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2015 Annual Science Report

University of Southern California Reporting  |  JAN 2015 – DEC 2015

Executive Summary

Our multi-disciplinary team from the University of Southern California, California Institute of Technology, Jet Propulsion Lab, Desert Research Institute, Rensselaer Polytechnic Institute, and Northwestern University is developing and employing field, laboratory, and modeling approaches aimed at detecting and characterizing microbial life in the subsurface the intraterrestrials. We posit that if life exists, or ever existed, on Mars or other planetary body in our solar system, evidence thereof would most likely be found in the subsurface. This study takes advantage of unique opportunities to explore the subsurface ecosystems on Earth through bore-holes, mine shafts, sediment coring, marine vents and seeps, and deeply-sourced springs. Access to the subsurface—both continental and marine—and broad characterization of the rocks, fluids, and microbial inhabitants is central to this study. Our focused research themes require subsurface samples for laboratory and in situ experiments. Specifically, we are carrying out in situ life detection, culturing and isolation of heretofore unknown intraterrestrial archaea and bacteria using numerous novel and traditional techniques, and incorporating new and existing data into regional and global metabolic energy models. Here, we provide brief summaries of the main accomplishments in 2015 on our four major research themes: (A) access to the subsurface and broad characterization, (B) in-situ life detection and characterization, © guided cultivation of intraterrestrials, and (D) energy flow and metabolic modeling.

A. Access to the Subsurface and Broad Characterization
In 2015, the Life Underground project built upon our 2014 and prior work at the Sanford Underground Research Facility (SURF) in South Dakota and greatly expanded our work at a borehole site near Death Valley, CA; we also continued ongoing work at an ophiolite site in northern California called ‘the Cedars’. In the marine realm, work continued on samples acquired from the Shimokita Peninsula (Japan) in the northwestern Pacific (IODP Drilling Expedition 337), and collaborations continued with the NSF-funded Science and Technology Center for Dark Energy Biosphere Investigations (C-DEBI), which focuses on the marine subseafloor bio-sphere. For all sites—continental and marine—collections of standardized samples and metadata continued, including: temperature, pH, oxidation-reduction potential, dissolved oxygen, total dissolved solids, aqueous and nutrient chemistry analysis, metal speciation, dissolved gas compositional and isotopic characterizations (δC and δ2H), sulfur and water isotopes (e.g. δ34S and δ2H/δ18O), radiocarbon, organic constituents, electron microscopy, planktonic cell abundance, cultivations, single cell genomics, filters for DNA and lipids, and bulk water for microbial cultivation. We have shifted in focus from our early strategy of preliminary site characterization to one of time series sampling and the establishment of long-term monitoring at the SURF, BLM-1, and the Cedars.

B. In-situ Life Detection and Characterization, and Mission Relevance.
In this theme, we aim to detect and characterize in situ life based on spatial distribution of organics (e.g., microorganisms), minerals, elements and isotopes, in the context of textural features, from the macro to the micro scale. The team uses a number of optical techniques covering the electromagnetic spectrum from the deep UV (<250 nm) to the IR; using an array of spectral phenomena such as absorption, Raman scattering, fluorescence, and reflectance, for noninvasive means of assessing macro to micro structure, organics, minerals, and elements. These methods help refine samples to smaller targets of interest for analysis by more “invasive” but chemically-specific analyses, including phylogenetic identification of microorganisms and community structure to elemental/isotopic analysis using techniques such as nanoSIMS. In 2015, we made substantial progress in a) instrument calibration with cultured archaea and bacteria; b) in situ sample analysis and colonization experiments and development of the macro-to-micro life detection pipeline; c) integration of instrumentation aligned with the Mars 2020 payload and field testing; d) in situ field deployments at SURF, BLM-1, and the Cedars; and e) deep subseafloor sampling and stable isotope probing experiments.

