Title:

Environmental and Engineered Factors Influence Membrane Features of Shale Taxa

Halotolerant anaerobic microbial communities, dominated by Halanaerobium, colonize fractured shale and adapt to extreme subsurface conditions. Despite the role these microorganisms play in altering biogeochemical reactions, effective energy capture, and well longevity, in situ growth kinetics and activities, including interactions with fluids and shale matrices are poorly understood. The microbial membrane protects the cell from external stressors and mediates critical physiologies, including transport, metabolism, aggregation and cell-surface interactions. Membrane functions are associated with the activities of peripheral and integral proteins, which in turn depend on biophysical properties such as bilayer symmetry, viscosity, curvature, elasticity and thickness. These properties are collectively dictated, to a large extent, by the membrane lipidome comprised of polar head groups and hydrophobic fatty acid tails. For Halanaerobium and other persistent microbial taxa of fractured shale, salinity and hydraulic retention time (HRT) are important perturbants of cell membrane structure. Hence, we used a suite of analytical techniques to investigate the effects of salinity (7%, 13% and 20% NaCl) and HRT (19.2 h, 24 h and 48 h) on membrane fatty acid composition and mechanics of Halanaerobium congolense WG10 and mixed enrichment cultures from hydraulically fractured wells in West Virginia. For these experiments, cultures were grown in chemostat vessels operated in continuous flow mode under strict anoxia and constant stirring. Our findings show that salinity and HRT induce changes in membrane fatty acid chemistry and biophysical properties of H. congolense WG10 in distinct and complementary ways. Notably, under suboptimal salt concentrations (7% and 20% NaCl), H. congolense WG10 elevates the proportion of polyunsaturated fatty acids (PUFAs) in its membrane, and this results in an apparent increase in fluidity (homeoviscous adaptation principle) and thickness. Taken together, these results provide insights into our understanding of how environmental and engineered factors might disrupt the physical and biogeochemical equilibria of fractured shale by inducing physiologically relevant changes in the membrane of persistent microbial taxa.

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