Potential energy sources for the deep continental biosphere in isolated anoxic brines

William S. Dowd, Christopher J. Schuler, Cara M. Santelli, Brandy M. Toner, Cody S. Sheik, Kelden Pehr, Jill M. McDermott

Research output: Contribution to journalArticlepeer-review

Abstract

In isolated fracture networks in the Precambrian Shield, long-term water and rock interactions produce saline anoxic fluids that host extant microbial communities deep within the continental subsurface. Light and oxygen (O2) are absent in these environments. Thus, chemotrophic organisms inhabiting these systems rely on anaerobic reactions for energy. Viable electron donors include short-chain alkanes, such as methane (CH4) and C2+ alkanes, while alternative electron acceptors include sulfate (SO2−4), nitrate (NO−3), and ferric iron (Fe3+). Here, we constrain the potential sources of energy for microorganisms in Neoarchean bedrock on the 27th level west drift of the Soudan Underground Mine State Park, MN, USA (713.5 meters below the surface). The Gibbs Free Energy (ΔG) of 11 reactions are modeled and expressed as available chemical potential energy per mass fluid (J/kgfluid). Metabolic reactions involving CH4 oxidation by SO2−4 would yield the highest potential energy of reactions modeled in this study (−111 J/kgfluid). The free energy for methanogenesis via the breakdown of dimethylamine (DMA; ∑(CH3)2NH(aq)) is exergonic but with near-zero available energy per mass fluid, suggesting that DMA may be cycled quickly to produce biological CH4 at Soudan. We examine all the possible pathways by which CH4 and other short-chain alkanes may be formed. Conventional δ13CCH4 values and C1/C2+ abundance ratios support a mixed biological and non-biological origin of CH4. Doubly substituted ‘clumped’ CH4 isotope 13CH3D values are consistent with formation temperatures of 84-89 °C that exceed current environmental conditions of 11.5-12.1 °C. These estimated formation temperatures are too low for CH4 to be formed solely through thermogenic degradation of organic matter. Further, low or undetectable H2 rules out active abiogenesis of CH4 from CO2 reduction. It is more likely that the bulk CH4 pool reflects a mixture of microbial CH4 with Δ13CH3D values equilibrated at 11.5-12.1 °C and thermogenic CH4 formed at temperatures >100 °C. Understanding the origin and cycling of these electron donors contributes to a fundamental understanding of how microbial activity may promote, maintain, or suppress the habitability of these isolated systems over long timescales.

Original languageEnglish (US)
Article number117720
JournalEarth and Planetary Science Letters
Volume595
DOIs
StatePublished - Oct 1 2022

Bibliographical note

Funding Information:
This work was funded by National Science Foundation Grants # EAR-1813237 and # EAR-1813526 , and the NASA Astrobiology Grant # 80NSSC18M0094 . This material is based upon research supported by the National Aeronautics and Space Administration through the NASA Astrobiology Institute under Cooperative Agreement No. 80NSSC18M0094 issued through the Science Mission Directorate. We thank the Soudan Underground Mine State Park staff for providing access to the field site and assisting with permit applications. We are grateful to mine staff and colleagues from Lehigh University, University of Minnesota Twin Cities, and University of Minnesota Duluth for helping coordinate multiple sampling trips. We thank editor Boswell Wing and two anonymous reviewers for providing helpful feedback that improved this manuscript.

Funding Information:
This work was funded by National Science Foundation Grants #EAR-1813237 and #EAR-1813526, and the NASA Astrobiology Grant #80NSSC18M0094. This material is based upon research supported by the National Aeronautics and Space Administration through the NASA Astrobiology Institute under Cooperative Agreement No. 80NSSC18M0094 issued through the Science Mission Directorate. We thank the Soudan Underground Mine State Park staff for providing access to the field site and assisting with permit applications. We are grateful to mine staff and colleagues from Lehigh University, University of Minnesota Twin Cities, and University of Minnesota Duluth for helping coordinate multiple sampling trips. We thank editor Boswell Wing and two anonymous reviewers for providing helpful feedback that improved this manuscript.

Publisher Copyright:
© 2022 The Author(s)

Keywords

  • Gibbs free energy
  • alkanes
  • anoxic brine
  • clumped methane
  • deep biosphere
  • dimethylamine

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