Abstract

Serpentinization is a widespread geochemical process associated with aqueous alteration of ultramafic rocks that produces abundant reductants (H2 and CH4) for life to exploit, but also potentially challenging conditions, including high pH, limited availability of terminal electron acceptors, and low concentrations of inorganic carbon. As a consequence, past studies of serpentinites have reported low cellular abundances and limited microbial diversity. Establishment of the Coast Range Ophiolite Microbial Observatory (California, U.S.A.) allowed a comparison of microbial communities and physicochemical parameters directly within serpentinization-influenced subsurface aquifers. Samples collected from seven wells were subjected to a range of analyses, including solute and gas chemistry, microbial diversity by 16S rRNA gene sequencing, and metabolic potential by shotgun metagenomics, in an attempt to elucidate what factors drive microbial activities in serpentinite habitats. This study describes the first comprehensive interdisciplinary analysis of microbial communities in hyperalkaline groundwater directly accessed by boreholes into serpentinite rocks. Several environmental factors, including pH, methane, and carbon monoxide, were strongly associated with the predominant subsurface microbial communities. A single operational taxonomic unit (OTU) of Betaproteobacteria and a few OTUs of Clostridia were the almost exclusive inhabitants of fluids exhibiting the most serpentinized character. Metagenomes from these extreme samples contained abundant sequences encoding proteins associated with hydrogen metabolism, carbon monoxide oxidation, carbon fixation, and acetogenesis. Metabolic pathways encoded by Clostridia and Betaproteobacteria, in particular, are likely to play important roles in the ecosystems of serpentinizing groundwater. These data provide a basis for further biogeochemical studies of key processes in serpentinite subsurface environments.

Highlights

  • The Earth’s subsurface is predicted to be an expansive habitat for microorganisms (Whitman et al, 1998; Edwards et al, 2012; Kallmeyer et al, 2012)

  • Fluids were collected from seven wells within the Coast Range Ophiolite Microbial Observatory (CROMO), which were drilled for the purpose of monitoring biogeochemistry and microbial community dynamics with high temporal and spatial resolution (Cardace et al, 2013)

  • Samples from wells CSW1.1 and QV1.1 are characterized by extremely high pH (12.2 and 11.5, respectively) and generally reducing character (Table 1)

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Summary

Introduction

The Earth’s subsurface is predicted to be an expansive habitat for microorganisms (Whitman et al, 1998; Edwards et al, 2012; Kallmeyer et al, 2012). Researchers have used caves (Northrup and Lavoie, 2001; Engel et al, 2004), mines (Onstott et al, 2003; Chivian et al, 2008), springs (Brazelton et al, 2012, 2013; Suzuki et al, 2013; Cardace et al, 2015), and isolated boreholes (Stevens and McKinley, 1995; Itävaara et al, 2011) as windows into the subsurface environment These features grant access to an otherwise inaccessible environment, but they represent opportunistic sampling locations. A series of wells were drilled directly into serpentinizationinfluenced aquifers of the Coast Range Ophiolite, a portion of ancient seafloor in northern California, USA, to sample microbial communities in serpentinizing rocks and groundwater This observatory represents the first opportunity to investigate microbial communities with direct access to the range of conditions in the serpentinizing subsurface (Cardace et al, 2013)

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