Salinity Drives Functional and Taxonomic Diversities in Global Water Metagenomes

A tight association between microbial function and taxonomy is the basis of functional prediction based on taxonomy, but such associations have been controversial in water biomes largely due to the probable prevalence of functional redundancy. However, previous studies on this topic used a relatively coarse resolution of ecosystem functioning, potentially inflating the estimated functional redundancy. Thus, a comprehensive evaluation of the association between high-resolution functional traits and taxonomic diversity obtained from fresh and saline water metagenomic data is urgently needed. Here, we examined 938 functionally and taxonomically annotated water metagenomes obtained worldwide to scrutinize the connection between function and taxonomy, and to identify the key driver of water metagenomes function or taxonomic composition at a global scale. We found that pairwise similarity of function was significantly associated with taxonomy, though taxonomy had higher global dissimilarity than function. Classification into six water biomes resulted in greater variation in taxonomic compositions than functional profiles, as the key regulating factor was salinity. Fresh water microbes harbored distinct functional and taxonomic structures from microbes in saline water biomes, despite that taxonomy was more susceptible to gradient of geography and climate than function. In summary, our results find a significant relationship between taxonomic diversity and microbial functioning in global water metagenomes, although microbial taxonomic compositions vary to a larger extent than functional profiles in aquatic ecosystems, suggesting the possibility and necessity for functional prediction of microorganisms based on taxonomy in global aquatic ecosystems.