functioning of entire plant communities (Moora & Zobel, 1996; Hartnett & Wilson, 1999; Bever, 2002). Studies on individual plant traits are useful in determining fitness benefits to the plant (e.g. increased growth, resistance to pathogens, etc.), whereas studies on community-level interactions can potentially explain constraints on host–symbiont web architecture (e.g. Bluthgen et al., 2007). Community-level studies have been limited, however, to small subsets of natural plant communities, because processing and identifying AMF species associated with numerous plant root systems have proven costly and painstaking. Recent advances in next-generation sequencing technologies (Margulies et al., 2005) have removed this hurdle and improved the detection of rare AMF species (Opik et al., 2009). This increased capacity in describing whole plant–AMF networks provides an opportunity to identify the causes, and assess the functional consequences, of symbiotic network architectures (i.e. topology). Network theory, originally developed to describe the flow of information within computational and social networks (Emerson, 1972), has more recently been applied to ecological studies of various mutualistic systems (Jordano et al., 2003; Olesen et al., 2007; Joppa et al., 2010). The major advantage of an ecological network approach is that topological metrics can be quantified for any given network involving two or more groups of interacting organisms (e.g. plants and pollinators, food webs, etc.). For example, ecological networks may be described in terms of their ‘nestedness’. High nestedness occurs when specialist species interact with a subset of partners with which generalist species also interact. For example, a specialist pollinator would tend to specialize on a generalist plant, and vice versa (Fig. 1a). This absence of reciprocal specialization was shown to be a pervasive feature of pollination networks (Bascompte et al., 2003; Joppa et al., 2009, 2010) that potentially favors diversity and stability of ecological communities (Memmott et al., 2004; Burgos et al., 2007; Bastolla et al., 2009; Thébault & Fontaine, 2010). Ecological networks can also be described according to their ‘modularity’, that is, the tendency of species to be grouped into modules in which interactions are more frequent than with the rest of the community (Fig. 1b). Thompson (2005) suggested that communities may assemble into distinct modules based on the functional complementarity of their traits, and this may offer some insight into coevolutionary dynamics between symbiotic species (Guimarães et al., 2007). In this Letter, we argue that an ecological network approach could provide a framework by which to characterize and compare plant–AMF communities from different environments or at different successional stages. This, in turn, could improve our understanding of mechanisms structuring mycorrhizal communities and bring mycorrhizal science to a more predictive level (Johnson et al., 2006). In a recent study, Opik et al. (2009) used pyrosequencing to describe AMF communities associated with 10 plant species in a forest understory community. Here, we have used their published data set to demonstrate the applicability of ecological network theory to characterize plant–AMF communities. Our exercise revealed that this particular plant–AMF network was both highly nested and modular. We discuss possible reasons and implications for such topological features, Forum

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.

Interaction type influences ecological network structure more than local abiotic conditions: evidence from endophytic and endolichenic fungi at a continental scale

Understanding the factors that shape community assembly remains one of the most enduring and important questions in modern ecology. Network theory can reveal rules of community assembly within and across study systems and suggest novel hypotheses regarding the formation and stability of communities. However, such studies generally face the challenge of disentangling the relative influence of factors such as interaction type and environmental conditions on shaping communities and associated networks. Endophytic and endolichenic symbioses, characterized by microbial species that occur within healthy plants and lichen thalli, represent some of the most ubiquitous interactions in nature. Fungi that engage in these symbioses are hyperdiverse, often horizontally transmitted, and functionally beneficial in many cases, and they represent the diversification of multiple phylogenetic groups. We evaluated six measures of ecological network structure for >4100 isolates of endophytic and endolichenic fungi collected systematically from five sites across North America. Our comparison of these co-occurring interactions in biomes ranging from tundra to subtropical forest showed that the type of interactions (i.e., endophytic vs. endolichenic) had a much more pronounced influence on network structure than did environmental conditions. In particular, endophytic networks were less nested, less connected, and more modular than endolichenic networks in all sites. The consistency of the network structure within each interaction type, independent of site, is encouraging for current efforts devoted to gathering metadata on ecological network structure at a global scale. We discuss several mechanisms potentially responsible for such patterns and draw attention to knowledge gaps in our understanding of networks for diverse interaction types.