C. Guided Cultivation of Intraterrestrials.
Since the characterization of the subsurface biosphere is often challenging because many resident microbes appear ‘unculturable’ using traditional growth methods, we are focused on developing and harnessing new cultivation and enrichment techniques that go beyond these traditional limitations. Our approaches have been applied both in situ and ex situ to mimic the complex interactions and energetic gradients present in the NAI field sites, in order to reveal the full diversity of subsurface microorganisms. During this reporting period, we made progress on several fronts regarding cultivation. Down-flow hanging sponge reactors were used to investigate microbial communities in porous media, and at least two novel bacteria were isolated—one in the genus Thermincola and one in the family Spirochaetaceae. During this reporting period, several other bacteria were isolated from biomass associated with electrode cultivation. The extracellular electron transfer abilities of the isolated Delftia strain and Azonexus strain were confirmed in electrochemical reactors using working electrodes. Both genera were previously observed in mixed communities of microbial fuel cell enrichments, but this is the first direct measurement of their electrochemical activity. In addition to our laboratory-based efforts, we designed, constructed, and deployed an in situ electrode cultivation (ISEC) bioreactor. This experimental system, which is the first of its kind, was deployed at 4850 ft below the surface, fed with water from legacy hole 3A at SURF. Lastly, we have also constructed and instrumented gradient chambers with electrodes that can be independently poised to precise potential to serve either as anode or cathode to support bioenergetics. With this system, we investigated the production of biogenic minerals using the dissimilatory iron-reducing bacterium, Shewanella oneidensis as the catalytic agent.

D. Energy Flow and Metabolic Modeling.
Several projects in this theme made significant advances in 2015. We finished studies and published papers in peer-reviewed journals on a) the quantitative relationship between rates of microbial catalysis, energy supply and demand, and population size; b) the power limits of microbial life; c) a new view of extremophiles that specifically considers energetics; d) energy calculations of chemolithotrophic reactions in a hydrothermal system; e) the energetics of anabolism across a range of physico-chemical conditions; and f) a modeling effort of microbial limitations going back to the time of life’s emergence on Earth more than 3.5 billion years ago.

Team-level outcomes made possible by NAI processes
Several achievements in 2015 were enabled by NAI processes. Although, we did not receive a DDF award, the proposal call initiated an exciting discussion between members of the Rock-Powered Life and Life Underground teams on predicting subsurface metabolic strategies based on water-rock interactions. The collaboration between these two NAI teams was also strengthened by the serpentinization synergy research theme led by Ken Nealson and Alexis Templeton. Lastly, at the in-person Executive Council meeting at USC in 2015, graduate student Lily Momper of the Life Underground team met Roger Summons, PI of the Foundations of Complex Life team. Consequently, Momper was invited to MIT for some sample analysis, which led to further discussion regarding a post-doc opportunity, and an NPP proposal that was recently selected for funding.

Publications

  • Bhartia, R., W.H. Hug, R.Reid, L. Beegle. (2015). Explosives Detection and Analysis by Fusing Deep UV Native Fluorescence and Resonance Raman Spectroscopy. In E. L. H. P.M. Pellegrino, M.E. Ferrell (Ed.), Laser-based Optical Detection methods of Explosives. Boca Raton, FL: Taylor & Francis Group.
  • Marlow, J., & Amend, J. (2015). The Energy of Life. Scientist, 29(2), 40-47.

  • (no authors found) (2015). PERSPECTIVE. Elements, 11(6), 384–385. doi:10.2113/gselements.11.6.384

  • Case, D. H., Pasulka, A. L., Marlow, J. J., Grupe, B. M., Levin, L. A., & Orphan, V. J. (2015). Methane Seep Carbonates Host Distinct, Diverse, and Dynamic Microbial Assemblages. mBio, 6(6), e01348–15. doi:10.1128/mbio.01348-15

  • Dawson, K. S., Osburn, M. R., Sessions, A. L., & Orphan, V. J. (2015). Metabolic associations with archaea drive shifts in hydrogen isotope fractionation in sulfate-reducing bacterial lipids in cocultures and methane seeps. Geobiology, 13(5), 462–477. doi:10.1111/gbi.12140

