Diversity of Rare and Abundant Prokaryotic Phylotypes in the Prony Hydrothermal Field and Comparison with Other Serpentinite-Hosted Ecosystems

Abstract

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.

Hydrostatic Pressure Helps to Cultivate an Original Anaerobic Bacterium From the Atlantis Massif Subseafloor (IODP Expedition 357): Petrocella atlantisensis gen. nov. sp. nov.

“…Chimera sequences were identified and removed using vsearch (v2.3.4). The clustering to Operational Taxonomic Units (OTUs) (>97%) and their quality filtration were carried out using QIIME 1.9.1 (Caporaso et al, 2010) as described in (Frouin et al, 2018). Taxonomic assignment of the filtered OTUs was performed using the Uclust method against the SILVA database release for QIIME (v.123).…”

A dynamic microbial sulfur cycle in a serpentinizing continental ophiolite

“…Recent biogeochemical studies show that formate oxidation, likely carried out by sulfate reducing bacteria, supports the base of the LCHF ecosystem (Lang et al, 2018). At the Prony Hydrothermal Field in New Caledonia, a hybrid between marine and terrestrial serpentinites, sulfur-cycling organisms similar to the strictly anaerobic Dethiobacter alkaliphilus were identified that can utilize acetate and sugars with elemental sulfur, polysulfides and thiosulfate, yet cannot reduce sulfate directly (Sorokin et al, 2008;Pisapia et al, 2017;Frouin et al, 2018). For comparison, freshwater sites such as the Santa Elena ophiolite in Costa Rica and The Cedars in California lack sulfate (i.e., < 5.0 μM) and to date show little evidence of sulfur cycling (Crespo-Medina et al, 2017).…”

Microbial ecology of the newly discovered serpentinite-hosted Old City hydrothermal field (southwest Indian ridge)

“…Despite differences in the composition of microbial communities retrieved at PBHF compared to LCHF, PBHF chimneys interestingly harbor Archaea related to LCMS and to another Methanosarcinales phylotype (The Cedars Methanosarcinales, TCMS) [15], identified in springs of The Cedars ophiolite (California, USA [19]). The dominant Bacteria in PBHF relate to anaerobic Firmicutes and aerobic or facultative anaerobic Chloroflexi, Proteobacteria, and Bipolaricaulota (formerly Acetothermia) [13][14][15][16]. The co-occurrence of aerobic and anaerobic metabolisms at both LCHF and PBHF has been attributed to variable influences of the hydrothermal discharge creating anoxic environments within chimneys and of oxidized seawater intrusions from outside the chimneys [12,15].…”

“…Microbial communities sustained by serpentinization have recently been explored using next-generation sequencing and '-omic' technologies, although oceanic hydrothermal systems remain poorly explored compared to terrestrial springs due to difficulties in discovering and sampling sites at great water depth. Microbial taxa inhabiting LCHF chimneys differ from other serpentinite-hosted ecosystems [10][11][12], and even from PBHF [13][14][15][16]. Nevertheless, LCHF shares some microbiological commonalities with these other serpentinization-influenced habitats, including its extremely low taxonomic diversity [10,12].…”

“…The dominant Bacteria in PBHF relate to anaerobic Firmicutes and aerobic or facultative anaerobic Chloroflexi, Proteobacteria, and Bipolaricaulota (formerly Acetothermia) [13][14][15][16]. The co-occurrence of aerobic and anaerobic metabolisms at both LCHF and PBHF has been attributed to variable influences of the hydrothermal discharge creating anoxic environments within chimneys and of oxidized seawater intrusions from outside the chimneys [12,15]. However, since PBHF represents the only submarine analog of LCHF identified to date, the factors driving microbial ecology in these systems remain unclear.…”