Lipid analysis of CO2-rich subsurface aquifers suggests an autotrophy-based deep biosphere with lysolipids enriched in CPR bacteria

Probst, Alexander J.; Elling, Felix J.; Castelle, Cindy J.; Zhu, Qingzeng; Elvert, Marcus; Birarda, Giovanni; Holman, Hoi-Ying N.; Lane, Katherine R.; Ladd, Bethany; Ryan, M. Cathryn; Woyke, Tanja; Hinrichs, Kai-Uwe; Banfield, Jillian F.

doi:10.1038/s41396-020-0624-4

Title: Lipid analysis of CO₂-rich subsurface aquifers suggests an autotrophy-based deep biosphere with lysolipids enriched in CPR bacteria

Journal Article · 13 March 2020 · The ISME Journal

DOI: https://doi.org/10.1038/s41396-020-0624-4 · OSTI ID:1634086

^[1];

^[2]; Castelle, Cindy J. ^[3]; Zhu, Qingzeng ^[4];

^[4];

^[5]; Holman, Hoi-Ying N. ^[6]; Lane, Katherine R. ^[7]; Ladd, Bethany ^[8]; Ryan, M. Cathryn ^[9];

^[10]; Hinrichs, Kai-Uwe ^[4];

^[7]

Univ. of California, Berkeley, CA (United States); Univ. of Duisburg-Essen (Germany)
Univ. of Bremen (Germany); Harvard Univ., Cambridge, MA (United States)
Univ. of California, Berkeley, CA (United States); Univ. of Bremen (Germany)
Univ. of Bremen (Germany)
Elettra-Sincrotrone Treiste (Italy); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Univ. of California, Berkeley, CA (United States)
Univ. of British Columbia, Vancouver, BC (Canada); Univ. of Calgary, AB (Canada)
Univ. of Calgary, AB (Canada)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)

Sediment-hosted CO₂-rich aquifers deep below the Colorado Plateau (USA) contain a remarkable diversity of uncultivated microorganisms, including Candidate Phyla Radiation (CPR) bacteria that are putative symbionts unable to synthesize membrane lipids. The origin of organic carbon in these ecosystems is unknown and the source of CPR membrane lipids remains elusive. We collected cells from deep groundwater brought to the surface by eruptions of Crystal Geyser, sequenced the community, and analyzed the whole community lipidome over time. Characteristic stable carbon isotopic compositions of microbial lipids suggest that bacterial and archaeal CO₂ fixation ongoing in the deep subsurface provides organic carbon for the complex communities that reside there. Coupled lipidomic-metagenomic analysis indicates that CPR bacteria lack complete lipid biosynthesis pathways but still possess regular lipid membranes. These lipids may therefore originate from other community members, which also adapt to high in situ pressure by increasing fatty acid unsaturation. An unusually high abundance of lysolipids attributed to CPR bacteria may represent an adaptation to membrane curvature stress induced by their small cell sizes. Our findings provide new insights into the carbon cycle in the deep subsurface and suggest the redistribution of lipids into putative symbionts within this community.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC); Sloan Foundation; German Research Foundation (DFG); Canadian National Science and Engineering Research Council

Grant/Contract Number:: AC02-05CH11231; G-2016-20166041; DFG PR 1603/1-1; 06509-2016

