Genome-resolved evidence for functionally redundant communities and novel nitrogen fixers in the deyin-1 hydrothermal...

Deep-sea hydrothermal vents represent unique ecosystems that redefine our understanding of the limits of life. They are widely distributed in deep oceans and typically form along mid-ocean ridges. To date, the hydrothermal systems in the Mid-Atlantic Ridge south of 14°S remain barely explored, limiting our understanding of the microbial community in this distinct ecosystem. The Deyin-1 is a newly discovered hydrothermal field in this area. By applying the metagenomic analysis, we aim at gaining much knowledge of the biodiversity and functional capability of microbial community inhabiting this field.

In the current study, 219 metagenomic assembled genomes (MAGs) were reconstructed, unveiling a diverse and variable community dominated by Bacteroidetes, Nitrospirae, Alpha-, Delta-, and Gammaproteobacteria in the active and inactive chimney samples as well as hydrothermal oxide samples. Most of these major taxa were potentially capable of using reduced sulfur and hydrogen as primary energy sources. Many members within the major taxa exhibited potentials of metabolic plasticity by possessing multiple energy metabolic pathways. Among these samples, different bacteria were found to be the major players of the same metabolic pathways, further supporting the variable and functionally redundant community in situ. In addition, a high proportion of MAGs harbored the genes of carbon fixation and extracellular carbohydrate-active enzymes, suggesting that both heterotrophic and autotrophic strategies could be essential for their survival. Notably, for the first time, the genus Candidatus Magnetobacterium was shown to potentially fix nitrogen, indicating its important role in the nitrogen cycle of inactive chimneys. Moreover, the metabolic plasticity of microbes, diverse and variable community composition, and functional redundancy of microbial communities may represent the adaptation strategies to the geochemically complex and fluctuating environmental conditions in deep-sea hydrothermal fields.

This represents the first assembled-genome-based investigation into the microbial community and metabolism of a hydrothermal field in the Mid-Atlantic Ridge south of 14°S. The findings revealed that a high proportion of microbes could benefit from simultaneous use of heterotrophic and autotrophic strategies in situ. It also presented novel members of potential diazotrophs and highlighted the metabolic plasticity and functional redundancy across deep-sea hydrothermal systems. Video abstract.