Dataset Information

Metagenomic and PCR-Based Diversity Surveys of [FeFe]-Hydrogenases Combined with Isolation of Alkaliphilic Hydrogen-Producing Bacteria from the Serpentinite-Hosted Prony Hydrothermal Field, New Caledonia.

ABSTRACT: High amounts of hydrogen are emitted in the serpentinite-hosted hydrothermal field of the Prony Bay (PHF, New Caledonia), where high-pH (~11), low-temperature (< 40°C), and low-salinity fluids are discharged in both intertidal and shallow submarine environments. In this study, we investigated the diversity and distribution of potentially hydrogen-producing bacteria in Prony hyperalkaline springs by using metagenomic analyses and different PCR-amplified DNA sequencing methods. The retrieved sequences of hydA genes, encoding the catalytic subunit of [FeFe]-hydrogenases and, used as a molecular marker of hydrogen-producing bacteria, were mainly related to those of Firmicutes and clustered into two distinct groups depending on sampling locations. Intertidal samples were dominated by new hydA sequences related to uncultured Firmicutes retrieved from paddy soils, while submarine samples were dominated by diverse hydA sequences affiliated with anaerobic and/or thermophilic submarine Firmicutes pertaining to the orders Thermoanaerobacterales or Clostridiales. The novelty and diversity of these [FeFe]-hydrogenases may reflect the unique environmental conditions prevailing in the PHF (i.e., high-pH, low-salt, mesothermic fluids). In addition, novel alkaliphilic hydrogen-producing Firmicutes (Clostridiales and Bacillales) were successfully isolated from both intertidal and submarine PHF chimney samples. Both molecular and cultivation-based data demonstrated the ability of Firmicutes originating from serpentinite-hosted environments to produce hydrogen by fermentation, potentially contributing to the molecular hydrogen balance in situ.

SUBMITTER: Mei N

PROVIDER: S-EPMC5003875 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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Publications

Metagenomic and PCR-Based Diversity Surveys of [FeFe]-Hydrogenases Combined with Isolation of Alkaliphilic Hydrogen-Producing Bacteria from the Serpentinite-Hosted Prony Hydrothermal Field, New Caledonia.

Mei Nan N Postec Anne A Monnin Christophe C Pelletier Bernard B Payri Claude E CE Ménez Bénédicte B Frouin Eléonore E Ollivier Bernard B Erauso Gaël G Quéméneur Marianne M

Frontiers in microbiology 20160830

High amounts of hydrogen are emitted in the serpentinite-hosted hydrothermal field of the Prony Bay (PHF, New Caledonia), where high-pH (~11), low-temperature (< 40°C), and low-salinity fluids are discharged in both intertidal and shallow submarine environments. In this study, we investigated the diversity and distribution of potentially hydrogen-producing bacteria in Prony hyperalkaline springs by using metagenomic analyses and different PCR-amplified DNA sequencing methods. The retrieved seque ...[more]

PMID: 27625634

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Project description:The southeastern part of New Caledonia main island (Grande Terre) is the location of a large ophiolitic formation that hosts several hyperalkaline springs discharging high pH (∼11) and warm (<40°C) fluids enriched in methane (CH4) and hydrogen (H2). These waters are produced by the serpentinization of the ultrabasic rock formations. Molecular surveys had previously revealed the prokaryotic diversity of some of these New Caledonian springs, especially from the submarine chimneys of Prony Bay hydrothermal field. Here we investigate the microbial community of hyperalkaline waters from on-land springs and their relationships with elevated concentrations of dissolved H2 (21.1-721.3 μmol/L) and CH4 (153.0-376.6 μmol/L). 16S rRNA gene analyses (metabarcoding and qPCR) provided evidence of abundant and diverse prokaryotic communities inhabiting hyperalkaline fluids at all the collected springs. The abundance of prokaryotes was positively correlated to the H2/CH4 ratio. Prokaryotes consisted mainly of bacteria that use H2 as an energy source, such as microaerophilic Hydrogenophaga/Serpentinimonas (detected in all sources on land) or anaerobic sulfate-reducing Desulfonatronum, which were exclusively found in the most reducing (Eh ref H2 ∼ -700 mV) and the most H2-enriched waters discharging at the intertidal spring of the Bain des Japonais. The relative abundance of a specific group of uncultured Methanosarcinales that thrive in serpentinization-driven ecosystems emitting H2, considered potential H2-consuming methanogens, was positively correlated with CH4 concentrations, and negatively correlated to the relative abundance of methylotrophic Gammaproteobacteria. Firmicutes were also numerous in hyperalkaline waters, and their relative abundance (e.g., Gracilibacter or Dethiobacter) was proportional to the dissolved H2 concentrations, but their role in the H2 budget remains to be assessed. The prokaryotic communities thriving in New Caledonia hyperalkaline waters are similar to those found in other serpentinite-hosted high-pH waters worldwide, such as Lost City (North Atlantic) and The Cedars (California).

