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Redox traits characterize the organization of global microbial communities

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Significance Biological communities are conventionally described as assemblages of species, whose ecological roles are known or predictable from their observable morphology. In microbial ecology, such a taxonomic approach is hindered… Click to show full abstract

Significance Biological communities are conventionally described as assemblages of species, whose ecological roles are known or predictable from their observable morphology. In microbial ecology, such a taxonomic approach is hindered by limited capacity to discriminate among different microbes, which bear highly dynamic genomes and establish complex associations. Approaches based on culture-independent functional genes profiling might overcome these problems, but a set of usable established genes in a general situation is still lacking. We show that genes related to reduction-oxidation (redox) processes separate microbial communities into their corresponding biomes. This redox-based characterization is linked to the microbial energetics of ecosystems and to most biogeochemical cycles and might be useful for assessing the impact of environmental degradation on the ecosystem services, underpinned by microorganisms. The structure of biological communities is conventionally described as profiles of taxonomic units, whose ecological functions are assumed to be known or, at least, predictable. In environmental microbiology, however, the functions of a majority of microorganisms are unknown and expected to be highly dynamic and collectively redundant, obscuring the link between taxonomic structure and ecosystem functioning. Although genetic trait-based approaches at the community level might overcome this problem, no obvious choice of gene categories can be identified as appropriate descriptive units in a general ecological context. We used 247 microbial metagenomes from 18 biomes to determine which set of genes better characterizes the differences among biomes on the global scale. We show that profiles of oxidoreductase genes support the highest biome differentiation compared with profiles of other categories of enzymes, general protein-coding genes, transporter genes, and taxonomic gene markers. Based on oxidoreductases’ description of microbial communities, the role of energetics in differentiation and particular ecosystem function of different biomes become readily apparent. We also show that taxonomic diversity is decoupled from functional diversity, e.g., grasslands and rhizospheres were the most diverse biomes in oxidoreductases but not in taxonomy. Considering that microbes underpin biogeochemical processes and nutrient recycling through oxidoreductases, this functional diversity should be relevant for a better understanding of the stability and conservation of biomes. Consequently, this approach might help to quantify the impact of environmental stressors on microbial ecosystems in the context of the global-scale biome crisis that our planet currently faces.

Keywords: redox traits; traits characterize; organization global; characterize organization; global microbial; microbial communities

Journal Title: Proceedings of the National Academy of Sciences of the United States of America
Year Published: 2019

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