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

Marianne Quéméneur,Eléonore Frouin,Méline Bes,Fabrice Armougom,Bernard Ollivier,Gaël Erauso,Anne Postec,Didier Debroas

doi:10.3389/fmicb.2018.00102

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.

Highlights

Serpentinization is the alteration process that abiotically transforms olivine and pyroxene-rich rocks into serpentinites and yields alkaline hot fluids enriched in H2 and CH4 (Chavagnac et al, 2013)
The species richness distribution varied significantly from one site to another, with at least a twofold decrease in operational taxonomic units (OTUs) abundance for Bain des Japonais” (BdJ), ST07, and ST09 compared to the ST12 site (1203 OTUs, Supplementary Table S2)
The presence of more than 780 OTUs, specific to the ST12 site (Supplementary Figure S1A) and comprising mainly of rare taxa, might result from a lower in situ pH condition, in comparison with the other studied PHF sites (Monnin et al, 2014). This trend has previously been observed in the Coast Range Ophiolite serpentinizing site, where circumneutral pH wells contained many rare taxa that were absent in the high pH ones (Twing et al, 2017), most likely because these latter drastic conditions selected the few most alkaliphilic members within the prokaryotic community

Summary

Introduction

Serpentinization is the alteration process that abiotically transforms olivine and pyroxene-rich rocks into serpentinites and yields alkaline hot fluids enriched in H2 and CH4 (Chavagnac et al, 2013). Terrestrial ones, have recently been studied by molecular approaches using generation sequencing, to reveal the indigenous microbial community. They included the Cabeço de Vide Aquifer (CVA, Portugal) (Tiago and Veríssimo, 2013) and the ophiolites of Tablelands (Canada) (Brazelton et al, 2013), Santa Elena (Costa Rica) (Sánchez-Murillo et al, 2014; Crespo-Medina et al, 2017), Zambales (Philippines) (Woycheese et al, 2015), Samail (Oman) (Rempfert et al, 2017), Chimaera (Turkey) (Neubeck et al, 2017), Voltri (Italy) (Quéméneur et al, 2015; Brazelton et al, 2016), The Cedars (Placer, CA, United States) (Suzuki et al, 2017) and the nearby site of Coast Range Ophiolite Microbial Observatory (CROMO, Burbank, CA, United States) (Twing et al, 2017). The emblematic Lost-City hydrothermal field (LCHF) was the only serpentinizing ecosystem to be subjected to microbiological study targeting the rare biosphere (Brazelton et al, 2010)

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Conclusion