OSTI ID:: 1634086

Journal Information:: The ISME Journal, Vol. 14, Issue 6; ISSN 1751-7362

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 16 works

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Concentrations, fractional abundance, and characteristics of intact polar lipids in lipid extracts obtained by filtering eruption fluids from Crystal Geyser, sample CG09 Probst, Alexander J.; Elling, Felix J.; Castelle, C. J. PANGAEA - Data Publisher for Earth & Environmental Science https://doi.org/10.1594/pangaea.914894	dataset	January 2020
Concentrations, fractional abundance, and characteristics of intact polar lipids in lipid extracts obtained by filtering eruption fluids from Crystal Geyser, sample CG19 Probst, Alexander J.; Elling, Felix J.; Castelle, C. J. PANGAEA - Data Publisher for Earth & Environmental Science https://doi.org/10.1594/pangaea.914899	dataset	January 2020
Concentrations, fractional abundance, and characteristics of intact polar lipids in lipid extracts obtained by filtering eruption fluids from Crystal Geyser, sample CG17 Probst, Alexander J.; Elling, Felix J.; Castelle, C. J. PANGAEA - Data Publisher for Earth & Environmental Science https://doi.org/10.1594/pangaea.914898	dataset	January 2020
Concentrations, fractional abundance, and characteristics of intact polar lipids in lipid extracts obtained by filtering eruption fluids from Crystal Geyser, sample CG07 Probst, Alexander J.; Elling, Felix J.; Castelle, C. J. PANGAEA - Data Publisher for Earth & Environmental Science https://doi.org/10.1594/pangaea.914893	dataset	January 2020
Concentrations, fractional abundance, and characteristics of intact polar lipids in lipid extracts obtained by filtering eruption fluids from Crystal Geyser, sample CG05 Probst, Alexander J.; Elling, Felix J.; Castelle, C. J. PANGAEA - Data Publisher for Earth & Environmental Science https://doi.org/10.1594/pangaea.914892	dataset	January 2020
Concentrations, fractional abundance, and characteristics of intact polar lipids in lipid extracts obtained by filtering eruption fluids from Crystal Geyser, sample CG03 Probst, Alexander J.; Elling, Felix J.; Castelle, C. J. PANGAEA - Data Publisher for Earth & Environmental Science https://doi.org/10.1594/pangaea.914891	dataset	January 2020
Genome‐inferred spatio‐temporal resolution of an uncultivated Roizmanbacterium reveals its ecological preferences in groundwater Geesink, Patricia; Wegner, Carl‐Eric; Probst, Alexander J. Environmental Microbiology, Vol. 22, Issue 2 https://doi.org/10.1111/1462-2920.14865	journal	December 2019
Hydrological data from Crystal Geyser, Utah, USA, determined with levelogger 2 Probst, Alexander J.; Elling, Felix J.; Castelle, C. J. PANGAEA - Data Publisher for Earth & Environmental Science https://doi.org/10.1594/pangaea.914864	dataset	January 2020
Hydrological data from Crystal Geyser, Utah, USA, determined with levelogger 1 Probst, Alexander J.; Elling, Felix J.; Castelle, C. J. PANGAEA - Data Publisher for Earth & Environmental Science https://doi.org/10.1594/pangaea.914863	dataset	January 2020
Concentrations, fractional abundance, and characteristics of intact polar lipids in lipid extracts obtained by filtering eruption fluids from Crystal Geyser, sample CG23 Probst, Alexander J.; Elling, Felix J.; Castelle, C. J. PANGAEA - Data Publisher for Earth & Environmental Science https://doi.org/10.1594/pangaea.914901	dataset	January 2020
Carbon isotopic composition of dissolved inorganic carbon and IPL-derived fatty acids and phytane in lipid extracts obtained by filtering eruption fluids from Crystal Geyser Probst, Alexander J.; Elling, Felix J.; Castelle, C. J. PANGAEA - Data Publisher for Earth & Environmental Science https://doi.org/10.1594/pangaea.914989	dataset	January 2020
Concentrations, fractional abundance, and characteristics of intact polar lipids in lipid extracts obtained by filtering eruption fluids from Crystal Geyser, sample CG21 Probst, Alexander J.; Elling, Felix J.; Castelle, C. J. PANGAEA - Data Publisher for Earth & Environmental Science https://doi.org/10.1594/pangaea.914900	dataset	January 2020
Concentrations of IPL-derived fatty acids and phytane in lipid extracts obtained by filtering eruption fluids from Crystal Geyser Probst, Alexander J.; Elling, Felix J.; Castelle, C. J. PANGAEA - Data Publisher for Earth & Environmental Science https://doi.org/10.1594/pangaea.914988	dataset	January 2020
Sampling information from Crystal Geyser, Utah, USA Probst, Alexander J.; Elling, Felix J.; Castelle, C. J. PANGAEA - Data Publisher for Earth & Environmental Science https://doi.org/10.1594/pangaea.914865	dataset	January 2020
