Virginia Edgcomb from the Woods Hole Oceanographic Institution discusses deep ocean drilling, a process that reveals earth history, geological processes and a deep biosphere
The marine deep subsurface includes sedimentary and rocky horizons both tightly connected to the ocean via circulation through the crust over geological timescales. The International Ocean Discovery Program (IODP) and its predecessor programs since the 1960s have significantly expanded our knowledge about the deep ocean, Earth history, subsurface geology, and the buried deep biosphere.
Its impact is illustrated by examples of the breadth of contributions in 2020 alone, which include the discovery of viable cells in nutrient-poor 4.3-101.5 million years old subsurface sediments below the South Pacific Gyre that may have survived in a state of suspended animation over such timeframes (Morono et al. 2020). We learned how the carbon cycle and global climate have been interacting over the last 35 million years (De Vleeschouwer et al. 2020) and how multiple catastrophic ice discharges into the North Pacific contributed to, and maybe triggered hemispheric-scale changes to Earth’s climate during the last ice age (Walczak et al. 2020). More than five decades of data produced an unprecedented understanding of variability in Earth’s climate over the last 66 million years (Westerhold et al. 2020).
My interests focus on the deep microbial biosphere. In subsurface realms, microorganisms must cope with many challenges, including increasing temperatures and pressures, access to fluids and pore spaces, and limited availability of sources of carbon and energy. The lithified subsurface is relatively unexplored regarding microbial life compared to sedimentary realms. The National Science Foundation (NSF) has supported investigations by my laboratory of deep biosphere samples from around the world, and I was fortunate to sail on two IODP expeditions as a shipboard scientist, one to the Indian Ocean, and one to Guaymas Basin, Mexico.
Investigations of subsurface sediments from diverse locations revealed the presence of complex and metabolically active microbial communities, including representatives from all three domains of life down to >2-2.5 km below the seafloor (e.g., Inagaki et al. 2015). IODP Expedition 385 in 2019 to the Gulf of California, Mexico, was the first to drill directly into subsurface sediments and sediment-hosted basalt sill intrusions of an active hydrothermal basin. This provided a direct microbiological window into a deep hydrothermal biosphere across an active plate spreading centre where complex hydrocarbons are generated by heating of buried organic matter under temperature and pressure. Analyses of these samples are ongoing.
We aim to learn 1) how abundance, diversity, and distribution of fungi and co-inhabiting bacteria and archaea changes in samples exhibiting a wide range of in situ temperatures, available nutrients and pressure, 2) what is the active fraction of cells along these gradients, 3) how do Fungi impact carbon cycling in this biosphere and 4) whether/how fungi and bacteria metabolically interact to break down hydrocarbon substrates predicted to be available. Our methods include culturing fungal isolates by Gaëtan Burgaud at the University of Brest, analyses of active cells using biorthogonal non-cannonical amino acid tagging (BONCAT) by Roland Hatzenpichler at MSU, analysis of fungal lipid biomarkers by Florence Schubotz at the University of Bremen, cell counts and associated microscopy by Yuki Morono at KOCHI/JAMSTEC, Japan and genomics, stable isotope probing, and culture-based studies of microbial metabolites and hydrocarbon degradation (my lab and colleagues).
The rocky deep biosphere: the case of lower ocean crust at Atlantis Bank
Investigations of the igneous basement are fewer and reveal microbial communities that include uncharacterised taxa with metabolic strategies and impacts on global biogeochemical cycles that remain poorly constrained. This hinders our understanding of contributions of the deep biosphere to global carbon cycling. Because the lower crust typically underlies up to thousands of meters of continental crust, marine sediments and/or basalts of the upper crust, Earth’s lower oceanic crust is more difficult to access. IODP Expedition 360 to the Atlantis Bank Oceanic Core Complex on the SW Indian Ridge, Indian Ocean provided a window into this realm.
The Atlantis Bank exposes the largest known gabbro complex in the oceans in only ~700m of water, providing unique drilling access to this otherwise largely inaccessible realm. Jason Sylvan (Texas A&M University) and I sailed as shipboard microbiologists and conducted the first exploration of the lower oceanic crust to combine enzyme assays, cell counts, microscopy, culture-based, and DNA, RNA, and lipid biomarker approaches. We learned there is a heterogeneously-distributed, low-biomass community that includes active cells that compete for limited and sporadically-available resources, have adaptations for withstanding long periods of austerity, and are likely efficient recyclers of available organic matter (Li et al. 2020). Communities include microbial Fungi, whose biosignatures and/or cultured representatives were recovered from the basaltic upper ocean crust (Ivarsson et al. 2016) and now the gabbroic lower ocean crust (Quémener et al. 2020).
Future work
We are learning that deep biosphere microbial Fungi participate in the degradation of refractory organics and cycling of metals and produce novel metabolites with interesting properties. Future studies of the deep biosphere will inform on origins of life on Earth, the extent of marine carbon cycling, limits of life, how life adapts to environmental change, and on potential biomarkers for detecting life in extraterrestrial analogue habitats.
References
De Vleeschouwer, D., Drury, A.J., Vahlenkamp, M., Rochholz, F., Liebrand, D., Palike, H. 2020. High-latitude biomes and rock weathering mediate climate-carbon cycle feedbacks on eccentricity timescales. Nature Communications doi:10.1038/s41467-020-18733-w.
Inagaki, F., Hinrichs, K.-U., Kubo, Y., Boles, M.W., Heuer, V.B., Long, W.-L., Hoshino, T., Ijiri, A., Imachi, H., Ito, M., et al. 2015. Exploring deep marine microbial life in coal-bearing sediment down to ~2.5 km below the ocean floor. Science 349:420-424.
Ivarsson, M., Bengtson, S., and Neubeck, A. 2016. The igneous oceanic crust – Earth’s largest fungal habitat? Fungal Ecology 20: 249–255.
Li, J., *Mara, P., Schubotz, F., Sylvan, J.B., Burgaud, G., Klein, F., Beaudoin, D., Wee, S.-Y., Dick, H., Lott, S., Cox, R., Meyer, L.A.E., Quemener, M., Blackman, D.K., Edgcomb, V.P. 2020. Recycling and metabolic flexibility dictate life in the lower oceanic crust. Nature, https://nature.com/articles/s41586-020-2075-5, doi:10.1038/s41586-020-2075-5
Morono, Y., Ito, M., Hoshino, T., Terada, T., Hori, T., Ikehara, M., D’Hondt, S., Inagaki, F. 2020. Aerobic microbial life persists in oxic marine sediment as old as 101.5 million years. Nature Communications 11, 3626, doi: 10.1038/s41467-020-17330-1.
Quemener, M., Mara, P., Schubotz, F., Beaudoin, D., Li, W., Pachiadaki, M., Sehein, T., Sylvan, J., Barbier, G., Edgcomb, V., Burgaud, G. 2020. Meta-omics highlights the diversity, activity and adaptations of fungi in deep oceanic crust. Environmental Microbiology, doi:10.1111/1462-2920.15181.
Walczak, M.H., Mix, A.C., Cowan, E.A., Fallon, S., Fifield, L.K., Alder, J.R. 2020. Phasing of millennial-scale climate variability in the Pacific and Atlantic Oceans. Science 370(6517):716-720.
Westerhold, T., Marwan, N., Drury, A.J., Liebrand, D., Agnini, C., Anagnostou, E., Barnet, J.S.K., Bohaty, S.M., De Vleeschouwer, D., Florindo, F. 2020. An astronomically dated record of Earth’s climate and its predictability over the last 66 million years. Science 369(6509):1383-1387.
*Please note: This is a commercial profile
