Abstract
Deep-sea hydrothermal vents may provide one of the largest reservoirs on Earth for hydrogen-oxidizing microorganisms. Depending on the type of geological setting, hydrothermal environments can be considerably enriched in hydrogen (up to millimolar concentrations). As hot, reduced hydrothermal fluids ascend to the seafloor they mix with entrained cold, oxygenated seawater, forming thermal and chemical gradients along their fluid pathways. Consequently, in these thermally and chemically dynamic habitats biochemically distinct hydrogenases (adapted to various temperature regimes, oxygen and hydrogen concentrations) from physiologically and phylogenetically diverse Bacteria and Archaea can be expected. Hydrogen oxidation is one of the important inorganic energy sources in these habitats, capable of providing relatively large amounts of energy (237 kJ/mol H2) for driving ATP synthesis and autotrophic CO2 fixation. Therefore, hydrogen-oxidizing organisms play a key role in deep-sea hydrothermal vent ecosystems as they can be considerably involved in light-independent primary biomass production. So far, the specific role of hydrogen-utilizing microorganisms in deep-sea hydrothermal ecosystems has been investigated by isolating hydrogen-oxidizers, measuring hydrogen consumption (ex situ), studying hydrogenase gene distribution and more recently by analyzing metatranscriptomic and metaproteomic data. Here we summarize this available knowledge and discuss the advent of new techniques for the identification of novel hydrogen-uptake and -evolving enzymes from hydrothermal vent microorganisms.
Highlights
Hydrogen conversion, the reversible reaction of molecular hydrogen (H2) to protons and electrons, plays a major role for metabolic processes in microbial cells: generally, energy conservation and the recycling of reducing equivalents is accomplished by enzymatic hydrogen evolution (Vignais and Billoud, 2007; Hallenbeck, 2009)
This review summarizes the work that has been done on hydrogen-metabolizing microorganisms colonizing hydrothermally influenced environments with respect to their diversity, hydrogen consumption rates in incubation experiments and protein biochemistry
A newly developed screen enables the search for environmental hydrogenases: It is based on the recombinant expression of metagenome-derived genes in a [NiFe]-hydrogenase deletion mutant of Shewanella oneidensis MR-1 (Adam and Perner, 2017)
Summary
The reversible reaction of molecular hydrogen (H2) to protons and electrons, plays a major role for metabolic processes in microbial cells: generally, energy conservation and the recycling of reducing equivalents (in microbial fermentation or light-dependent photosynthesis) is accomplished by enzymatic hydrogen evolution (Vignais and Billoud, 2007; Hallenbeck, 2009). There is a trend in the use of alternative electron donors with respect to the thermal preferences: while thermophilic members of the order Nautiliales tend to use formate (e.g., Nagata et al, 2017), mesophilic Campylobacterota like Sulfurimonas paralvinellae have the ability to use different reduced sulfur species such as thiosulfate or elemental sulfur as energy sources (Takai et al, 2006) Based on their metabolic and physiological versatility, Campylobacterota occupy diverse niches and can dominate microbial communities in hydrothermal vent environments. More than 90% of the intra- and inter-vent changes in the community compositions observed within this study could be explained with the geochemical variables determined for the different fluid, plume and background samples (e.g., temperature, pH, hydrogen, sulfide and nitrate concentrations) (Fortunato et al, 2018) Such clear-cut, proportional relations between abiotic environmental parameters and the corresponding microbial (metabolic) diversity are often difficult to draw. Symbiont-hosting Bathimodiolus tissue from basalt-hosted Comfortless Cove field, MAR basalt-hosted Lilliput field, MAR
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