Abstract
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.
Highlights
Deep-sea hydrothermal vents host some of the most diverse microbial communities on Earth (Takai and Nakamura 2011)
Comparison of existing chemolithotrophic microbial communities with the results of thermodynamic modeling Above, we have provided the theoretical basis for relationships between the geological environments of hydrothermal activity, physical and chemical variations in hydrothermal fluids, and the compositional diversity of potentially bioavailable energy for various vent-endemic chemolithotrophic metabolisms estimated using thermodynamic models
Peterson et al (2011) showed that the thio- and H2-trophic endosymbionts hosted by different Bathymodiolus populations living in geographically and geologically distinct hydrothermal systems of the MAR and Pacific had much lower specific H2 consumption activities than the endosymbiotic population from the H2-abundant mid-ocean ridges (MOR)-U hydrothermal system (Logatchev field). These results provide strong evidence that the metabolic activity of chemolithotrophic symbionts is controlled by hydrothermal fluid chemistry and is related to the geological background of the hydrothermal system, as suggested by our model calculations
Summary
Deep-sea hydrothermal vents host some of the most diverse microbial communities on Earth (Takai and Nakamura 2011). Many studies have identified high compositional and functional diversity of chemosynthetic ecosystems in geographically and geologically diverse hydrothermal systems (e.g., in reviews by Huber and Holden 2008; Nakagawa and Takai 2008; Takai et al 2006b) Some of these studies have noted possible relationships between the metabolic abundances and compositions of hydrothermal vent-endemic microbial communities and the chemical characteristics of hydrothermal vent fluids in deep-sea hydrothermal systems (Perner et al 2007, 2010; Reysenbach and Shock 2002; Takai and Horikoshi 1999; Takai et al 2001, 2004a). Takai and Nakamura (2010, 2011) first provided clear evidence of biogeochemical relationships among microbiological community development, the chemical composition of hydrothermal fluids, and the geological environment of deep-sea hydrothermal systems through both thermodynamic calculations of the potential energy yields of various in situ metabolic reactions and observed compositional and functional diversity of chemosynthetic ecosystems in the mixing zones of these habitats. We conducted a more comprehensive evaluation of the relationships among variations in geology, geochemistry, and microbial metabolisms and the diversity of communities in global deep-sea hydrothermal environments, based on compilation of a substantial hydrothermal fluid chemistry data set and microbial communities in the mixing zones of a wide variety of habitats
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