Hydrocarbon seepage in the deep seabed links subsurface and seafloor biospheres

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Significance

The marine subsurface is one of the largest habitats on Earth composed exclusively of microorganisms and harboring on the order of 10 ²⁹ microbial cells. It is unclear if deep subsurface life impacts overlying seafloor diversity and biogeochemical cycling in the deep ocean. We analyzed the microbial communities of 172 seafloor surface sediment samples, including gas and oil seeps as well as sediments not subject to upward fluid flow. A strong correlation between typical subsurface clades and active geofluid seepage suggests that subsurface life is injected into the deep ocean floor at hydrocarbon seeps, a globally widespread hydrogeological phenomenon. This supply of subsurface-derived microbial populations, biomass, and metabolic potential thus increases biodiversity and impacts carbon cycling in the deep ocean.

Abstract

Marine cold seeps transmit fluids between the subseafloor and seafloor biospheres through upward migration of hydrocarbons that originate in deep sediment layers. It remains unclear how geofluids influence the composition of the seabed microbiome and if they transport deep subsurface life up to the surface. Here we analyzed 172 marine surficial sediments from the deep-water Eastern Gulf of Mexico to assess whether hydrocarbon fluid migration is a mechanism for upward microbial dispersal. While 132 of these sediments contained migrated liquid hydrocarbons, evidence of continuous advective transport of thermogenic alkane gases was observed in 11 sediments. Gas seeps harbored distinct microbial communities featuring bacteria and archaea that are well-known inhabitants of deep biosphere sediments. Specifically, 25 distinct sequence variants within the uncultivated bacterial phyla Atribacteria and Aminicenantes and the archaeal order Thermoprofundales occurred in significantly greater relative sequence abundance along with well-known seep-colonizing members of the bacterial genus Sulfurovum, in the gas-positive sediments. Metabolic predictions guided by metagenome-assembled genomes suggested these organisms are anaerobic heterotrophs capable of nonrespiratory breakdown of organic matter, likely enabling them to inhabit energy-limited deep subseafloor ecosystems. These results point to petroleum geofluids as a vector for the advection-assisted upward dispersal of deep biosphere microbes from subsurface to surface environments, shaping the microbiome of cold seep sediments and providing a general mechanism for the maintenance of microbial diversity in the deep sea.

Related collections

Most cited references 38

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Microbial ecology of the dark ocean above, at, and below the seafloor.

Beth N. Orcutt, Jason Sylvan, Nina J Knab … (2011)

The majority of life on Earth--notably, microbial life--occurs in places that do not receive sunlight, with the habitats of the oceans being the largest of these reservoirs. Sunlight penetrates only a few tens to hundreds of meters into the ocean, resulting in large-scale microbial ecosystems that function in the dark. Our knowledge of microbial processes in the dark ocean-the aphotic pelagic ocean, sediments, oceanic crust, hydrothermal vents, etc.-has increased substantially in recent decades. Studies that try to decipher the activity of microorganisms in the dark ocean, where we cannot easily observe them, are yielding paradigm-shifting discoveries that are fundamentally changing our understanding of the role of the dark ocean in the global Earth system and its biogeochemical cycles. New generations of researchers and experimental tools have emerged, in the last decade in particular, owing to dedicated research programs to explore the dark ocean biosphere. This review focuses on our current understanding of microbiology in the dark ocean, outlining salient features of various habitats and discussing known and still unexplored types of microbial metabolism and their consequences in global biogeochemical cycling. We also focus on patterns of microbial diversity in the dark ocean and on processes and communities that are characteristic of the different habitats.

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Biogeographical distribution and diversity of microbes in methane hydrate-bearing deep marine sediments on the Pacific Ocean Margin.

