Species’ functional traits and interactions drive nitrate-mediated sulfur-oxidizing community structure and functioning

ABSTRACT Understanding processes and mechanisms governing microbial community structure and function is a central goal in microbial ecology. Previous studies disentangling the community assembly mechanisms were mainly based on taxonomic diversity but were rarely combined with species’ functional traits and interactions. Here, we showed how species’ functional traits and interactions determined microbial community structure and functions by a well-controlled laboratory experiment with nitrate-mediated sulfur oxidation systems using both culture-independent and culture-dependent technologies. The results showed that species were different in functional traits of nitrate-mediated sulfide and thiosulfate oxidation, which determined their relative abundance in the nitrate-mediated sulfur oxidation systems. Those thiosulfate-oxidizing microbes co-occurred with Thiobacillus by using intermediates (e.g., thiosulfate) secreted by Thiobacillus during sulfide oxidation process. Such metabolic dependencies exerted great effects on community functions. Metabolic dependencies between Thiobacillus and genera that oxidized thiosulfate to more sulfate (e.g., Ciceribacter) sustained high and stable oxidation activities of sulfide to sulfate. In contrast, metabolic dependencies between Thiobacillus and genera that oxidized thiosulfate to tetrathionate (e.g., Pseudoxanthomonas) slowed down the production of sulfate, indicating changes in the metabolic flow. In addition, competitions among species were mostly detrimental to the stability of community function. These results revealed that species’ functional traits and interactions were the intrinsic factors determining community structure and functions. This study advances our understanding of microbial community assembly and functions of the nitrate-mediated sulfur oxidation process from the perspectives of species’ functional traits and interactions and has important implications for designing and constructing microbiomes with expected functions. Importance Understanding the processes and mechanisms governing microbial community assembly and their linkages to ecosystem functioning has long been a core issue in microbial ecology. An in-depth insight still requires combining with analyses of species’ functional traits and microbial interactions. Our study showed how species’ functional traits and interactions determined microbial community structure and functions by a well-controlled laboratory experiment with nitrate-mediated sulfur oxidation systems using high-throughput sequencing and culture-dependent technologies. The results provided solid evidences that species’ functional traits and interactions were the intrinsic factors determining community structure and function. More importantly, our study established quantitative links between community structure and function based on species’ functional traits and interactions, which would have important implications for the design and synthesis of microbiomes with expected functions. Understanding the processes and mechanisms governing microbial community assembly and their linkages to ecosystem functioning has long been a core issue in microbial ecology. An in-depth insight still requires combining with analyses of species’ functional traits and microbial interactions. Our study showed how species’ functional traits and interactions determined microbial community structure and functions by a well-controlled laboratory experiment with nitrate-mediated sulfur oxidation systems using high-throughput sequencing and culture-dependent technologies. The results provided solid evidences that species’ functional traits and interactions were the intrinsic factors determining community structure and function. More importantly, our study established quantitative links between community structure and function based on species’ functional traits and interactions, which would have important implications for the design and synthesis of microbiomes with expected functions.