title: Mineralizing Filamentous Bacteria from the Prony Bay Hydrothermal Field Give New Insights into the Functioning of Serpentinization-Based Subseafloor Ecosystems.
abstract: Despite their potential importance as analogs of primitive microbial metabolisms, the knowledge of the structure and functioning of the deep ecosystems associated with serpentinizing environments is hampered by the lack of accessibility to relevant systems. These hyperalkaline environments are depleted in dissolved inorganic carbon (DIC), making the carbon sources and assimilation pathways in the associated ecosystems highly enigmatic. The Prony Bay Hydrothermal Field (PHF) is an active serpentinization site where, similar to Lost City (Mid-Atlantic Ridge), high-pH fluids rich in H2and CH4are discharged from carbonate chimneys at the seafloor, but in a shallower lagoonal environment. This study aimed to characterize the subsurface microbial ecology of this environment by focusing on the earliest stages of chimney construction, dominated by the discharge of hydrothermal fluids of subseafloor origin. By jointly examining the mineralogy and the microbial diversity of the conduits of juvenile edifices at the micrometric scale, we find a central role of uncultivated bacteria belonging to theFirmicutesin the ecology of the PHF. These bacteria, along with members of the phylaAcetothermiaandOmnitrophica, are identified as the first chimneys inhabitants before archaealMethanosarcinales. They are involved in the construction and early consolidation of the carbonate structuresviaorganomineralization processes. Their predominance in the most juvenile and nascent hydrothermal chimneys, and their affiliation with environmental subsurface microorganisms, indicate that they are likely discharged with hydrothermal fluids from the subseafloor. They may thus be representative of endolithic serpentinization-based ecosystems, in an environment where DIC is limited. In contrast, heterotrophic and fermentative microorganisms may consume organic compounds from the abiotic by-products of serpentinization processes and/or from life in the deeper subsurface. We thus propose that theFirmicutesidentified at PHF may have a versatile metabolism with the capability to use diverse organic compounds from biological or abiotic origin. From that perspective, this study sheds new light on the structure of deep microbial communities living at the energetic edge in serpentinites and may provide an alternative model of the earliest metabolisms.
authors.affiliation: Geomicrobiology Group, Institut de Physique du Globe de Paris, Sorbonne Paris Cité, Université Paris Diderot, Centre National de la Recherche ScientifiqueParis, France; DISCO beamline, Synchrotron SOLEILSaint Aubin, France.
authors.forename: Céline
authors.initials: C
authors.lastname: Pisapia
authors.affiliation: Geomicrobiology Group, Institut de Physique du Globe de Paris, Sorbonne Paris Cité, Université Paris Diderot, Centre National de la Recherche Scientifique Paris, France.
authors.forename: Emmanuelle
authors.initials: E
authors.lastname: Gérard
authors.affiliation: Institut de Minéralogie, de Physique des Matériaux et de Cosmochimie, Institut de Recherche pour le Développement, Université Pierre et Marie Curie Paris, France.
authors.forename: Martine
authors.initials: M
authors.lastname: Gérard
authors.affiliation: Institut de Minéralogie, de Physique des Matériaux et de Cosmochimie, Institut de Recherche pour le Développement, Université Pierre et Marie Curie Paris, France.
authors.forename: Léna
authors.initials: L
authors.lastname: Lecourt
authors.affiliation: Department of Earth and Ocean Sciences, School of the Earth, Ocean and Environment, University of South Carolina, Columbia SC, USA.
authors.forename: Susan Q
authors.initials: SQ
authors.lastname: Lang
authors.affiliation: GIS Grand Observatoire de l'environnement et de la biodiversité terrestre et marine dans le Pacifique Sud, Centre IRD de Nouméa Nouméa, New Caledonia.
authors.forename: Bernard
authors.initials: B
authors.lastname: Pelletier
authors.affiliation: UR227 COREUS, Centre IRD de Nouméa Nouméa, New Caledonia.
authors.forename: Claude E
authors.initials: CE
authors.lastname: Payri
authors.affiliation: Géosciences Environnement Toulouse, Université Paul Sabatier, Centre National de la Recherche Scientifique, Institut de Recherche pour le Développement Toulouse, France.
authors.forename: Christophe
authors.initials: C
authors.lastname: Monnin
authors.affiliation: UR227 COREUS, Centre IRD de NouméaNouméa, New Caledonia; Laboratoire Matériaux Polymères Interfaces Environnement Marin EA 4323, Université de ToulonLa Garde, France; Mediterranean Institute of Oceanography, Centre IRD de NouméaNouméa, New Caledonia; Laboratoire Insulaire du Vivant et de l'Environnement, Université de la Nouvelle-CalédonieNouméa, New Caledonia.
authors.forename: Linda
authors.initials: L
authors.lastname: Guentas
authors.affiliation: Aix Marseille Université, Centre National de la Recherche Scientifique - Institut National des Sciences de L'Univers, Université de Toulon, Institut de Recherche pour le Développement, Mediterranean Institute of Oceanography Marseille, France.
authors.forename: Anne
authors.initials: A
authors.lastname: Postec
authors.affiliation: Aix Marseille Université, Centre National de la Recherche Scientifique - Institut National des Sciences de L'Univers, Université de Toulon, Institut de Recherche pour le Développement, Mediterranean Institute of Oceanography Marseille, France.
authors.forename: Marianne
authors.initials: M
authors.lastname: Quéméneur
authors.affiliation: Aix Marseille Université, Centre National de la Recherche Scientifique - Institut National des Sciences de L'Univers, Université de Toulon, Institut de Recherche pour le Développement, Mediterranean Institute of Oceanography Marseille, France.
authors.forename: Gaël
authors.initials: G
authors.lastname: Erauso
authors.affiliation: Geomicrobiology Group, Institut de Physique du Globe de Paris, Sorbonne Paris Cité, Université Paris Diderot, Centre National de la Recherche Scientifique Paris, France.
authors.forename: Bénédicte
authors.initials: B
authors.lastname: Ménez
keywords: Acetothermia; Firmicutes; Omnitrophica; alkaline hydrothermalism; deep life; organic carbon; serpentinization