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Radiolytic Support For Oxidative Metabolism In An Ancient Subsurface Brine System

By Keith Cowing

Status Report

ISME Communications

November 7, 2024

Filed under abiotic stress, aerobic heterotrophy, Agrococcus, Atopococcus, brine, Caenispirillum, catabolic energy, Chromohalobacter, Curtobacterium, extremophile, habitability, Habitable Zone, Halomonas, Halomondaceae, Idiomarina, Idiomarinaceae, ISME Communications, Microbacteriaceae, Microbacterium, microbiology, Moab Khotsong, Pseudomonas, radionuclides, Shinella, subsurface brine environment, xenobiotic

Radiolytic Support For Oxidative Metabolism In An Ancient Subsurface Brine System — Images of cells via optical microscopy for 95-level (a), and via fluorescence microscopy combined with SYTO-9 staining for the (b) 101-level, (c) 1200-level, and (d) service water. Scale bar on the lower right of each image represents 5 μm. Magnification was 50x for (a) and 1000x for (b), (c) and (d). Cells in (a) are circular features entrapped in halite fluid inclusions and identified by red arrows. Cells in (b), (c), and (d) appear as bright green shapes. In (b), green background fluorescence highlights the high level of dissolved organic carbon debris for this sample [29]. Cell counts for the 95-, 101-, service water, and 1200-levels were 102 cells/mL ±10, 104 cells/mL ± 102, 106 cells/mL ± 104.5, 105 cells/mL ±103.3, respectively (error in standard deviation). A schematic is included to the right showing the depth and major lithology of fluid sampling sites considered in this study. — ISME Communications

Long-isolated subsurface brine environments (Ma-Ga residence times) may be habitable if they sustainably provide substrates, e.g. through water-rock reaction, that support microbial catabolic energy yields exceeding maintenance costs.

The relative inaccessibility and low biomass of such systems has led to limited understanding of microbial taxonomic distribution, metabolism, and survival under abiotic stress exposure in these extreme environments.

In this study, taxonomic and metabolic annotations of 95 single cell amplified genomes (SAGs) were obtained for one low biomass (103–104 cells/mL), hypersaline (246 g/L), radiolytically enriched brine obtained from 3.1 km depth in South Africa’s Moab Khotsong mine.

The majority of SAGs belonged to three halophilic families (Halomondaceae (58%), Microbacteriaceae (24%), and Idiomarinaceae (8%)) and did not overlap with any family-level identifications from service water or a less saline dolomite aquifer sampled in the same mine.

Functional annotation revealed complete metabolic modules for aerobic heterotrophy (organic acids and xenobiotics oxidation), fermentation, denitrification and thiosulfate oxidation, suggesting metabolic support in a microoxic environment.

SAGs also contained complete modules for degradation of complex organics, amino acid and nucleotide synthesis, and motility. This work highlights a long-isolated subsurface fluid system with microbial metabolism fueled by radiolytically generated substrates, including O₂, and suggests subsurface brines with high radionuclide concentrations as putatively habitable and redox-sustainable environments over long (ka-Ga) timescales.

Total community nutrient cycling diagrams for 101-level brine SAGs as determined by METABOLIC-C for (a) carbon (b) nitrogen, and (c) sulfur. Red arrows indicate the metabolic function is present in at least one SAG in the community (≥75% of gene annotations found for that function in a SAG). Symbols indicate genera associated with a particular pathway, based on individual nutrient cycling annotations for the top three most complete SAGs in each genus, including: Agrococcus (right triangle), Atopococcus (three-quarter circle), Caenispirillum (circle), Chromohalobacter (diamond), Curtobacterium (trapezoid), Halomonas (square), Idiomarina (star), Microbacterium (x mark), Pseudomonas (equilateral triangle), Shinella (plus sign).– ISME Communications

Radiolytic support for oxidative metabolism in an ancient subsurface brine system, ISME Communications, (open access)

Astrobiology,

Keith Cowing

Explorers Club Fellow, ex-NASA Space Station Payload manager/space biologist, Away Teams, Journalist, Lapsed climber, Synaesthete, Na’Vi-Jedi-Freman-Buddhist-mix, ASL, Devon Island and Everest Base Camp veteran, (he/him) 🖖🏻

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