Abstract

Studies of the ecological and evolutionary relationships between plants and their associated microbes have long been focused on single microbes, or single microbial guilds, but in reality, plants associate with a diverse array of microbes from a varied set of guilds. As such, multitrophic interactions among plant-associated microbes from multiple guilds represent an area of developing research, and can reveal how complex microbial communities are structured around plants. Interactions between coniferous plants and their associated microbes provide a good model system for such studies, as conifers host a suite of microorganisms including mutualistic ectomycorrhizal (ECM) fungi and foliar bacterial endophytes. To investigate the potential role ECM fungi play in structuring foliar bacterial endophyte communities, we sampled three isolated, native populations of Monterey pine (Pinus radiata), and used constrained analysis of principal coordinates to relate the community matrices of the ECM fungi and bacterial endophytes. Our results suggest that ECM fungi may be important factors for explaining variation in bacterial endophyte communities but this effect is influenced by population and environmental characteristics, emphasizing the potential importance of other factors — biotic or abiotic — in determining the composition of bacterial communities. We also classified ECM fungi into categories based on known fungal traits associated with substrate exploration and nutrient mobilization strategies since variation in these traits allows the fungi to acquire nutrients across a wide range of abiotic conditions and may influence the outcome of multi-species interactions. Across populations and environmental factors, none of the traits associated with fungal foraging strategy types significantly structured bacterial assemblages, suggesting these ECM fungal traits are not important for understanding endophyte-ECM interactions. Overall, our results suggest that both biotic species interactions and environmental filtering are important for structuring microbial communities but emphasize the need for more research into these interactions.

Highlights

  • All plants associate with a diverse array of microorganisms throughout their tissues, but microbes associated with above- and belowground portions of plants are typically studied separately

  • We investigate the extent to which the belowground ECM fungal community of a conifer is associated with its aboveground foliar bacterial endophyte communities, and whether host population and environmental characteristics alter this relationship

  • When % silt and % sand were combined into a single metric, correlations of operational taxonomic units (OTUs) with environmental characteristics changed marginally

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Summary

Introduction

All plants associate with a diverse array of microorganisms throughout their tissues, but microbes associated with above- and belowground portions of plants are typically studied separately. The degree to which non-wild and wild systems are comparable for plant–microbe interactions remains unclear as there are major differences in both phylogenetic diversity and species composition of plant hosts between agroecosystems and the associated forest regions (Griffin and Carson, 2015) Coniferous plants and their associated microbes provide a good model system for exploring the interaction of above- and belowground plant-associated microbes as conifers interact with a suite of microorganisms including mutualistic mycorrhizal fungi (Smith and Read, 2008), pathogenic eukaryotic microbes (Fogel, 1988), and foliar bacterial and fungal endophytes (Carroll, 1988; Pirttilä et al, 2005; Arnold et al, 2007; Carrell and Frank, 2014, 2015; Oono et al, 2014). The relationships between conifers and their microbes may be important since conifers grow in impoverished acidic soils at both mid and high latitudes, potentially facilitated by their relationship with various microbes (Axelrod, 1986; Lepage et al, 1997; Richardson, 2000; Carrell and Frank, 2014)

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