Rock powered life in the Samail ophiolite: an analog for early Earth

Abstract

Serpentinization is a geochemical process wherein the oxidation of Fe(II)-bearing minerals in ultramafic rock couples with the reduction of water to generate H 2, which in turn can reduce inorganic carbon to biologically useful substrates such as carbon monoxide and formate. Serpentinization has been proposed to fuel a subsurface biosphere and may have promoted life's emergence on early Earth. However, highly reacted waters exhibit high pH and low concentrations of potential electron acceptors for microbial metabolism, including CO 2. To characterize how serpentinization shapes the distribution and diversity of microbial life, direct cell counts, microcosm-based activity assays, and genomic inferences were performed on environmental rock and water samples from the Samail Ophiolite, Oman. Microbial communities were shaped by water type with cell densities and activities generally declining with increasing pH. However, cells inhabiting highly reacted waters exhibited adaptations enabling them to minimize stresses imposed by serpentinization, including preferentially assimilating carbon substrates for biomolecule synthesis rather than dissimilating them for energy generation, maintaining small genomes, and synthesizing proteins comprised of more reduced amino acids to minimize energetic costs and maximize protein stability in highly reducing waters. Two distinct lineages of a genus of methanogens, Methanobacterium, were recovered from subsurface waters. One lineage was most abundant in high pH waters exhibiting millimolar concentrations of H2, yet lacked two key oxidative [NiFe]-hydrogenases whose functions were presumably replaced by formate dehydrogenases that oxidize formate to yield reductant and CO 2. This allows cells to overcome CO 2/oxidant limitation in high pH waters via a pathway that is unique among characterized Methanobacteria. Finally, gabbro cores from the Stillwater Mine (Montana, U.S.A) were used to develop methods for detecting the activities of cells inhabiting mafic to ultramafic igneous rocks while controlling for potential contaminants. Optimized protocols were applied to rock cores from the Samail Ophiolite, where rates of biological formate and acetate metabolism were higher in rocks interfacing less reacted waters as compared with more extensively reacted waters, and in some cases may greatly exceed activities previously measured in fracture waters. This dissertation provides new insights into the distribution, activities, and adaptations exhibited by life in a modern serpentinizing environment.