  • Gross, B. J., & El-Naggar, M. Y. (2015). A combined electrochemical and optical trapping platform for measuring single cell respiration rates at electrode interfaces. Review of Scientific Instruments, 86(6), 064301. doi:10.1063/1.4922853

  • Inskeep, W. P., Jay, Z. J., MacUr, R. E., Clingenpeel, S., Tenney, A., Lovalvo, D., … Nealson, K. (2015). Geomicrobiology of sublacustrine thermal vents in Yellowstone Lake: geochemical controls on microbial community structure and function. Frontiers in Microbiology, 6. doi:10.3389/fmicb.2015.01044

  • Ishii, S. i., Suzuki, S., Tenney, A., Norden-Krichmar, T. M., Nealson, K. H., & Bretschger, O. (2015). Microbial metabolic networks in a complex electrogenic biofilm recovered from a stimulus-induced metatranscriptomics approach. Scientific Reports, 5, 14840. doi:10.1038/srep14840

  • LaRowe, D. E., & Amend, J. P. (2015). Catabolic rates, population sizes and doubling/replacement times of microorganisms in natural settings. American Journal of Science, 315(3), 167–203. doi:10.2475/03.2015.01

  • LaRowe, D. E., & Amend, J. P. (2015). Power limits for microbial life. Frontiers in Microbiology, 6. doi:10.3389/fmicb.2015.00718

  • Li, S-L., & Nealson, K. H. (2015). Enriching distinctive microbial communities from marine sediments via an electrochemical-sulfide-oxidizing process on carbon electrodes. Frontiers in Microbiology, 6. doi:10.3389/fmicb.2015.00111

  • Lin, H-T., Amend, J. P., LaRowe, D. E., Bingham, J-P., & Cowen, J. P. (2015). Dissolved amino acids in oceanic basaltic basement fluids. Geochimica et Cosmochimica Acta, 164, 175–190. doi:10.1016/j.gca.2015.04.044

  • Marlow, J., Peckmann, J., & Orphan, V. (2015). Autoendoliths: a distinct type of rock-hosted microbial life. Geobiology, 13(4), 303–307. doi:10.1111/gbi.12131

  • Mason, O. U., Case, D. H., Naehr, T. H., Lee, R. W., Thomas, R. B., Bailey, J. V., & Orphan, V. J. (2015). Comparison of Archaeal and Bacterial Diversity in Methane Seep Carbonate Nodules and Host Sediments, Eel River Basin and Hydrate Ridge, USA. Microbial Ecology, 70(3), 766–784. doi:10.1007/s00248-015-0615-6

  • McFarlane, I. R., Lazzari-Dean, J. R., & El-Naggar, M. Y. (2015). Field effect transistors based on semiconductive microbially synthesized chalcogenide nanofibers. Acta Biomaterialia, 13, 364–373. doi:10.1016/j.actbio.2014.11.005

  • McGlynn, S. E., Chadwick, G. L., Kempes, C. P., & Orphan, V. J. (2015). Single cell activity reveals direct electron transfer in methanotrophic consortia. Nature, 526(7574), 531–535. doi:10.1038/nature15512

  • Nakano, C. M., Byun, H. S., Ma, H., Wei, T., & El-Naggar, M. Y. (2015). A framework for stochastic simulations and visualization of biological electron-transfer dynamics. Computer Physics Communications, 193, 1–9. doi:10.1016/j.cpc.2015.03.009

  • Nealson, K. H. (2015). Ex-phot: a new take on primitive utilization of solar energy. Environmental Microbiology Reports, 7(1), 33–35. doi:10.1111/1758-2229.12256

  • Osburn, M. R., Owens, J., Bergmann, K. D., Lyons, T. W., & Grotzinger, J. P. (2015). Dynamic changes in sulfate sulfur isotopes preceding the Ediacaran Shuram Excursion. Geochimica et Cosmochimica Acta, 170, 204–224. doi:10.1016/j.gca.2015.07.039

  • Price, R. E., LaRowe, D. E., Italiano, F., Savov, I., Pichler, T., & Amend, J. P. (2015). Subsurface hydrothermal processes and the bioenergetics of chemolithoautotrophy at the shallow-sea vents off Panarea Island (Italy). Chemical Geology, 407-408, 21–45. doi:10.1016/j.chemgeo.2015.04.011

