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2014 Annual Science Report

University of Southern California Reporting  |  SEP 2013 – DEC 2014

Executive Summary

Our cross-disciplinary team from the University of Southern California, the California Institute of Technology, the Jet Propulsion Laboratory, the Desert Research Institute, the Rensselaer Polytechnic Institute, and now also Northwestern University is developing and employing field, laboratory, and modeling approaches to detect and characterize microbial life in the subsurface. On Earth, microorganisms appear to inhabit all space that provides the minimum requirements for life. These include the availability of water, carbon, nutrients, and light or chemical energy. While these are generally abundant in surface or near-surface environments, their mode and distribution in the subsurface are poorly constrained. Nevertheless, it has been shown that archaea and bacteria inhabit deeply buried rocks and sediments where they contribute to biogeochemical cycles. On other planets in our solar system, putative extant or extinct life would most likely be found underground. With a focus on near-by planets where landed missions are more than just a possibility, access to the subsurface will be highly desirable. Robust strategies for subsurface life detection on Mars, Europa, or other potential targets are poorly developed. The search for extant life or its biosignatures is scientifically and technologically extremely difficult; on Earth, it is a formidable but tractable challenge.

To expand our understanding of the subsurface biosphere on Earth and to inform future exploration of subsurface ecosystems elsewhere, our Life Underground project focuses on several accessible and geologically diverse subsurface sites, both continental and marine. In 2014, we had major accomplishments in each of our four main research themes. Theme 1—Access to the subsurface: sampling and other field operations were carried out at the Sanford Underground Research Facility (SURF) in South Dakota, including the drilling and coring of four new holes (145-343 m in length) on the 4850-foot level of the mine; a borehole (BLM-1) in the Great Basin near Death Valley, including two-month-long incubations at several depths with a range of physical substrates; the deeply-sourced springs at the Cedars in northern California; and shale beds, sandstones, and coal seams down to 2.2 km below the seafloor off the Shimokita Peninsula (Japan). Theme 2—In situ life detection and characterization, including mission relevance: further development of a deep UV Raman/fluorescence technique for the analysis of minerals, organics, and possibly microbial cells; selection of this technique as a flight instrument (SHER-LOC) for the upcoming Mars mission; and optimization of our macro-to-micro life detection and characterization pipeline, including new sample collection protocol, analysis software, and data handling from various instruments over a series of spatial scales. Theme 3—Guided cultivation of intraterrestrials: construction and operation of down-flow hanging sponge bioreactors, including the enrichment of a Thaumarchaeon, which is a group of microorganisms we know very little about and for which only a couple of isolates are currently culturable; development and use of the first electrode cultivation reactor targeting subsurface microorganisms; development and deployment of the first-ever in situ electrode cultivation bioreactor (operating at the 4850-foot level at SURF); isolation and characterization of an extremely high pH-loving organism from the Cedars (Serpentinomonas); and successful application of a new electrode cultivation technique to isolate microbes from marine sediments. Theme 4—Energy flow and metabolic modeling: development of global models of the distribution of water, organic carbon, temperature, and pore space in marine sediments; calculations of the power limits of microbial life in low energy environments; computations of chemolithotrophic reaction energetics in several sub-surface environments; and modeling of limitations on bacterial body size, cellular composition, and evolution.

Publications

  • Gilhooly, W. P., Fike, D. A., Druschel, G. K., Kafantaris, F-C., Price, R. E., & Amend, J. P. (2014). Sulfur and oxygen isotope insights into sulfur cycling in shallow-sea hydrothermal vents, Milos, Greece. Geochemical Transactions, 15(1), None. doi:10.1186/s12932-014-0012-y

  • LaRowe, D. E., Dale, A. W., Aguilera, D. R., L’Heureux, I., Amend, J. P., & Regnier, P. (2014). Modeling microbial reaction rates in a submarine hydrothermal vent chimney wall. Geochimica et Cosmochimica Acta, 124, 72–97. doi:10.1016/j.gca.2013.09.005

