Microbiome functioning depends on individual and interactive effects of the environment and community structure

Abstract

How ecosystem functioning changes with microbial communities remains an open question in natural ecosystems. Both present-day environmental conditions and historical events, such as past differences in dispersal, can have a greater influence over ecosystem function than the diversity or abundance of both taxa and genes. Here, we estimated how individual and interactive effects of microbial community structure defined by diversity and abundance, present-day environmental conditions, and an indicator of historical legacies influenced ecosystem functioning in lake sediments. We studied sediments because they have strong gradients in all three of these ecosystem properties and deliver important functions worldwide. By characterizing bacterial community composition and functional traits at eight sites fed by discrete and contrasting catchments, we found that taxonomic diversity and the normalized abundance of oxidase-encoding genes explained as much variation in CO production as present-day gradients of pH and organic matter quantity and quality. Functional gene diversity was not linked to CO production rates. Surprisingly, the effects of taxonomic diversity and normalized oxidase abundance in the model predicting CO production were attributable to site-level differences in bacterial communities unrelated to the present-day environment, suggesting that colonization history rather than habitat-based filtering indirectly influenced ecosystem functioning. Our findings add to limited evidence that biodiversity and gene abundance explain patterns of microbiome functioning in nature. Yet we highlight among the first time how these relationships depend directly on present-day environmental conditions and indirectly on historical legacies, and so need to be contextualized with these other ecosystem properties.

Microbial assembly, interaction, functioning, activity and diversification: a review derived from community compositional data

“…Environmental conditions determine the availability of electronic donors/acceptors to microbes and shape the process of biogeochemical reactions. In addition to the environment, stochastic processes may also affect diversity and influence ecosystem functioning (Orland et al 2018;Zhou et al 2013). Overall, the positive DEF relationship in microorganisms is supportive of phylogenetic conservation in functional traits.…”

“…The microbial DEF relationship can be confounded by environmental variations, as environmental factors can exert influences on both diversity and ecosystem functioning. Orland et al (2018) demonstrated that pH and organic matter quantity and quality explained as much variation in CO 2 production as did taxonomic diversity in lake sediments; these environmental factors exerted direct influences on ecosystem functioning due to their unrelatedness to taxonomic diversity. Comparatively, Delgado-Baquerizo et al (2016b) found in a global set of soil samples that the DEF relationship was maintained when accounting for edaphic factors, which suggests that taxonomic diversity can exert influences on ecosystem functioning independently of environmental variabilities.…”

Chemical and microbial diversity covary in fresh water to influence ecosystem functioning

“…carbon cycling | chemical diversity | microbial diversity | fresh waters A handful of fresh water contains thousands of dissolved organic molecules of varying origin and composition (1,2), but the biological significance of this chemodiversity remains largely unknown. Chemodiversity should have broad consequences for biogeochemical cycles (1), because variation in the composition of dissolved organic molecules influences the diversity, structure, and functioning of microbial communities (3)(4)(5)(6). Microbial consortia also produce chemodiversity by degrading larger molecules into smaller structures and releasing new molecules into the environment, such as for communication and defense (7).…”

“…Chemodiversity should ultimately relate to microbial and ecosystem functioning because greater biodiversity often promotes ecosystem functioning (6,(18)(19)(20). Biodiversity can explain increasingly more variation in ecosystem functioning where microbial functions are phylogenetically dispersed and facultative, as it will more closely reflect the diversity of traits present in communities (21).…”

Aquatic microbial community is partially functionally redundant: insights from an in situ reciprocal transplant experiment

“…In recent years, the focus of microbial ecology studies has shifted from understanding the community diversity to understanding what microbes are doing and how they respond to changes in the environment, and delineating community function relationships in diverse ecosystems (Tringe SG et al, 2005; Louca S et al, 2016; Mooshammer M et al, 2017; Louca S et al, 2018; Galand PE et al, 2018; Orland C et al, 2019) . With advancements in sequencing technology and relative improvements in metagenomic analyses, efforts have been made to establish community function relationships in pristine and disturbed ecosystems.…”