  • Robador, A., Jungbluth, S. P., LaRowe, D. E., Bowers, R. M., Rappé, M. S., Amend, J. P., & Cowen, J. P. (2015). Activity and phylogenetic diversity of sulfate-reducing microorganisms in low-temperature subsurface fluids within the upper oceanic crust. Frontiers in Microbiology, 5. doi:10.3389/fmicb.2014.00748

  • 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

  • Skennerton, C. T., Ward, L. M., Michel, A., Metcalfe, K., Valiente, C., Mullin, S., … Orphan, V. J. (2015). Genomic Reconstruction of an Uncultured Hydrothermal Vent Gammaproteobacterial Methanotroph (Family Methylothermaceae) Indicates Multiple Adaptations to Oxygen Limitation. Frontiers in Microbiology, 6. doi:10.3389/fmicb.2015.01425

  • Stern, J. C., Sutter, B., Freissinet, C., Navarro-González, R., McKay, C. P., Archer, P. D., … Mahaffy, P. R. (2015). Evidence for indigenous nitrogen in sedimentary and aeolian deposits from the Curiosity rover investigations at Gale crater, Mars. Proc Natl Acad Sci USA, 112(14), 4245–4250. doi:10.1073/pnas.1420932112

  • Sylvan, J. B., Amend, J. P., Momper, L. M., Edwards, K. J., Toner, B. M., & Hoffman, C. L. (2015). Bacillus rigiliprofundi sp. nov., an endospore-forming, Mn-oxidizing, moderately halophilic bacterium isolated from deep subseafloor basaltic crust. International Journal of Systematic and Evolutionary Microbiology, 65(6), 1992–1998. doi:10.1099/ijs.0.000211

  • Thacher, R., Hsu, L., Ravindran, V., Nealson, K. H., & Pirbazari, M. (2015). Modeling the transport and bioreduction of hexavalent chromium in aquifers: Influence of natural organic matter. Chemical Engineering Science, 138, 552–565. doi:10.1016/j.ces.2015.08.011

  • White, L. M., Bhartia, R., Stucky, G. D., Kanik, I., & Russell, M. J. (2015). Mackinawite and greigite in ancient alkaline hydrothermal chimneys: Identifying potential key catalysts for emergent life. Earth and Planetary Science Letters, 430, 105–114. doi:10.1016/j.epsl.2015.08.013

  • Inagaki, F., Hinrichs, K-U., Kubo, Y., Bowles, M. W., Heuer, V. B., Hong, W-L., … Yamada, Y. (2015). Exploring deep microbial life in coal-bearing sediment down to  2.5 km below the ocean floor. Science, 349(6246), 420–424. doi:10.1126/science.aaa6882

  • Kieft, T. L., Onstott, T. C., Ahonen, L., Aloisi, V., Colwell, F. S., Engelen, B., … Wilkins, M. J. (2015). Workshop to develop deep-life continental scientific drilling projects. Sci. Dril., 19, 43–53. doi:10.5194/sd-19-43-2015

  • LaRowe, D. E., & Amend, J. P. (2016). The energetics of anabolism in natural settings. The ISME Journal, 10(6), 1285–1295. doi:10.1038/ismej.2015.227

  • McKay, L., Klokman, V. W., Mendlovitz, H. P., LaRowe, D. E., Hoer, D. R., Albert, D., … Teske, A. (2016). Thermal and geochemical influences on microbial biogeography in the hydrothermal sediments of Guaymas Basin, Gulf of California. Environmental Microbiology Reports, 8(1), 150–161. doi:10.1111/1758-2229.12365

  • Salas, E. C., Bhartia, R., Anderson, L., Hug, W. F., Reid, R. D., Iturrino, G., & Edwards, K. J. (2015). In situ Detection of Microbial Life in the Deep Biosphere in Igneous Ocean Crust. Frontiers in Microbiology, 6. doi:10.3389/fmicb.2015.01260