Adaptations to Submarine Hydrothermal Environments Exemplified by the Genome of Nautilia profundicola

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.

Genome and physiology of a model Epsilonproteobacterium responsible for sulfide detoxification in marine oxygen depletion zones

“…GD1, this organism was also capable of using hydrogen as an electron donor with nitrate as electron acceptor (Table S2); this has also been observed in microbes of deep-sea hydrothermal habitats (12). The presence of multiple hydrogenases in the genome (Table S3) suggests adaptations to different concentrations of hydrogen, as an important alternative electron donor, and a variety of electron acceptors (29). S. gotlandica str.…”

“…GD1. Hydrothermal vent Epsilonproteobacteria have numerous signal sensing and transduction mechanisms, essential for free-living bacteria in highly variable environments (29,31). Compared with previously described Epsilonproteobacteria, however, the total number of protein domains involved in environmental sensing and signal transduction is notably increased in the genome of S. gotlandica str.…”

“…GD1 (Fig. 4B), compared with the epsilonproteobacterial genomes from hydrothermal vents or from vent-associated metazoans, such as Caminibacter mediatlanticus, N. profundicola, and Nitratiruptor sp., for which a relatively simple electron transport chain has been described (29).…”

Elemental sulfur and acetate can support life of a novel strictly anaerobic haloarchaeon

“…However, in the presence of sulfide, a significant amount of S 0 is transformed into soluble inorganic polysulfide (Hedderich et al, 1999). One of the mechanisms of its utilization as a terminal acceptor was described for bacterial sulfur reducers Wolinella succinogenes and Nautilia profundicola (Klimmek et al, 1998;Campbell et al, 2009). The process relies on the activity of a periplasmic sulfurtransferase/ rhodanese-like protein (Sud), which acts as a polysulfide-binding carrier and represents the actual substrate for the catalytic molybdenum (Mo)-containing subunit PsrA.…”

Deep-sea hydrothermal ventEpsilonproteobacteriaencode a conserved and widespread nitrate reduction pathway (Nap)

“…Within the Epsilonproteobacteria, the napA gene has been detected in the genomes of the rumen bacterium W. succinogenes (Simon et al, 2003); of the pathogens Helicobacter hepaticus (Suerbaum et al, 2003), Campylobacter jejuni (Parkhill et al, 2000) and several other Campylobacter spp. (Kern and Simon, 2009a); and of Arcobacter butzleri (Miller et al, 2007), Sulfurimonas denitrificans and several Epsilonproteobacteria isolated from marine geothermal environments Voordeckers et al, 2005;Nakagawa et al, 2007;Campbell et al, 2009;Sikorski et al, 2010;Giovannelli et al, 2011). The genome sequence of these organisms showed that Epsilonproteobacteria encode the periplasmic nitrate reductase, NapA, and not for the membrane-bound enzyme, NarG (in contrast to, for example, E. coli, which encodes both enzymes).…”