Abstract

The production of hydrogen and methane by geochemical reactions associated with the serpentinization of ultramafic rocks can potentially support subsurface microbial ecosystems independent of the photosynthetic biosphere. Methanogenic and methanotrophic microorganisms are abundant in marine hydrothermal systems heavily influenced by serpentinization, but evidence for methane-cycling archaea and bacteria in continental serpentinite springs has been limited. This report provides metagenomic and experimental evidence for active methanogenesis and methanotrophy by microbial communities in serpentinite springs of the Voltri Massif, Italy. Methanogens belonging to family Methanobacteriaceae and methanotrophic bacteria belonging to family Methylococcaceae were heavily enriched in three ultrabasic springs (pH 12). Metagenomic data also suggest the potential for hydrogen oxidation, hydrogen production, carbon fixation, fermentation, and organic acid metabolism in the ultrabasic springs. The predicted metabolic capabilities are consistent with an active subsurface ecosystem supported by energy and carbon liberated by geochemical reactions within the serpentinite rocks of the Voltri Massif.

Highlights

  • Hydrothermal systems hosted in ultramafic rocks rich in serpentine minerals can support active and unique microbial communities

  • All genes required for methanogenesis are present in the combined-spring assembly (Fig. 3), and many of these were collected in a single metagenomic bin corresponding to the Methanobacteriaceae taxa that are enriched in the ultrabasic springs (Fig. 2)

  • Methanol and formate are among the single carbon compounds predicted to be abiogenic products of serpentinization (Shock, 1992; Shock & Schulte, 1998; Seewald, Zolotov & McCollom, 2006), so these metagenomic data are consistent with the possibility that Methanobacteriaceae methanogens at this site are directly supported by subsurface serpentinization reactions

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Summary

Introduction

Hydrothermal systems hosted in ultramafic rocks rich in serpentine minerals can support active and unique microbial communities (see Schrenk, Brazelton & Lang, 2013 for review). The role of methane-cycling organisms in serpentinizing systems has been enigmatic since the discovery of thick biofilms of methanogens belonging to order Methanosarcinales in carbonate-brucite chimneys of the Lost City hydrothermal field (Schrenk et al, 2004). Whether these organisms are primarily involved in methane production or methane oxidation remains uncertain (Proskurowski et al, 2008; Bradley, Hayes & Summons, 2009; Brazelton et al, 2011; Lang et al, 2012; Méhay et al, 2013). Similar methanogens belonging to order Methanosarcinales have been identified in Prony Bay, New Caledonia, where freshwater serpentinizing fluids are venting into shallow marine waters and forming carbonate chimneys on the seafloor (Quéméneur et al, 2014). 16S rRNA genes associated with methanotrophic bacteria have been detected at Lost City (Brazelton et al, 2006) and Prony Bay (Quéméneur et al, 2014)

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