The diversity and ecological significance of microbial traits potentially involved in B12 biosynthesis in the global ocean

Jiayin Zhou; Wei Qin; Xinda Lu; Yunfeng Yang; David Stahl; Nianzhi Jiao; Jizhong Zhou; Jihua Liu; Qichao Tu

doi:10.1002/mlf2.12095

The diversity and ecological significance of microbial traits potentially involved in B₁₂ biosynthesis in the global ocean

mLife. 2023 Dec 26;2(4):416-427. doi: 10.1002/mlf2.12095. eCollection 2023 Dec.

Authors

Jiayin Zhou^{1

2}, Wei Qin³, Xinda Lu^{4

5}, Yunfeng Yang⁶, David Stahl⁷, Nianzhi Jiao^{1

8}, Jizhong Zhou^{3

9

10

11

12}, Jihua Liu^{1

2}, Qichao Tu^{1

2}

Affiliations

¹ Institute of Marine Science and Technology Shandong University Qingdao China.
² Joint Lab for Ocean Research and Education at Dalhousie University Shandong University and Xiamen University Qingdao China.
³ School of Biological Sciences University of Oklahoma Norman Oklahoma USA.
⁴ Department of Civil and Environmental Engineering Massachusetts Institute of Technology Cambridge Massachusetts USA.
⁵ Present address: DermBiont Inc. Boston Massachusetts USA.
⁶ State Key Joint Laboratory of Environment Simulation and Pollution Control, School of Environment Tsinghua University Beijing China.
⁷ Department of Civil and Environmental Engineering University of Washington Seattle Washington USA.
⁸ Institute of Marine Microbes and Ecospheres Xiamen University Xiamen China.
⁹ Earth and Environmental Sciences, Lawrence Berkeley National Laboratory Berkeley California USA.
¹⁰ Institute for Environmental Genomics, University of Oklahoma Norman Oklahoma USA.
¹¹ School of Civil Engineering and Environmental Sciences, University of Oklahoma Norman Oklahoma USA.
¹² School of Computer Sciences, University of Oklahoma Norman Oklahoma USA.

Abstract

Cobalamin (B₁₂), an essential nutrient and growth cofactor for many living organisms on Earth, can be fully synthesized only by selected prokaryotes in nature. Therefore, microbial communities related to B₁₂ biosynthesis could serve as an example subsystem to disentangle the underlying ecological mechanisms balancing the function and taxonomic make-up of complex functional assemblages. By anchoring microbial traits potentially involved in B₁₂ biosynthesis, we depict the biogeographic patterns of B₁₂ biosynthesis genes and the taxa harboring them in the global ocean, despite the limitations of detecting de novo B₁₂ synthesizers via metagenomes alone. Both the taxonomic and functional composition of B₁₂ biosynthesis genes were strongly shaped by depth, differentiating the epipelagic zones from the mesopelagic layers. Functional genes related to B₁₂ biosynthesis were relatively stably distributed across different oceans, but the taxa harboring them varied considerably, showing clear functional redundancy among microbial systems. Microbial taxa carrying B₁₂ biosynthesis genes in the surface water were influenced by environmental factors such as temperature, oxygen, and nitrate. However, the composition of functional genes was only weakly associated with these environmental factors. Null model analyses demonstrated that determinism governed the variations in B₁₂ biosynthesis genes, whereas a higher degree of stochasticity was associated with taxonomic variations. Significant associations were observed between the chlorophyll a concentration and B₁₂ biosynthesis, confirming its importance in primary production in the global ocean. The results of this study reveal an essential ecological mechanism governing the assembly of microbes in nature: the environment selects for function rather than taxonomy; functional redundancy underlies stochastic community assembly.

Keywords: B12 biosynthesis; community assembly; functional genes; functional redundancy; ocean primary production.