Genome-resolved metagenomics reveals that sulfur metabolism dominates the microbial ecology of rising hydrothermal plumes

Abstract:

Deep-sea hydrothermal plumes occur when hot fluids from hydrothermal vents replete with chemically reduced elements and compounds like sulfide, methane, hydrogen, ammonia, iron and manganese mix with cold, oxic seawater. Chemosynthetic microbes use these reduced chemicals to power primary production and are pervasive throughout the deep sea, even at sites far removed from hydrothermal vents.

Although neutrally-buoyant hydrothermal plumes have been well-studied, rising hydrothermal plumes have received little attention even though they represent an important interface in the deep-sea where microbial metabolism and particle formation processes control the transformation of important elements and impact global biogeochemical cycles.

In this study, we used genome-resolved metagenomic analyses and thermodynamic-bioenergetic modeling to study the microbial ecology of rising hydrothermal plumes at five different hydrothermal vents spanning a range of geochemical gradients at the Eastern Lau Spreading Center (ELSC) in the Western Pacific Ocean. Our analyses show that differences in the geochemistry of hydrothermal vents do not manifest in microbial diversity and community composition, both of which display only minor variance across ELSC hydrothermal plumes. Microbial metabolism is dominated by oxidation of reduced sulfur species and supports a diversity of bacteria, archaea and viruses that provide intriguing insights into metabolic plasticity and virus-mediated horizontal gene transfer in the microbial community. The manifestation of sulfur oxidation genes in hydrogen and methane oxidizing organisms hints at metabolic opportunism in deep-sea microbes that would enable them to respond to varying redox conditions in hydrothermal plumes. Finally, we infer that the abundance, diversity and metabolic versatility of microbes associated with sulfur oxidation impart functional redundancy that could allow it to persist in the dynamic settings of hydrothermal plumes.