Executive Summary:
Geomicrobiology

The deep biosphere is alive but remains enigmatic

Scope. The deep biosphere is the habitable zone within the Earth’s lithosphere (continental and oceanic) in which microbial life exists (1,2). Here, microbial metabolisms shape the chemistry of soils and sediments, provide critical habitat/symbiosis for plant root zones (shallow and deep), and to deeper subsurface environments where carbon and other elements are metabolized across geologic time. One common feature of the deep biosphere is the isolation of microorganisms from Earth’s surface processes over varying geologic timescales. However, we continually see that human activities can short-circuit and accelerate microbiological processes in the subsurface through mineral and hydrocarbon extraction, contaminant spills, and storage. Furthermore, microbes are responsible for concentrating and degrading ore and fossil fuel deposits, can remediate or exacerbate subsurface pollution, are responsible for the corrosion of buried infrastructure, and are a source of greenhouse gasses to the atmosphere. Access to the deepest biosphere has hindered our view of life and, therefore, it remains one of the most poorly characterized components of living biomass on Earth (3,4). Despite the many unknowns, the deep biosphere has been shown to greatly influence modern surface processes, like carbon cycling above subduction zones (5). We know that subsurface microbial life is fueled through chemosynthetic metabolisms or through heterotrophy of ancient carbon (6), and these processes affect groundwater and ocean chemistry.  Thus, the extent to which subsurface microorganisms can drive global element cycles is likely greater than what is currently recognized. Finally, by studying the deep biosphere, we can inform and improve strategies for waste storage (e.g., near-surface sanitary landfills, deeper injection wells, nuclear waste), energy generation and exploitation, development of a hydrogen economy, and how subsurface carbon affects the climate of Earth’s atmospheric compartment.

Theme 1. Active processes connect the deep biosphere to Earth's surface conditions, affecting climate, energy extraction, and waste disposal. With limited study to date, we understand that the deep subsurface biosphere provides many ecosystem services that sustain humanity. Linkages between geological and biological processes in the deep subsurface biosphere may provide clues to life's origin and early evolution. With this understanding come questions:

●      What is the distribution and diversity of life’s three domains and viruses in the subsurface?

○      What are the key environmental parameters controlling distribution and diversity?

○      What are the dispersal patterns, modes, and rates in the subsurface?

○      How do we define evolution when population sizes are vanishingly small and cell growth and metabolic rates are extremely slow?

○      What biodiversity remains to be discovered (i.e., microbial dark matter)?

●      What biotic-abiotic interactions result in positive and negative feedback on habitat suitability (e.g., fracture formation or closure)?

○      What are the key cellular physiological adaptations?

○      What is the role of fluid flow on feedback between biotic and abiotic processes in the deep biosphere?

○      Which minerals and metals are critical to microbial function in the deep biosphere?

Theme 2. Longevity of the deep biosphere and its role in elemental cycling on geologic timescales. The study of Theme 2 ultimately has the benefit of revealing Earth’s processes, evolution, and cycling of elements, interpretation of the rock record, and consideration of life elsewhere. We do not yet know the extent of chemosynthetic life on Earth nor what is possible elsewhere in our local and distant universe. Key questions to explore include:

●      What is the role of lithology and fluid flow in controlling species distribution, dispersal, and metabolism patterns?

●      What are the energy requirements and microbial strategies for long-term survival and maintenance of subsurface life?

●      What is the potential for the deep biosphere to serve as a repository for ancient lineages?

●      How do we observe past subsurface microbial activity as recorded by rocks and minerals?

●      What is the role of tectonics (e.g. fault movement), magmatism, planetary collisions, and other large-scale geological or planetary processes in releasing substrates for microbial growth and what role does this play in the evolution of life?

Challenges and Proposed Solutions. The deep biosphere must be explored through continental drilling expeditions led by deep biosphere research questions using deep biosphere methodologies and contamination controls (7-10). Microbiological analyses, whose methods have been available and refined for decades, are ready to be used in studying the deep continental biosphere as lead efforts. Twenty years after the 2003 EarthLab report to NSF (7), impediments to scientific advances continue primarily in the form of funding structures and infrastructure that do not serve the continental geomicrobiology community.

●      Infrastructure. Assembling, shipping, maintaining, and storing essential microbiological tools on-site is an impediment to geomicrobiology research activities in continental drilling. Potential solutions include transportable “bug labs” that can be requested for funded projects.

●      Logistics. Due to the sensitivity of subsurface microbes to oxygen, deep biosphere samples need to be taken immediately after the core is retrieved. Contamination must be checked on-site to determine which samples are suitable for analysis. These requirements make the presence of a geomicrobiology science team on site a prerequisite. This is different from most other disciplines, which can work on cores much later.