Project description:The Bay of Prony, South of New Caledonia, represents a unique serpentinite-hosted hydrothermal field due to its coastal situation. It harbors both submarine and intertidal active sites, discharging hydrogen- and methane-rich alkaline fluids of low salinity and mild temperature through porous carbonate edifices. In this study, we have extensively investigated the bacterial and archaeal communities inhabiting the hydrothermal chimneys from one intertidal and three submarine sites by 16S rRNA gene amplicon sequencing. We show that the bacterial community of the intertidal site is clearly distinct from that of the submarine sites with species distribution patterns driven by only a few abundant populations, affiliated to the Chloroflexi and Proteobacteria phyla. In contrast, the distribution of archaeal taxa seems less site-dependent, as exemplified by the co-occurrence, in both submarine and intertidal sites, of two dominant phylotypes of Methanosarcinales previously thought to be restricted to serpentinizing systems, either marine (Lost City Hydrothermal Field) or terrestrial (The Cedars ultrabasic springs). Over 70% of the phylotypes were rare and included, among others, all those affiliated to candidate divisions. We finally compared the distribution of bacterial and archaeal phylotypes of Prony Hydrothermal Field with those of five previously studied serpentinizing systems of geographically distant sites. Although sensu stricto no core microbial community was identified, a few uncultivated lineages, notably within the archaeal order Methanosarcinales and the bacterial class Dehalococcoidia (the candidate division MSBL5) were exclusively found in a few serpentinizing systems while other operational taxonomic units belonging to the orders Clostridiales, Thermoanaerobacterales, or the genus Hydrogenophaga, were abundantly distributed in several sites. These lineages may represent taxonomic signatures of serpentinizing ecosystems. These findings extend our current knowledge of the microbial diversity inhabiting serpentinizing systems and their biogeography.

Project description:A non-bifurcating NADH-dependent, dimeric [FeFe]-hydrogenase (HydAB) from Syntrophus aciditrophicus was heterologously produced in Escherichia coli, purified and characterized. Purified recombinant HydAB catalyzed NAD+ reduction coupled to hydrogen oxidation and produced hydrogen from NADH without the involvement of ferredoxin. Hydrogen partial pressures (2.2-40.2 Pa) produced by the purified recombinant HydAB at NADH to NAD+ ratios of 1-5 were similar to the hydrogen partial pressures generated by pure and cocultures of S. aciditrophicus (5.9-36.6 Pa). Thus, the hydrogen partial pressures observed in metabolizing cultures and cocultures of S. aciditrophicus can be generated by HydAB if S. aciditrophicus maintains NADH to NAD+ ratios greater than one. The flavin-containing beta subunits from S. aciditrophicus HydAB and the non-bifurcating NADH-dependent S. wolfei Hyd1ABC share a number of conserved residues with the flavin-containing beta subunits from non-bifurcating NADH-dependent enzymes such as NADH:quinone oxidoreductases and formate dehydrogenases. A number of differences were observed between sequences of these non-bifurcating NADH-dependent enzymes and [FeFe]-hydrogenases and formate dehydrogenases known to catalyze electron bifurcation including differences in the number of [Fe-S] centers and in conserved residues near predicted cofactor binding sites. These differences can be used to distinguish members of these two groups of enzymes and may be relevant to the differences in ferredoxin-dependence and ability to mediate electron-bifurcation. These results show that two phylogenetically distinct syntrophic fatty acid-oxidizing bacteria, Syntrophomonas wolfei a member of the phylum Firmicutes, and S. aciditrophicus, a member of the class Deltaproteobacteria, possess functionally similar [FeFe]-hydrogenases that produce hydrogen from NADH during syntrophic fatty acid oxidation without the involvement of reduced ferredoxin. The reliance on a non-bifurcating NADH-dependent [FeFe]-hydrogenases may explain the obligate requirement that many syntrophic metabolizers have for a hydrogen-using partner microorganism when grown on fatty, aromatic and alicyclic acids.

Dataset Information

Metagenomic and PCR-Based Diversity Surveys of [FeFe]-Hydrogenases Combined with Isolation of Alkaliphilic Hydrogen-Producing Bacteria from the Serpentinite-Hosted Prony Hydrothermal Field, New Caledonia.

Publications

Metagenomic and PCR-Based Diversity Surveys of [FeFe]-Hydrogenases Combined with Isolation of Alkaliphilic Hydrogen-Producing Bacteria from the Serpentinite-Hosted Prony Hydrothermal Field, New Caledonia.

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