Theoretical constraints of physical and chemical properties of hydrothermal fluids on variations in chemolithotrophic microbial communities in seafloor hydrothermal systems

In the past few decades, chemosynthetic ecosystems at deep-sea hydrothermal vents have received attention as plausible analogues to the early ecosystems of Earth, as well as to extraterrestrial ecosystems. These ecosystems are sustained by chemical energy obtained from inorganic redox substances (e.g., H2S, CO2, H2, CH4, and O2) in hydrothermal fluids and ambient seawater. The chemical and isotope compositions of the hydrothermal fluid are, in turn, controlled by subseafloor physical and chemical processes, including fluid–rock interactions, phase separation and partitioning of fluids, and precipitation of minerals. We hypothesized that specific physicochemical principles describe the linkages among the living ecosystems, hydrothermal fluids, and geological background in deep-sea hydrothermal systems. We estimated the metabolic energy potentially available for productivity by chemolithotrophic microorganisms at various hydrothermal vent fields. We used a geochemical model based on hydrothermal fluid chemistry data compiled from 89 globally distributed hydrothermal vent sites. The model estimates were compared to the observed variability in extant microbial communities in seafloor hydrothermal environments. Our calculations clearly show that representative chemolithotrophic metabolisms (e.g., thiotrophic, hydrogenotrophic, and methanotrophic) respond differently to geological and geochemical variations in the hydrothermal systems. Nearly all of the deep-sea hydrothermal systems provide abundant energy for organisms with aerobic thiotrophic metabolisms; observed variations in the H2S concentrations among the hydrothermal fluids had little effect on the energetics of thiotrophic metabolism. Thus, these organisms form the base of the chemosynthetic microbial community in global deep-sea hydrothermal environments. In contrast, variations in H2 concentrations in hydrothermal fluids significantly impact organisms with aerobic and anaerobic hydrogenotrophic metabolisms. Particularly in H2-rich ultramafic rock-hosted hydrothermal systems, anaerobic and aerobic hydrogenotrophy is more energetically significant than thiotrophy. The CH4 concentration also has a considerable impact on organisms with aerobic and anaerobic methanotrophic metabolisms, particularly in sediment-associated hydrothermal systems. Recently clarified patterns and functions of existing microbial communities and their metabolisms are generally consistent with the results of our thermodynamic modeling of the hydrothermal mixing zones. These relationships provide important directions for future research addressing the origin and early evolution of life on Earth as well as for the search for extraterrestrial life.