●      Financing. With the current project funding structure, several separate grants are needed to see a project to completion. Cores for geomicrobiological analysis cannot be stored unprocessed or partially processed while project PIs seek additional funding. Unlike the IODP, continental drilling lacks a mechanism to support participants on pilot-scale grants as they gather data necessary for successful larger proposals. Overall, the current structure is prone to failure for experienced researchers and is a barrier to entry for early career researchers. The situation impedes the collection of baseline data overall, keeps the geomicrobiology of the deep biosphere in its infancy, and stifles innovation. Potential solutions include:

○      New pathways for funding, from project development to drilling operations to sample analyses, in the form of new programs, new mechanisms to coordinate across existing programs (e.g. IODP and ICDP), and new resource request structures (e.g. Academic Research Fleet and dedicated sample ‘vans’).  

○      Workshops, seminar series, and/or YouTube channels are resources for training early career and new interested PIs (in all fields) to navigate continental drilling projects.

○      Multi-agency funding for multi-disciplinary teams for high-impact research.

●      Integrated Multi-Disciplinary Project Planning. This is a sample- and data-starved field. What we know of the distribution, ecology, phylogeny, and physiology of microbial life in the deep continental subsurface is based on a limited number of studies that comprise a minute fraction of its total habitable volume (4). Collaborations on drilling expeditions to remote locations hamper sample collection, handling, and storage. Analyses are sensitive to environmental conditions and are personnel intensive. A potential solution is for NSF requirements for project planning steps that support and verify logistics, financing, and decision-making to create successful conditions for geomicrobiological research in funded drilling projects.

Suggested Citation

Toner, B., Spear, J., Kiel Reese, B., Sheik, C., Steen, A., 2024. Geomicrobiology Science Planning for Continental Drilling and Coring 2024. https://sites.google.com/umn.edu/csdscienceplanning/home/geomicrobiology-executive-summary

References

(1) Gold, T. 1992. “The Deep Hot Biosphere.” Proc. Natl. Acad. Sci. 89: 6045-6049.

(2) Colman, D.R., S. Poudel, B.W. Stamps, E.S. Boyd and J.R. Spear.  2017. “The Deep Hot Biosphere: Twenty-Five Years of Retrospection.”  Proc. Natl. Acad. Sci., 114(27): 6895-6903.

(3) Bar-On, Y.M., Phillips, R., Milo, R. (2018). The biomass distribution on Earth. PNAS: 115(25), 6506-6511. DOI: 10.1073/pnas.1711842115

(4) Magnabosco, C., L.-H. Lin, H. Dong, M. Bomberg, W. Ghiorse, H. Stan-Lotter, K. Pedersen, T. Kieft, E. van Heerden and T.C. Onstott. 2018. “The Biomass and Biodiversity of the Continental Subsurface.” Nature Geoscience, 11: 707-717.

(5) Barry, P.H., de Moor, J.M., Giovannelli, D. et al. Forearc carbon sink reduces long-term volatile recycling into the mantle. Nature 568, 487–492 (2019). https://doi.org/10.1038/s41586-019-1131-5

(6) Fullerton, K.M., Schrenk, M.O., Yücel, M. et al. Effect of tectonic processes on biosphere–geosphere feedbacks across a convergent margin. Nat. Geosci. 14, 301–306 (2021). https://doi.org/10.1038/s41561-021-00725-0

(7) McPherson, B. 2003. “EarthLab: A Subterranean Laboratory and Observatory to Study Microbial Life, Fluid Flow and Rock Deformation.” National Science Foundation.

(8) Wilkins, M.J., R.A. Daly, P.J. Mouser, R. Trexler, S. Sharma, D.R. Cole, K.C. Wrighton, J.F. Biddle, E.H. Denis, J.K. Fredrickson, T.L. Kieft, T.C. Onstott, L. Peterson, S.M. Pfiffner, T.J. Phelps and M.O. Schrenk. 2014. “Trends and Future Challenges in Sampling the Deep Terrestrial Biosphere.” Frontiers in Microbiology, 5: doi: 10.3389/fmicb.2014.00481

(9) Kieft, T.L., T.C. Onstott, L. Ahonen, V. Aloisi, F.S. Colwell, B. Engelen, S. Fendrihan, E. Gaidos, U. Harms, I. Head, J. Kallmeyer, B. Kiel Reese, L.-H. Lin, P.E. Long, D.P. Moser, H. Mills, P.Sar, D. Schulze-Makuch, H. Stan-Lotter, D. Wagner, P.-L. Wang, F. Westall and M.J. Wilkins. 2015. “Workshop to Develop Deep-life Continental Scientific Drilling Projects.” Scientific Drilling, 19: 43-53.

(10) Sheik, C.S., B. Kiel Reese, K.I. Twing, J.B. Sylvan, S.L. Grim, M.O. Schrenk, M.L. Sogin and F.S. Colwell. “Identification and Removal of Contaminant Sequences from Ribosomal Gene Databases: Lessons From the Census of Deep Life.” Frontiers in Microbiology, 9: doi: 10.3389/fmicb.2018.00840.