F. Inagaki, T. Nunoura, S. Nakagawa … (2006)

The deep subseafloor biosphere is among the least-understood habitats on Earth, even though the huge microbial biomass therein plays an important role for potential long-term controls on global biogeochemical cycles. We report here the vertical and geographical distribution of microbes and their phylogenetic diversities in deeply buried marine sediments of the Pacific Ocean Margins. During the Ocean Drilling Program Legs 201 and 204, we obtained sediment cores from the Peru and Cascadia Margins that varied with respect to the presence of dissolved methane and methane hydrate. To examine differences in prokaryotic distribution patterns in sediments with or without methane hydrates, we studied >2,800 clones possessing partial sequences (400-500 bp) of the 16S rRNA gene and 348 representative clone sequences (approximately 1 kbp) from the two geographically separated subseafloor environments. Archaea of the uncultivated Deep-Sea Archaeal Group were consistently the dominant phylotype in sediments associated with methane hydrate. Sediment cores lacking methane hydrates displayed few or no Deep-Sea Archaeal Group phylotypes. Bacterial communities in the methane hydrate-bearing sediments were dominated by members of the JS1 group, Planctomycetes, and Chloroflexi. Results from cluster and principal component analyses, which include previously reported data from the West and East Pacific Margins, suggest that, for these locations in the Pacific Ocean, prokaryotic communities from methane hydrate-bearing sediment cores are distinct from those in hydrate-free cores. The recognition of which microbial groups prevail under distinctive subseafloor environments is a significant step toward determining the role these communities play in Earth's essential biogeochemical processes.

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DEEP BIOSPHERE. Exploring deep microbial life in coal-bearing sediment down to ~2.5 km below the ocean floor.

F Inagaki, K-U Hinrichs, Michael D. Y. Kubo … (2015)

Microbial life inhabits deeply buried marine sediments, but the extent of this vast ecosystem remains poorly constrained. Here we provide evidence for the existence of microbial communities in ~40° to 60°C sediment associated with lignite coal beds at ~1.5 to 2.5 km below the seafloor in the Pacific Ocean off Japan. Microbial methanogenesis was indicated by the isotopic compositions of methane and carbon dioxide, biomarkers, cultivation data, and gas compositions. Concentrations of indigenous microbial cells below 1.5 km ranged from <10 to ~10(4) cells cm(-3). Peak concentrations occurred in lignite layers, where communities differed markedly from shallower subseafloor communities and instead resembled organotrophic communities in forest soils. This suggests that terrigenous sediments retain indigenous community members tens of millions of years after burial in the seabed.

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Author and article information

Journal

Journal ID (nlm-ta): Proc Natl Acad Sci U S A

Journal ID (iso-abbrev): Proc. Natl. Acad. Sci. U.S.A

Journal ID (hwp): pnas

Journal ID (pmc): pnas

Journal ID (publisher-id): PNAS

Title: Proceedings of the National Academy of Sciences of the United States of America

Publisher: National Academy of Sciences

ISSN (Print): 0027-8424

ISSN (Electronic): 1091-6490

Publication date (Print): 19 May 2020

Publication date (Electronic): 30 April 2020

Publication date PMC-release: 30 April 2020

Volume: 117

Issue: 20

Pages: 11029-11037

Affiliations

[1] ^aDepartment of Biological Sciences, University of Calgary , Calgary, AB T2N 1N4, Canada;

[2] ^bDepartment of Geoscience, University of Calgary , Calgary, AB T2N 1N4, Canada;

[3] ^cEcosystems Center and J. Bay Paul Center for Comparative Molecular Biology and Evolution, Marine Biological Laboratory , Woods Hole, MA 02543;

[4] ^dSchool of Marine Sciences, Sun Yat-Sen University , 519082 Zhuhai, People's Republic of China;

[5] ^eSouthern Marine Science and Engineering Guangdong Laboratory (Zhuhai) , 519000 Zhuhai, People's Republic of China;

[6] ^fTDI-Brooks International , College Station, TX 77845

Author notes

¹To whom correspondence may be addressed. Email: anirban.chakraborty@ 123456ucalgary.ca or chubert@ 123456ucalgary.ca .

Edited by David M. Karl, University of Hawaii at Manoa, Honolulu, HI, and approved March 26, 2020 (received for review February 6, 2020)

Author contributions: A.C. and C.R.J.H. designed research; A.C., S.E.R., X.D., E.D.E., C.L., J.M.B., and B.B.B. performed research; A.C., S.E.R., X.D., J.M.B., J.M., and B.B.B. analyzed data; and A.C., S.E.R., X.D., and C.R.J.H. wrote the paper.