Microbial taxa related to natural hydrogen and methane emissions in serpentinite-hosted hyperalkaline springs of New Caledonia

Marianne Quéméneur; Nan Mei; Christophe Monnin; Anne Postec; Sophie Guasco; Julie Jeanpert; Pierre Maurizot; Bernard Pelletier; Gaël Erauso

doi:10.3389/fmicb.2023.1196516

Microbial taxa related to natural hydrogen and methane emissions in serpentinite-hosted hyperalkaline springs of New Caledonia

Front Microbiol. 2023 Jul 6:14:1196516. doi: 10.3389/fmicb.2023.1196516. eCollection 2023.

Authors

Affiliations

¹ Aix Marseille Univ, Université de Toulon, CNRS, IRD, MIO, Marseille, France.
² School of Chemistry, Chemical Engineering, and Life Science, Wuhan University of Technology, Wuhan, China.
³ Géosciences Environnement Toulouse, UMR 5563 (CNRS/UPS/IRD/CNES), Toulouse, France.
⁴ Direction de l'Industrie, des Mines et de l'Energie, Nouméa, New Caledonia.
⁵ Centre IRD de Nouméa, Nouméa, New Caledonia.

^# Contributed equally.

Abstract

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 (E_h 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).

Keywords: archaea; bacteria; geothermal springs; high-pH water; methane; microbial diversity; natural hydrogen; serpentinization.

Grants and funding

This project was financially supported by the French Institute of Research for Development (IRD), the INTERVIE CNRS INSU program, the H2NAT project funded by the Midi-Pyrénées Observatory (OMP, Toulouse), and the ANR MICROPRONY (N°19-CE02-0020-02).