Geomicrobiology Working Group

Brandi Kiel Reese, University of South Alabama

Cody Sheik, University of Minnesota Duluth

Andrew Steen, University of Tennessee Knoxville

John Spear, Colorado School of Mines

Brandy Toner, University of Minnesota

Geomicrobiology Community Editors

Chris Ballentine, University of Oxford

Peter H. Barry, Woods Hole Oceanographic Institution

Marco Basili, Institute of Marine Biological Resources and Biotechnologies

Wayne Belcher, United States Geological Survey

Will Berelson, University of Southern California Dornsife

Jennifer Biddle, University of Delaware

Daniel Bond, University of Minnesota

Eric Boyd, Montana State University

James Bradley, Mediterranean Institute of Oceanography

Billy Brazelton, University of Utah

Joy Buongiorno, Maryville College

Frederick Colwell, Oregon State University

Frank Corsetti, University of Southern California Dornsife

Giuseppe d’Errico, Università Politecnica delle Marche

Steve D'Hondt, University of Rhode Island Graduate School of Oceanography

J. Maarten de Moor, Observatorio Vulcanológico y Sismológico de Costa Rica

Aaron Diefendorf, University of Cincinnati

Hailiang Dong, China University of Geosciences-Beijing

William Dowd, Gradient

Bert Engelen, University of Oldenburg

Daniele Fattorini, Università Politecnica delle Marche

Scott Fendorf, Stanford University

Sergiu Fendrihan, Institute of Plant Protection Research and Development

Tobias Fischer, University of New Mexico

Woody Fischer, California Institute of Technology

Chris Francis, Stanford University

Katherine Freeman, Penn State University

Esteban Gazel, Cornell University

Donato Giovannelli, University of Naples “Federico II”

Jennifer Glass, Georgia Institute of Technology

Jeffrey Gralnick, University of Minnesota

Sæmundur Ari Halldórsson, University of Iceland

Scott Hamilton-Brehm, Southern Illinois University

Mark Hausner, Desert Research Institute

Ron Hershey, Desert Research Institute

Tori Hoehler, NASA

Casey Hubert, University of Calgary

Daniel Hummer, Southern Illinois University

Kayla Lacovino, NASA

Gerdhard Jessen, Instituto de Ciencias Marinas y Limnológicas

Jens Kallmeyer, GFZ Potsdam

Peter Kang, University of Minnesota

Thomas Kieft, New Mexico Tech

Sebastian Kopf, University of Colorado Boulder

Brittany Krueger, Desert Research Institute

Justin Kulongoski, United States Geological Survey

Doug LaRowe, University of Southern California Dornsife

Woonghee Lee, University of Minnesota

Karen G. Lloyd, University of Southern California Dornsife

Philip Long, Lawrence Berkeley National Laboratory

Taryn Lopez, University of Alaska Fairbanks

Tim Lyons, University of California Riverside

Jennifer Macalady, Penn State University

María Martínez, Observatorio Vulcanológico y Sismológico de Costa Rica

Jill McDermott, Lehigh University

D'Arcy Meyer-Dombard, University of Illiinois Chicago

Heather Miller, Michigan State University

Shaunna M. Morrison, Carnegie Institution for Science

Duane Moser, Desert Research Institute

Dianne Newman, Caltech

Alison Olcott, University of Kansas

Shuhei Ono, Massachusetts Institute of Technology

Victoria Orphan, Caltech

Magdalena Osburn, Northwestern University

Vicky Petryshyn, University of Southern California Dornsife

Kalen Rasmussen, National Renewable Energy Laboratory

Francesco Regoli, Università Politecnica delle Marche

Chuck Russell, Desert Research Institute

Matthew Schrenk, Michigan State University

Chris Schuler, University of Minnesota

Alex Sessions, Caltech

Russell Shapiro, Sub-Terra Heritage Resource Investigations

Barbara Sherwood Lollar, University of Toronto

Everett Shock, Arizona State University

Katie Snell, University of Colorado Boulder

Gordon Southam, University of Queensland

Trisha Spanbauer, University of Toledo

Ramunas Stepanauskas, Bigelow Laboratory for Ocean Sciences

Bradley Stevenson, Northwestern University

Donald Sweetkind, United States Geological Survey

Jason Sylvan, Texas A&M University

Alexis Templeton, University of Colorado Boulder

Patrick Thieringer, Colorado School of Mines

Jim Thomas, Desert Research Institute

Elizabeth Trembath-Reichert, Arizona State Unviversity

Lizzy Trower, University of Colorado Boulder

Costantino Vetriani, Rutgers University

Michael Wilkins, Colorado State University

Jon Wilson, United States Geological Survey

Boswell Wing, University of Colorado Boulder

Tanja Woyke, Lawrence Berkeley National Laboratory

Mustafa Yücel, Middle East Technical University

Chuanlun Zhang, Southern University of Sciences and Techonlogy China

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