Metagenomic Evidence for H2 Oxidation and H2 Production by Serpentinite-Hosted Subsurface Microbial Communities

Matthew O Schrenk,William J Brazelton,Bridget Nelson

doi:10.3389/fmicb.2011.00268

Abstract

Ultramafic rocks in the Earth’s mantle represent a tremendous reservoir of carbon and reducing power. Upon tectonic uplift and exposure to fluid flow, serpentinization of these materials generates copious energy, sustains abiogenic synthesis of organic molecules, and releases hydrogen gas (H2). In order to assess the potential for microbial H2 utilization fueled by serpentinization, we conducted metagenomic surveys of a marine serpentinite-hosted hydrothermal chimney (at the Lost City hydrothermal field) and two continental serpentinite-hosted alkaline seeps (at the Tablelands Ophiolite, Newfoundland). Novel [NiFe]-hydrogenase sequences were identified at both the marine and continental sites, and in both cases, phylogenetic analyses indicated aerobic, potentially autotrophic Betaproteobacteria belonging to order Burkholderiales as the most likely H2-oxidizers. Both sites also yielded metagenomic evidence for microbial H2 production catalyzed by [FeFe]-hydrogenases in anaerobic Gram-positive bacteria belonging to order Clostridiales. In addition, we present metagenomic evidence at both sites for aerobic carbon monoxide utilization and anaerobic carbon fixation via the Wood–Ljungdahl pathway. In general, our results point to H2-oxidizing Betaproteobacteria thriving in shallow, oxic–anoxic transition zones and the anaerobic Clostridia thriving in anoxic, deep subsurface habitats. These data demonstrate the feasibility of metagenomic investigations into novel subsurface habitats via surface-exposed seeps and indicate the potential for H2-powered primary production in serpentinite-hosted subsurface habitats.

Highlights

The potentially vast microbial diversity and biomass of the subsurface biosphere (Whitman et al, 1998) has been frequently noted (Biddle et al, 2006; Huber et al, 2007; Santelli et al, 2008; Schrenk et al, 2010), but there is very little evidence to indicate how much of it is supported by new primary production or by recycling of buried organic carbon
It is possible that a more representative sample of the www.frontiersin.org subsurface habitat underlying the spring could reveal more abundant evidence of acetogenesis, as well as other anaerobic metabolic pathways. Both the marine and continental serpentinite springs investigated in this study show evidence of aerobic organisms capable of H2-fueled primary production (i.e., Burkholderiales) and anaerobic organisms capable of H2 production from fermentation of organic carbon (i.e., Clostridia)
This community structure resembles that of the deep subsurface habitat sampled by a ∼3 km deep borehole in South Africa (Moser et al, 2005), indicating that the surface-exposed springs described in this study provide access to organisms flushed from the subsurface

Summary

Introduction

The potentially vast microbial diversity and biomass of the subsurface biosphere (Whitman et al, 1998) has been frequently noted (Biddle et al, 2006; Huber et al, 2007; Santelli et al, 2008; Schrenk et al, 2010), but there is very little evidence to indicate how much of it is supported by new primary production or by recycling of buried organic carbon. Methane and larger hydrocarbon chains with up to four carbon atoms in Lost City fluids show evidence of an abiogenic origin in the deep subsurface (Proskurowski et al, 2008), but the amount of microbial activity supported by this abiotic source of organics has not been quantified. The anoxic interiors of Lost City carbonate chimneys are dominated by Methanosarcinales-related archaea potentially involved in methane production and oxidation (Schrenk et al, 2004; Brazelton et al, 2011). The role of H2-metabolizing bacteria in Lost City chimneys, though, has not been explicitly investigated

Methods

Results

Discussion

Conclusion