Functional Traits Resolve Mechanisms Governing the Assembly and Distribution of Nitrogen-Cycling Microbial Communities in the Global Ocean

• Published in: mBio Vol. 13; no. 2; p. e0383221
• Main Authors: Song, Wen, Liu, Jihua, Qin, Wei, Huang, Jun, Yu, Xiaoli, Xu, Mengzhao, Stahl, David, Jiao, Nianzhi, Zhou, Jizhong, Tu, Qichao
• Format: Journal Article
• Language: English
• Published: United States American Society for Microbiology 26.04.2022; American Society for Microbiology (ASM)
• Subjects: community assembly; diversity patterns; Environmental Microbiology; functional redundancy; functional traits; marine nitrogen cycle; Metagenome; Microbiology; Microbiota; Nitrogen; Nitrogen Cycle; Oceans and Seas; Research Article; stochasticity; diversity patterns; stochasticity; functional redundancy; marine nitrogen cycle; functional traits; community assembly
• ISSN: 2150-7511; 2150-7511
• DOI: 10.1128/mbio.03832-21

Microorganisms drive much of the marine nitrogen (N) cycle, which jointly controls the primary production in the global ocean. However, our understanding of the microbial communities driving the global ocean N cycle remains fragmented. Focusing on "who is doing what, where, and how?", this study draws a clear picture describing the global biogeography of marine N-cycling microbial communities by utilizing the Oceans shotgun metagenomes. The marine N-cycling communities are highly variable taxonomically but relatively even at the functional trait level, showing clear functional redundancy properties. The functional traits and taxonomic groups are shaped by the same set of geo-environmental factors, among which, depth is the major factor impacting marine N-cycling communities, differentiating mesopelagic from epipelagic communities. Latitudinal diversity gradients and distance-decay relationships are observed for taxonomic groups, but rarely or weakly for functional traits. The composition of functional traits is strongly deterministic as revealed by null model analysis, while a higher degree of stochasticity is observed for taxonomic composition. Integrating multiple lines of evidence, in addition to drawing a biogeographic picture of marine N-cycling communities, this study also demonstrated an essential microbial ecological theory-determinism governs the assembly of microbial communities performing essential biogeochemical processes; the environment selects functional traits rather than taxonomic groups; functional redundancy underlies stochastic taxonomic community assembly. A critical question in microbial ecology is how the complex microbial communities are formed in natural ecosystems with the existence of thousands different species, thereby performing essential ecosystem functions and maintaining ecosystem stability. Previous studies disentangling the community assembly mechanisms mainly focus on microbial taxa, ignoring the functional traits they carry. By anchoring microbial functional traits and their carrying taxonomic groups involved in nitrogen cycling processes, this study demonstrated an important mechanism associated with the complex microbial community assembly. Evidence shows that the environment selects functional traits rather than taxonomic groups, and functional redundancy underlies stochastic taxonomic community assembly. This study is expected to provide valuable mechanistic insights into the complex microbial community assembly in both natural and artificial ecosystems.