  • Marlow, J. J., LaRowe, D. E., Ehlmann, B. L., Amend, J. P., & Orphan, V. J. (2014). The Potential for Biologically Catalyzed Anaerobic Methane Oxidation on Ancient Mars. Astrobiology, 14(4), 292–307. doi:10.1089/ast.2013.1078

  • Marlow, J. J., Steele, J. A., Case, D. H., Connon, S. A., Levin, L. A., & Orphan, V. J. (2014). Microbial abundance and diversity patterns associated with sediments and carbonates from the methane seep environments of Hydrate Ridge, OR. Frontiers in Marine Science, 1. doi:10.3389/fmars.2014.00044

  • Marlow, J. J., Steele, J. A., Ziebis, W., Thurber, A. R., Levin, L. A., & Orphan, V. J. (2014). Carbonate-hosted methanotrophy represents an unrecognized methane sink in the deep sea. Nat Comms, 5, 5094. doi:10.1038/ncomms6094

  • Meyer-Dombard, D. A. R., & Amend, J. P. (2014). Geochemistry and microbial ecology in alkaline hot springs of Ambitle Island, Papua New Guinea. Extremophiles, 18(4), 763–778. doi:10.1007/s00792-014-0657-6

  • Okamoto, A., Hashimoto, K., & Nealson, K. H. (2014). Flavin Redox Bifurcation as a Mechanism for Controlling the Direction of Electron Flow during Extracellular Electron Transfer. Angew. Chem. Int. Ed., 53(41), 10988–10991. doi:10.1002/anie.201407004

  • Okamoto, A., Kalathil, S., Deng, X., Hashimoto, K., Nakamura, R., & Nealson, K. H. (2014). Cell-secreted Flavins Bound to Membrane Cytochromes Dictate Electron Transfer Reactions to Surfaces with Diverse Charge and pH. Scientific Reports, 4. doi:10.1038/srep05628

  • Okamoto, A., Nakamura, R., Nealson, K. H., & Hashimoto, K. (2014). Bound Flavin Model Suggests Similar Electron-Transfer Mechanisms in Shewanella and Geobacter. CHEMELECTROCHEM, 1(11), 1808–1812. doi:10.1002/celc.201402151

  • Orcutt, B. N., & Edwards, K. J. (2014). Life in the Ocean Crust. Developments in Marine Geology, None, 175–196. doi:10.1016/b978-0-444-62617-2.00007-4

  • Osburn, M. R., LaRowe, D. E., Momper, L. M., & Amend, J. P. (2014). Chemolithotrophy in the continental deep subsurface: Sanford Underground Research Facility (SURF), USA. Frontiers in Microbiology, 5. doi:10.3389/fmicb.2014.00610

  • Rowe, A. R., Chellamuthu, P., Lam, B., Okamoto, A., & Nealson, K. H. (2015). Marine sediments microbes capable of electrode oxidation as a surrogate for lithotrophic insoluble substrate metabolism. Frontiers in Microbiology, 5. doi:10.3389/fmicb.2014.00784

  • Suzuki, S., Kuenen, J. G., Schipper, K., Van Der Velde, S., Ishii, S. i., Wu, A., … Nealson, K. H. (2014). Physiological and genomic features of highly alkaliphilic hydrogen-utilizing Betaproteobacteria from a continental serpentinizing site. Nat Comms, 5. doi:10.1038/ncomms4900

  • Takai, K., Nakamura, K., LaRowe, D., & Amend, J. P. (2014). Life at Subseafloor Extremes. Developments in Marine Geology, None, 149–174. doi:10.1016/b978-0-444-62617-2.00006-2

  • Torres, M. A., West, A. J., & Nealson, K. (2014). Microbial Acceleration of Olivine Dissolution via Siderophore Production. Procedia Earth and Planetary Science, 10, 118–122. doi:10.1016/j.proeps.2014.08.041