Serpentinization is the hydration and oxidation of ultramafic rock, which occurs as oceanic lithosphere is emplaced onto continental margins (ophiolites), and along the seafloor as faulting exposes this mantle-derived material to circulating hydrothermal fluids. This process leads to distinctive fluid chemistries as molecular hydrogen (H 2 ) and hydroxyl ions (OH − ) are produced and reduced carbon compounds are mobilized. Serpentinizing ophiolites also serve as a vector to transport sulfur compounds from the seafloor onto the continents. We investigated hyperalkaline, sulfur-rich, brackish groundwater in a serpentinizing continental ophiolite to elucidate the role of sulfur compounds in fuelling in situ microbial activities. Here we illustrate that key sulfur-cycling taxa, including Dethiobacter, Desulfitispora and 'Desulforudis', persist throughout this extreme environment. Biologically catalysed redox reactions involving sulfate, sulfide and intermediate sulfur compounds are thermodynamically favourable in the groundwater, which indicates they may be vital to sustaining life in these characteristically oxidant-and energy-limited systems. Furthermore, metagenomic and metatranscriptomic analyses reveal a complex network involving sulfate reduction, sulfide oxidation and thiosulfate reactions. Our findings highlight the importance of the complete inorganic sulfur cycle in serpentinizing fluids and suggest sulfur biogeochemistry provides a key link between terrestrial serpentinizing ecosystems and their submarine heritage.
Selenium (Se) redox chemistry is a determining factor for its environmental toxicity and mobility. Currently, millions of people are impacted by Se deficiency or toxicity, and in geologic history, several mass extinctions have been linked to extreme Se deficiency. Importantly, microbial activity and interactions with other biogeochemically active elements can drastically alter Se oxidation state and form, impacting its bioavailability. Here, we use wet geochemistry, spectroscopy, and electron microscopy to identify a cryptic, or hidden, Se cycle involving the reoxidation of biogenic volatile Se compounds in the presence of biogenic manganese [Mn(III, IV)] oxides and oxyhydroxides (hereafter referred to as “Mn oxides”). Using two common environmental Ascomycete fungi, Paraconiothyrium sporulosum and Stagonospora sp., we observed that aerobic Se(IV and VI) bioreduction to Se(0) and Se(-II) occurs simultaneously alongside the opposite redox biomineralization process of mycogenic Mn(II) oxidation to Mn oxides. Selenium bioreduction produced stable Se(0) nanoparticles and organoselenium compounds. However, mycogenic Mn oxides rapidly oxidized volatile Se products, recycling these compounds back to soluble forms. Given their abundance in natural systems, biogenic Mn oxides likely play an important role mediating Se biogeochemistry. Elucidating this cryptic Se cycle is essential for understanding and predicting Se behavior in diverse environmental systems.
Serpentinization involves the hydration and alteration of ultramafic rocks, which produces hydrogen (H 2 ) and methane (CH 4 ) and results in distinctive groundwater chemistries. As reacted fluids mix with recharging surface water, gradients in chemistry and microbiology develop in the subsurface. We present a comprehensive analysis of biogeochemical gradients in the water column of a serpentinitehosted well, CSW1.1, at the Coast Range Ophiolite Microbial Observatory (CROMO) in California, USA. Samples for geochemistry, 16S rRNA gene sequencing, and metagenomics were collected at four discrete depths from the top of the well corresponding to 100%, 50%, 15%, and 0% of atmospheric oxygen (O 2 ) levels, and from the well base at 19.5 m depth. Gibbs energy calculations assessed the energy available for a suite of reactions coupled to O 2 , sulfate (SO 4 2− ), and nitrate (NO 3 − ). Metagenomic data from the profile was used to construct metagenome assembled genomes (MAGs) to evaluate the completeness of biochemical pathways and compare the relative abundance of key diagnostic genes. Bioenergetic data point to the favorability of CH 4 oxidation reactions despite little genetic evidence for this. Amplicon sequencing results highlight the abundance of key taxa affiliated with the genera Truepera, Serpentinomonas, and Dethiobacter. Although concentrations of NO 3 − and H 2 are low, genes for NO 3 − reduction and oxidation of H 2 and carbon monoxide (CO) were found in high abundance. Conceptual modeling results demonstrate the net depletion of H 2 and CO in the groundwater, the consumption of CO 2 and O 2 , and the potential for CH 4 emission into the atmosphere at this terrestrial site of serpentinization.Plain Language Summary Microorganisms living in extreme habitats on Earth generate energy by catalyzing chemical reactions using the compounds available. A water-rock interaction known as serpentinization creates high pH and low-oxygen waters, and a limited number of compounds for energy generation. Hydrogen, carbon monoxide, and methane are gases produced through serpentinization that may be used by microorganisms. To unravel small-scale subsurface processes, we studied a depth profile from a serpentinization-influenced groundwater well, and sampled the water at five depths. We measured chemical components of the groundwater (anions, dissolved gases), and calculated the energy available to organisms using a set of common metabolic reactions. We also assessed the microbial communities present, and determined their potential contributions to biogeochemical cycles. We found that three taxa, Serpentinomonas, Truepera, and Dethiobacter dominated. Despite high methane concentrations, genes for methane oxidation were absent throughout the profile. Rather, genes associated with the use of low abundance compounds, like carbon monoxide, hydrogen, and nitrate, were prevalent. This implies that carbon monoxide and hydrogen consumption can deplete these compounds before they reach the surface, and the lack of methane consumption ma...
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