Redox traits characterize the organization of global microbial communities

Abstract

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.