Concentrations, fractional abundance, and characteristics of intact polar lipids in lipid extracts obtained by filtering eruption fluids from Crystal Geyser, sample CG29 Probst, Alexander J.; Elling, Felix J.; Castelle, C. J. PANGAEA - Data Publisher for Earth & Environmental Science https://doi.org/10.1594/pangaea.914904	dataset	January 2020
Concentrations, fractional abundance, and characteristics of intact polar lipids in lipid extracts obtained by filtering eruption fluids from Crystal Geyser, sample CG25 Probst, Alexander J.; Elling, Felix J.; Castelle, C. J. PANGAEA - Data Publisher for Earth & Environmental Science https://doi.org/10.1594/pangaea.914903	dataset	January 2020
Concentrations, fractional abundance, and characteristics of intact polar lipids in lipid extracts obtained by filtering eruption fluids from Crystal Geyser, sample CG24 Probst, Alexander J.; Elling, Felix J.; Castelle, C. J. PANGAEA - Data Publisher for Earth & Environmental Science https://doi.org/10.1594/pangaea.914902	dataset	January 2020
An archaeal symbiont-host association from the deep terrestrial subsurface Schwank, Katrin; Bornemann, Till L. V.; Dombrowski, Nina The ISME Journal, Vol. 13, Issue 8 https://doi.org/10.1038/s41396-019-0421-0	journal	May 2019
Hydrological data from Crystal Geyser, Utah, USA, determined with levelogger 1 Probst, Alexander J.; Elling, Felix J.; Castelle, C. J. PANGAEA - Data Publisher for Earth & Environmental Science https://doi.org/10.1594/pangaea.914863	dataset	January 2020
Hydrological data from Crystal Geyser, Utah, USA, determined with levelogger 2 Probst, Alexander J.; Elling, Felix J.; Castelle, C. J. PANGAEA - Data Publisher for Earth & Environmental Science https://doi.org/10.1594/pangaea.914864	dataset	January 2020
Concentrations, fractional abundance, and characteristics of intact polar lipids in lipid extracts obtained by filtering eruption fluids from Crystal Geyser, sample CG21 Probst, Alexander J.; Elling, Felix J.; Castelle, C. J. PANGAEA - Data Publisher for Earth & Environmental Science https://doi.org/10.1594/pangaea.914900	dataset	January 2020
Concentrations of IPL-derived fatty acids and phytane in lipid extracts obtained by filtering eruption fluids from Crystal Geyser Probst, Alexander J.; Elling, Felix J.; Castelle, C. J. PANGAEA - Data Publisher for Earth & Environmental Science https://doi.org/10.1594/pangaea.914988	dataset	January 2020
Concentrations, fractional abundance, and characteristics of intact polar lipids in lipid extracts obtained by filtering eruption fluids from Crystal Geyser, sample CG23 Probst, Alexander J.; Elling, Felix J.; Castelle, C. J. PANGAEA - Data Publisher for Earth & Environmental Science https://doi.org/10.1594/pangaea.914901	dataset	January 2020
Carbon isotopic composition of dissolved inorganic carbon and IPL-derived fatty acids and phytane in lipid extracts obtained by filtering eruption fluids from Crystal Geyser Probst, Alexander J.; Elling, Felix J.; Castelle, C. J. PANGAEA - Data Publisher for Earth & Environmental Science https://doi.org/10.1594/pangaea.914989	dataset	January 2020
Sampling information from Crystal Geyser, Utah, USA Probst, Alexander J.; Elling, Felix J.; Castelle, C. J. PANGAEA - Data Publisher for Earth & Environmental Science https://doi.org/10.1594/pangaea.914865	dataset	January 2020
Concentrations, fractional abundance, and characteristics of intact polar lipids in lipid extracts obtained by filtering eruption fluids from Crystal Geyser, sample CG29 Probst, Alexander J.; Elling, Felix J.; Castelle, C. J. PANGAEA - Data Publisher for Earth & Environmental Science https://doi.org/10.1594/pangaea.914904	dataset	January 2020
Concentrations, fractional abundance, and characteristics of intact polar lipids in lipid extracts obtained by filtering eruption fluids from Crystal Geyser, sample CG24 Probst, Alexander J.; Elling, Felix J.; Castelle, C. J. PANGAEA - Data Publisher for Earth & Environmental Science https://doi.org/10.1594/pangaea.914902	dataset	January 2020
Concentrations, fractional abundance, and characteristics of intact polar lipids in lipid extracts obtained by filtering eruption fluids from Crystal Geyser, sample CG25 Probst, Alexander J.; Elling, Felix J.; Castelle, C. J. PANGAEA - Data Publisher for Earth & Environmental Science https://doi.org/10.1594/pangaea.914903	dataset	January 2020

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