Energetically informed niche models of hydrogenotrophs detected in serpentinized fluids of the Samail Ophiolite of Oman

Authors: HOWELLS, ALTA - Arizona State University; LEONG, JAMES - Arizona State University; ELY, TUCKER - Arizona State University; SANTANA, MICHELLE - Montana State University; ROBINSON, KIRT - Arizona State University; ESQUIVEL ELIZONDO, SOFIA - Arizona State University; COX, ALYSIA - Montana Tech; Poret-Peterson, Amisha; KRAJMALNIK-BROWN, ROSA - Arizona State University; SHOCK, EVERETT - Arizona State University

Submitted to: Journal of Geophysical Research-Biogeosciences
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/14/2022
Publication Date: N/A
Citation: N/A

Interpretive Summary: This study provides a framework for using high-throughput sequencing and physicochemical analyses to understand the distribution of microorganisms in the environment. A subsurface geological process called serpentinization, which produces hydrogen gas from water-rock interactions, and microbes that use hydrogen gas (hydrogenotrophs) are the focus of this study. To determine the physicochemical and biological factors that influence hydrogenotroph communities in a serpentinite-hosted ecosystem, we assessed the correspondence between hydrogenotroph distribution and chemical energy supplies used by their metabolism. We found that two different groups of hydrogenotrophs—sulfate reducers and methanogens—are differentially distributed in this ecosystem due to variation in the availability of their respective electron acceptors. Finally, by comparing hydrogentroph distribution to chemical energy supply, we characterized environmental thresholds for energy and substrates below which survival of these groups may be limited. This integrative approach to describe the environmental distribution of these particular microbes is applicable to other microbes and environments.

Technical Abstract: A geochemical gradient established by mixing between reduced, hyperalkaline (pH > 11), H2 rich fluids generated through the process of serpentinization and surrounding surface water (pH ~ 8) in the Samail Ophiolite of Oman provides an opportunity to characterize the geochemical and biological factors that influence the distribution of H2 oxidizing chemotrophs, hydrogenotrophs. In this study 16S rRNA gene amplicon sequencing was implemented to characterize hydrogenotrophs known to live in serpentinized fluids. A novel approach was implemented where hydrogenotroph phylotype distribution was evaluated across chemical energy supplies for their given metabolic redox reactions. Through this approach it was discovered that hydrogenotrophs are likely constrained to sites with < ~ 60 um O2, including microorganisms of the genus, Hydrogenophaga. Sulfate reducers of the family, Thermodesulfovibrionaceae, likely require > ~10 um SO4-2 for survival. At sites with > ~10 um SO4-2, sulfate reducers likely outcompete microorganisms of the methanogen genus, Methanobacterium, for H2. Additionally, differences in distribution between Thermodesulfovibrionaceae and Methanobacterium may be driven by the availability of electron acceptors and the redox reaction that is most energy yielding. Together, observations from the Oman geochemical gradient result in a hydrogenotroph niche model that can be used to evaluate global distribution patterns of hydrogenotrophs in continental serpentinized fluids. On a global scale, based on previous studies, Methanobacterium is constrained to fluids that have < ~ 10 um SO4-2. Overall, this study demonstrates the incredibly utility of evaluating 16S rRNA gene amplicon studies of chemotrophic communities within the framework geochemical energy supplies.