Evolutionary ecology of natural comammox Nitrospira populations

Abstract

Microbes commonly exists in diverse and complex communities where species interact, and their genomic repertoires evolve over time. Our understanding of species interactions and evolution has increased in the last decades, but most studies of evolutionary dynamics are based on single species in isolation or in experimental systems composed of few interacting species. Here, we use the microbial ecosystem found in groundwater-fed sand filters as a model to avoid this limitation. In these open systems, diverse microbial communities experience relatively stable conditions, and the coupling between chemical and biological processes is generally well defined. Metagenomic analysis of 12 sand filters revealed systematic co-occurrence of at least five comammox Nitrospira species, likely promoted by low ammonium concentrations. These Nitrospira species showed intra-population sequence diversity, although possible clonal expansion was detected in few abundant local comammox populations. They showed low homologous recombination and strong purifying selection, the latter process being especially strong in genes essential in energy metabolism. Positive selection was detected on genes related to resistance to foreign DNA and phages. We found that, compared to other habitats, groundwater-fed sand filters impose strong purifying selection and low recombination on comammox Nitrospira populations. These results suggest that evolutionary processes are more affected by habitat type than by species identity. Together, this study improves our understanding of species interactions and evolution in complex microbial communities, and sheds light on the environmental dependency of evolutionary processes.