Ecological and evolutionary implications of hyphal anastomosis in arbuscular mycorrhizal fungi

Arbuscular mycorrhizal (AM) fungi are important plant symbionts widespread worldwide. Like other fungi, they have the ability to perform hyphal anastomosis, that is, the fusion of encountering vegetative hyphae. Research in other fungal phyla has evidenced numerous potential functional and evolutionary consequences of anastomosis. Yet, in AM fungal research, anastomosis has almost strictly been discussed in the context of fungal response to disturbance and interindividual genetic exchange. Here, I review more broadly the implications of anastomosis for AM fungal ecology and evolution. I also identify major knowledge gaps and research prospects to better ground hyphal anastomosis strategies of AM fungi in their general life-history strategies.

Using molecular biology to study mycorrhizal fungal community ecology: Limits and perspectives

Molecular tools have progressively replaced morphological approaches to characterize microbial communities in nature. Arbuscular mycorrhizal (AM) fungi are no exception to this rule. Yet, one challenge posed by these symbionts is that they colonize simultaneously both plant roots and soil, which complicates their detection and quantification. In most studies conducted to date, AM fungal communities have been characterized from roots only, soil only or spores only. Here, we discuss the pitfalls associated to drawing ecological inferences using such datasets. We also conclude by arguing that molecular biology will contribute most to advance knowledge in AM fungal ecology if it is integrated into broader perspectives taking into account the natural history of these organisms. This calls for a better merging of molecular and morphological approaches, and the establishment of intensive, long-term research programs.

Is root DNA a reliable proxy to assess arbuscular mycorrhizal community structure

Arbuscular mycorrhizal (AM) fungi are widespread plant symbionts that extensively colonize both soil and roots. Given their influence on ecosystem processes, such as plant growth, soil carbon storage, and nutrient cycling, there is great interest in understanding the drivers of their community structure. AM fungal communities are increasingly characterized by selectively amplifying their DNA from plant roots, thus assuming that AM fungal community structure within roots provides a reliable portrait of the total (i.e., soil + roots) community. Through numerical simulations, we test this assumption using published data. We show that community structure and diversity is well preserved when analyzing only a subset of the community biomass (i.e., roots or soil), provided that the community shows a typical skewed abundance distribution, with few very dominant species and a high prevalence of rare species. Given that this community structure has been shown to be common in natural AM fungal communities, the present work would suggest that characterizing AM fungal communities using only roots or soil can provide a reliable portrait of the overall community. However, we show through additional analyses that the proportion of sample biomass used for molecular methods must be over a minimal threshold to properly characterize the community. Using published molecular data sets, we validate those results, which suggest that typical molecular protocols using low amounts of biomass may strongly influence AM fungal community characterization. Finally, we also discuss other assumptions implied by the molecular analysis of AM fungal communities, and point out urgent knowledge gaps.

Soil biotic quality lacks spatial structure and is positively associated with fertility in a northern grassland

When placing roots in the soil, plants integrate information about soil nutrients, plant neighbours and beneficial/detrimental soil organisms. While the fine-scale spatial heterogeneity in soil nutrients and plant neighbours have been described previously, virtually nothing is known about the spatial structure in soil biotic quality (measured here as a soil Biota-Induced plant Growth Response, or BIGR), or its correlation with nutrients or neighbours. Such correlations could imply trade-offs in root placement decisions. Theory would predict that soil BIGR is (1) negatively related to soil fertility and (2) associated with plant community structure, such that plants influence soil biota (and vice versa) through plant–soil feedbacks. We would also expect that since plants have species-specific impacts on soil organisms, spatially homogeneous plant communities should also homogenize soil BIGR. Here, we test these hypotheses in a semi-arid grassland by (1) characterizing the spatial structure of soil BIGR at a scale experienced by an individual plant and (2) correlating it to soil abiotic properties and plant community structure. We do so in two types of plant communities: (1) low-diversity patches dominated by an invasive grass (Bromus inermis Leyss.) and (2) patches covered mostly by native vegetation, with the expectation that dominance by Bromus would homogenize soil BIGR. Soil BIGR was spatially heterogeneous, but not autocorrelated. This was true in both vegetation types (Bromus-invaded vs. native patches). Conversely, soil abiotic properties and plant community structure were frequently spatially autocorrelated at similar scales. Also, contrary to many studies, we found a positive correlation between soil BIGR and soil fertility. Soil BIGR was also associated with plant community structure. Synthesis. The positive correlation between soil BIGR and some soil nutrient levels suggests that plants do not necessarily trade-off between foraging for nutrients vs. biotic interactions: nutritional cues could rather indicate the presence of beneficial soil biota. Moreover, the spatial structure in plant communities, coupled with their correlation with soil BIGR, jointly suggest that plant–soil feedbacks operate at local scales in the field: this has been identified in modelling studies as an important driver of plant coexistence.