Microbial communities associated with alkaline hydrothermal systems of Prony Bay, New Caledonia

International audienceA shallow submarine hydrothermal field comparable to that of Lost City (http://www.lostcity.washington.edu/) was discovered in Prony Bay in the south of New Caledonia (SW Pacific). Both Prony and Lost City are ultramafic hydrothermal systems driven by serpentinization reactions of water with mantle rocks resulting in warm, anoxic, highly alkaline fluids (up to pH 11) rich in calcium, dissolved hydrogen and methane but depleted in carbon oxides and metals. Thus they sharply contrast with the very hot, acidic metal rich fluids typical of sulfidic vents (“black smokers”) associated with magmatic heat. Like in Lost City, the Prony Hydrothermal Field (PHF) is characterized by large carbonate chimneys (up to 30 m in height) venting clear fluids, which temperature however do not exceed 40°C (while it can reach up to 90°C in LCHF). The main difference between the two sites is the geological setting: oceanic (800 m depth) on ultrabasic massif off the MAR for LCHF and a costal environment (0 to 50 m depth) on perodotite nappe in a tectonic active area for PHF. Here, we report the first investigation on the microbial communities inhabiting the carbonate chimneys in PHF, focusing on the inner parts, most alkaline and warmest. For spatio-temporal analyses, samples were collected (2005, 2010 and 2011), from different sections of chimneys (top to bottom, outer to inner), located in seven sites (1 to 5 km distant) at varied depths (0 to 47 m) in the Prony bay. The structure and diversity of microbial communities and functional groups were compared by fingerprinting (SSCP/DGGE) and sequences analyses of clone libraries of both 16S rRNA and functional genes for methanogenesis (mcrA), methanotrophy (pmoA), and sulfate-reduction (dsrAB). We found that overall microbial patterns varied little inside a given chimney but changed in time and dramatically differs from one site to another, likely due to variation in hydrothermal activity and local geological settings. In each site and chimney sample, the specific richness of bacteria was an order higher than of archaea, in agreement with previous studies on LCHF. Archaea were dominated by few phylotypes of Methanosarcinales, related to the ANME group 2 (responsible for anaerobic methane oxydation) Lost City Methanosarcinales (LCMS). Bacteria were mostly affiliated to Firmicutes, α-, β-, and δ-Proteobacteria. Uncultivated lineages(candidate divisions OP1 and OP7), Chloroflexi and deep branching phylotypes were also identified. Interestingly, many bacterial phylotypes were related to alkaliphiles (Desulfonatronum, Alkaliphilus) or, surprisingly, to thermophiles (Thermotagales, Thermus) of volcanic hydrothermal systems. The main metabolic groups were methylotrophs, sulphate-reducers, sulphide oxidizers for bacteria and methanogens or methanotrophs (ANME-related) for archaea indicating that microbial cycling of sulphur and methane must be the dominant biogeochemical processes in PHF as previously observed in LCHF. The overall functions occurring in this original microbial ecosystem resemble those reported for LCHF, meanwhile the microbial actors fulfilling these roles corresponds to unique phylotypes, endemic to PHF. These data provide an important initial microbiological description of a novel example of submarine alkaline hydrothermal ecosystem for meaningful comparison to the well-studied LCHF