Iron-Based Microbial Ecosystem on and Below the Seafloor: A Case Study of Hydrothermal Fields of the Southern Mariana Trough

Abstract

Microbial community structures in deep-sea hydrothermal vents fields are constrained by available energy yields provided by inorganic redox reactions, which are in turn controlled by chemical composition of hydrothermal fluids. In the past two decades, geochemical and microbiological studies have been conducted in deep-sea hydrothermal vents at three geographically different areas of the Southern Mariana Trough (SMT). A variety of geochemical data of hydrothermal fluids and an unparalleled microbiological dataset of various samples (i.e., sulfide structures of active vents, iron-rich mats, borehole fluids, and ambient seawater) are available for comparative analyses. Here, we summarize the geochemical and microbiological characteristics in the SMT and assess the relationship between the microbial community structures and the fluid geochemistry in the SMT by thermodynamic modeling. In the high temperature vent fluids, aerobic sulfide-oxidation has the potential to yield large amounts of bioavailable energy in the vent fluids, which is consistent with the detection of species related to sulfide-oxidizing bacteria (such as Thiomicrospira in the Gammaproteobacteria and Sulfurimonas in the Epsilonproteobacteria). Conversely, the bioavailable energy yield from aerobic iron-oxidation reactions in the low-temperature fluids collected from man-made boreholes and several natural vents were comparable to or higher than those from sulfide-oxidation. This is also consistent with the detection of species related to iron-oxidizing bacteria (Mariprofundus in the Zetaproteobacteria) in such low-temperature samples. The results of combination of microbiological, geochemical, and thermodynamic analyses in the SMT provide novel insights into the presence and significance of iron-based microbial ecosystems in deep-sea hydrothermal fields.

Intra-Field Variation of Prokaryotic Communities On and Below the Seafloor in the Back-Arc Hydrothermal System of the Southern Mariana Trough

“…Given that all or most of the Zetaproteobacteria are iron-oxidizers (Emerson et al 2010;Fleming et al 2013), any microbial ecosystem dominated by Zetaproteobacteria is supported by ferrous iron as the energy source (i.e., "iron-based ecosystem"). This is consistent with the thermodynamic calculation of bioavailable energy yields based on geochemical characteristics of the environments: the energy yield obtained from iron oxidation is comparable to or higher than that from oxidation of other reduced chemical species, such as hydrogen, hydrogen sulfide and methane (Kato et al 2012). Remarkably, iron-based ecosystems were found at both the Snail and Pika sites, even though their geological settings (on and off-ridge) are different (Seama et al Chap.…”

“…This group is related to the pSL12 clade that may contain ammonia oxidizers (Mincer et al 2007). These putative ammonia-oxidizing archaea potentially play a role as primary producers in prokaryotic ecosystems in the SMT, which is consistent with the high bioavailable energy yields obtained from ammonia oxidation (Kato et al 2012). …”

“…Members of the Zetaproteobacteria and Epsilonproteobacteria may use H 2 S or Fe 2+ dissolved in the venting hydrothermal fluids. Our previous study has shown that the diversity in bacterial community structures is consistent with the thermodynamic calculation of bioavailable energy yields from oxidation of reduced chemical species, such as hydrogen, hydrogen sulfide and iron, for each habitat (Kato et al 2012).…”

“…Thus, the development of iron-based ecosystems seems to be independent of these geological differences. Kato et al (2012) have suggested that higher concentration of ferrous iron than hydrogen sulfide, which can supply more energy for the growth of iron-oxidizers than sulfide-oxidizers, is needed for the development of ironbased ecosystems. In addition, the continuous supply of ferrous iron, the chemical conditions that make ferrous iron dissolve stably (i.e., low pH, low Eh and low concentration of sulfide), and the temperature at which the iron-oxidizers can grow may be also important for the development of iron-based ecosystems.…”

“…In particular, the chemosynthetic ecosystem supported by ferrous iron was found in the ironrich mats and crustal fluids (Kato et al 2012). However, comprehensive comparative analyses of the prokaryotic community structures among the SMT samples have not been carried out.…”