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ABSTRACT As environments worldwide change at unprecedented rates during the Anthropocene, understanding context dependency—how species interactions vary depending on environmental context—is crucial. Combining comparative genomics across 42 angiosperms with transcriptomics, genome‐wide association mapping and gene duplication origin analyses, we show for the first time that gene family expansions are important to context‐dependent regulation of species interactions. Gene families expanded in mycorrhizal fungi‐associating plants display up to 200% more context‐dependent gene expression and double the genetic variation associated with mycorrhizal benefits to plant fitness. Moreover, we discover these gene family expansions arise primarily from tandem duplications with > 2‐times more tandem duplications genome‐wide, indicating gene family expansions continuously supply genetic variation, allowing fine‐tuning of context dependency in species interactions throughout plant evolution. Taken together, our results spotlight how widespread gene duplications can provide molecular flexibility required for plant–microbial interactions to match changing environmental conditions. 

ABSTRACT Microorganisms underpin numerous ecosystem processes and support biodiversity globally. Yet, we understand surprisingly little about what structures environmental microbiomes, including how to efficiently identify key players. Microbiome network theory predicts that highly connected hubs act as keystones, but this has never been empirically tested in nature. Combining culturing, sequencing, networks and field experiments, we isolated ‘central’ (highly connected, hub taxa), ‘intermediate’ (moderately connected), and ‘peripheral’ (weakly/unconnected) microbes and experimentally evaluated their effects on soil microbiome assembly during early succession in nature. Central early colonisers significantly (1) enhanced biodiversity (35%–40% richer communities), (2) reshaped trajectories of microbiome assembly and (3) increased recruitment of additional influential microbes by > 60%. In contrast, peripheral microbes did not increase diversity and were transient taxa, minimally affected by the presence of other microbes. This work elucidates fundamental principles of network theory in microbial ecology and demonstrates for the first time in nature that central microbes act as keystone taxa. 

Abstract As ecosystems face unprecedented change and habitat loss, pursuing comprehensive and resilient habitat restoration will be integral to protecting and maintaining natural areas and the services they provide. Microbiomes offer an important avenue for improving restoration efforts as they are integral to ecosystem health and functioning. Despite microbiomes' importance, unresolved knowledge gaps hinder their inclusion in restoration efforts. Here, we address two critical gaps in understanding microbial roles in restoration—fungal microbiomes' importance in “reconstructive” restoration efforts and how management and restoration decisions interactively impact fungal communities and their cascading effects on trees. We combined field surveys, microbiome sequencing, and greenhouse experiments to determine how reconstructing an iconic landscape feature—tree islands—in the highly imperiled Everglades impacts fungal microbiomes and fungal effects on native tree species compared with their natural counterparts under different proposed hydrological management regimes. Constructed islands used in this research were built from peat soil and limestone collected from deep sloughs and levees nearby the restoration sites in 2003, providing 18 years for microbiome assembly on constructed islands. We found that while fungal microbiomes from natural and constructed tree islands exhibited similar diversity and richness, they differed significantly in community composition. These compositional differences arose mainly from changes to which fungal taxa were present on the islands rather than changes in relative abundances. Surprisingly, ~50% of fungal hub taxa (putative keystone fungi) from natural islands were missing on constructed islands, suggesting that differences in community composition of constructed island could be important for microbiome stability and function. The differences in fungal composition between natural and constructed islands had important consequences for tree growth. Specifically, these compositional differences interacted with hydrological regime (treatments simulating management strategies) to affect woody growth across the four tree species in our experiment. Taken together, our results demonstrate that reconstructing a landscape feature without consideration of microbiomes can result in diverging fungal communities that are likely to interact with management decisions leading to meaningful consequences for foundational primary producers. Our results recommend cooperation between restoration practitioners and ecologists to evaluate opportunities for active management and restoration of microbiomes during future reconstructive restoration. 

ABSTRACT Fungi play many essential roles in ecosystems. They facilitate plant access to nutrients and water, serve as decay agents that cycle carbon and nutrients through the soil, water and atmosphere, and are major regulators of macro‐organismal populations. Although technological advances are improving the detection and identification of fungi, there still exist key gaps in our ecological knowledge of this kingdom, especially related to function.Trait‐based approaches have been instrumental in strengthening our understanding of plant functional ecology and, as such, provide excellent models for deepening our understanding of fungal functional ecology in ways that complement insights gained from traditional and ‐omics‐based techniques. In this review, we synthesize current knowledge of fungal functional ecology, taxonomy and systematics and introduce a novel database of fungal functional traits (Fun^Fun). Fun^Funis built to interface with other databases to explore and predict how fungal functional diversity varies by taxonomy, guild, and other evolutionary or ecological grouping variables. To highlight how a quantitative trait‐based approach can provide new insights, we describe multiple targeted examples and end by suggesting next steps in the rapidly growing field of fungal functional ecology.