A dynamic microbial sulfur cycle in a serpentinizing continental ophiolite

Abstract

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.

Microbial Communities in a Serpentinizing Aquifer Are Assembled through Strong Concurrent Dispersal Limitation and Selection

“…In recent years, the microbiology of serpentinizing systems has been studied in a variety of marine ( 7 – 9 ) and terrestrial ( 6 , 10 – 16 ) environments. This work has confirmed the presence of endemic, low diversity, microbial communities capable of tolerating the extreme pH ( 15 , 16 ) and utilizing available hydrogen ( 17 , 18 ), carbon monoxide ( 17 , 19 ), methane ( 14 , 20 ), acetate ( 6 , 14 , 21 ), formate ( 18 – 21 ), and sulfur compounds ( 22 ) for both dissimilatory and assimilatory metabolic processes. Combined, this work has provided ample evidence that distinct communities of microorganisms inhabit serpentinizing environments and that they play active roles in these ecosystems.…”

Sulfide Dissolution and Awaruite Formation in Continental Serpentinization Environments and Its Implications to Supporting Life

“…In these rocks, evidence for microbial sulfate reduction can be traced to at least 150 m depths of the basement (Alt & Shanks, 1998). Similarly, sulfate reducers, sulfide oxidizers, and microbes using intermediate thiosulfate species have been detected within fluids of continental sites of serpentinization (e.g., Sabuda et al., 2020; Zwicker et al., 2018). While sulfate‐reducing microbes may live within fractures and cracks, the occurrence of finely disseminated sulfide minerals with biogenic signatures also suggests that they possibly live within the pore space of serpentinites (Schwarzenbach et al., 2018).…”

Aqueous Geochemical and Microbial Variation Across Discrete Depth Intervals in a Peridotite Aquifer Assessed Using a Packer System in the Samail Ophiolite, Oman

“…Homologs of proteins involved in sulfide oxidation were also detected in metagenomes from Lost City and the Liguria Ophiolite (W. J. Brazelton et al, 2017;Lang et al, 2018;Sabuda et al, 2020). Thus, microbes such as Thiobacillus may contribute to oxidation and mobilization of sulfide-S at the BA1 site and other serpentinizing settings.…”

“…This metabolic strategy may be particularly well-suited to  2 CO -depleted, hyperalkaline conditions, so long as there is a steady source of organic C. Moreover, low but detectable rates of microbial  2 4 SO reduction have been measured in groundwaters sampled from wells in the Samail Ophiolite and the Coast Range Ophiolite (Glombitza et al, 2021) and in nearby Oman Drilling Project well rock cores (Templeton et al, 2021). Taxa related to Thermodesulfovibrionia have been identified in other serpentizing settings including the Coast Range Ophiolite, USA (Glombitza et al, 2021;Sabuda et al, 2020), Zambales Ophiolite, the Philippines (Woycheese et al, 2015), Lost City hydrothermal field, Mid-Atlantic Ridge (W. J. Brazelton et al, 2006), La Crouen, New Caledonia (Quéméneur et al, 2021), Old City hydrothermal field, SW Indian NOTHAFT ET AL.…”

“…Ridge (Quéméneur et al, 2021), and the Chimaera Seeps, Turkey (Neubeck et al, 2017). Bioenergetic, metagenomic, and metatranscriptomic evidence of bacterial  2 4 SO reduction has been particularly strongly demonstrated at the Coast Range Ophiolite (Sabuda et al, 2020) and at Lost City (Lang et al, 2018). More broadly, the dominance of  2 4 SO reducers we find at depth in BA1A and BA1D is similar to a microbial community dominated by a single 16S rRNA gene phylotype related to thermophilic  2 4 SO reducers belonging to Firmicutes (>88 % of clones) in alkaline saline groundwater sampled at 2.8km depth in Archaean metabasalt within a South African gold mine, where radiolytically produced 2 H abounds (L.-H. Lin et al, 2006).…”