Geochemical energy sources for microbial primary production in the environment of hydrothermal vent shrimps

Abstract

At deep-sea hydrothermal vents, dense invertebrate communities prevail along chemoclines where the relaxation of redox-disequilibria sustains chemolithoautotrophic microbial CO2-fixation. At the Mid-Atlantic Ridge, swarms of thousands of Rimicaris exoculata shrimps thus assemble along the turbulent mixing interface between the hydrothermal fluid and oxygenated seawater. It was suggested that this environment provides ideal conditions for growth to the abundant chemosynthetic microbial epiflora that colonizes the shrimps' branchial cavity. Sulfide has long been considered as the prime electron donor used by the epibionts but, the oxidation of iron has recently been hypothesized as an alternative pathway for the iron-rich Rainbow site. In order to examine the potential energy sources for microbial primary production within the swarms at Rainbow, the chemical conditions along the mixing gradient have been modeled from field data. This model provides a basis for the quantitative comparison of energy-budgets available for chemolithoautotrophic primary production based on different oxidative pathways (e.g.: oxidation of sulfide-iron II-methane and hydrogen by oxygen). A comparison was proposed for TAG, another hydrothermal vent field at the mid-Atlantic Ridge which is characterized by the presence of similar swarms. Although the narrow temperature range of the shrimp environment is similar at both sites, their chemically contrasted environments suggest different metabolic pathways would benefit from the highest energy budgets. While sulfide oxidation is confirmed to be the energetically most favorable pathway at TAG, an original biogeochemical context is suggested for Rainbow. Here, the highest energy could be derived from iron oxidation. At this site, the oxidation of hydrogen possibly constitutes another dominant energy source, but this hypothesis still needs to be constrained by kinetic studies. Methane and sulfide appears as minor energy sources in the environment of shrimps. A wider and original diversity of the metabolic pathways involved in the microbial epibiosis can be expected at Rainbow in comparison to TAG.