Abstract
Submarine hydrothermal vents are model systems for the Archaean Earth environment, and some sites maintain conditions that may have favored the formation and evolution of cellular life. Vents are typified by rapid fluctuations in temperature and redox potential that impose a strong selective pressure on resident microbial communities. Nautilia profundicola strain Am-H is a moderately thermophilic, deeply-branching Epsilonproteobacterium found free-living at hydrothermal vents and is a member of the microbial mass on the dorsal surface of vent polychaete, Alvinella pompejana. Analysis of the 1.7-Mbp genome of N. profundicola uncovered adaptations to the vent environment—some unique and some shared with other Epsilonproteobacterial genomes. The major findings included: (1) a diverse suite of hydrogenases coupled to a relatively simple electron transport chain, (2) numerous stress response systems, (3) a novel predicted nitrate assimilation pathway with hydroxylamine as a key intermediate, and (4) a gene (rgy) encoding the hallmark protein for hyperthermophilic growth, reverse gyrase. Additional experiments indicated that expression of rgy in strain Am-H was induced over 100-fold with a 20°C increase above the optimal growth temperature of this bacterium and that closely related rgy genes are present and expressed in bacterial communities residing in geographically distinct thermophilic environments. N. profundicola, therefore, is a model Epsilonproteobacterium that contains all the genes necessary for life in the extreme conditions widely believed to reflect those in the Archaean biosphere—anaerobic, sulfur, H2- and CO2-rich, with fluctuating redox potentials and temperatures. In addition, reverse gyrase appears to be an important and common adaptation for mesophiles and moderate thermophiles that inhabit ecological niches characterized by rapid and frequent temperature fluctuations and, as such, can no longer be considered a unique feature of hyperthermophiles.
Highlights
Food webs at deep-sea hydrothermal vents are based on microbial primary productivity fueled by chemical reactions rather than light
Our analyses suggest that is N. profundicola the deepest branching epsilonproteobacterial genome to be sequenced to date, but its genome may provide evolutionary insights beyond what is required for growth at hydrothermal vents
Nautilia lithotrophica, isolated from the same geographic location as N. profundicola [23], returned negative results in this survey. These results suggest that if the Epsilonproteobacteria acquired rgy by horizontal gene transfer, it would have been prior to their split from other bacterial groups or prior to the split of the Nautiliales order, whereby some could have lost this gene or the gene sequence diverged enough to be undetectable with the degenerate primers used in the study
Summary
Food webs at deep-sea hydrothermal vents are based on microbial primary productivity fueled by chemical reactions rather than light. While a variety of diverse organisms have been isolated from hydrothermal environments [9,10], it is clear from molecular surveys and in situ hybridization studies that Epsilonproteobacteria are numerically dominant and likely key players in the cycling of C, N, and S at deep-sea hydrothermal vents [11]. We describe here the 1.7 Mbp genome of Nautilia profundicola strain Am-H, the first from a member of the order Nautiliales isolated from hydrothermal vents [20,21]. N. profundicola falls within the Nautiliales order of the Epsilonproteobacteria class, the deepest branching order of this subdivision [20,22,23,24,25] and is closely related to other vent isolates: Caminibacter hydrogeniphilus and Nautilia lithotrophica [22,23].
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