Abstract

The ancient origins of metabolism may be rooted deep in oceanic crust, and these early metabolisms may have persisted in the habitable thermal anoxic aquifer where conditions remain similar to those when they first appeared. The Wood–Ljungdahl pathway for acetogenesis is a key early biosynthetic pathway with the potential to influence ocean chemistry and productivity, but its contemporary role in oceanic crust is not well established. Here, we describe the genome of a novel acetogen from a thermal suboceanic aquifer olivine biofilm in the basaltic crust of the Juan de Fuca Ridge (JdFR) whose genome suggests it may utilize an ancient chemosynthetic lifestyle. This organism encodes the genes for the complete canonical Wood–Ljungdahl pathway, but is potentially unable to use sulfate and certain organic carbon sources such as lipids and carbohydrates to supplement its energy requirements, unlike other known acetogens. Instead, this organism may use peptides and amino acids for energy or as organic carbon sources. Additionally, genes involved in surface adhesion, the import of metallic cations found in Fe-bearing minerals, and use of molecular hydrogen, a product of serpentinization reactions between water and olivine, are prevalent within the genome. These adaptations are likely a reflection of local environmental micro-niches, where cells are adapted to life in biofilms using ancient chemosynthetic metabolisms dependent on H2 and iron minerals. Since this organism is phylogenetically distinct from a related acetogenic group of Clostridiales, we propose it as a new species, Candidatus Acetocimmeria pyornia.

Highlights

  • IntroductionWater–rock reactions common to the deep crust support active subsurface chemosynthetic microbial communities (Edwards et al, 2011; Lever et al, 2013) through the production of reduced compounds such as molecular hydrogen and labile organic carbon

  • The extrusive layer of igneous oceanic crust is one of Earth’s largest microbial habitats, and, though estimates vary widely, this habitat could contain up to 75% of the total carbon biomass on Earth (~200 Pg of carbon; Pg = 1015 g; Whitman et al, 1998; Heberling et al, 2010; Kallmeyer et al, 2012)

  • A. pyornia indicate this organism represents a novel acetogen within the bacterial Class Clostridia (Figure 1; Supplementary Figure 1)

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Summary

Introduction

Water–rock reactions common to the deep crust support active subsurface chemosynthetic microbial communities (Edwards et al, 2011; Lever et al, 2013) through the production of reduced compounds such as molecular hydrogen and labile organic carbon. These products are subsequently vented to the seafloor and may significantly increase secondary productivity and carbon cycling in the deep ocean (Mason et al, 2009; McCarthy et al, 2010). Acetogenesis may remain a key metabolic strategy in deep crustal aquifers, where contemporary conditions can often mirror those of the primordial state on early Earth (hot reducing fluids reacting with igneous minerals in oceanic crust)

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