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

Abstract

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.

Authors:
ORCiD logo [1]; ORCiD logo [2];  [3];  [4]; ORCiD logo [4]; ORCiD logo [5];  [6];  [7];  [8];  [9]; ORCiD logo [10];  [4]; ORCiD logo [7]
  1. Univ. of California, Berkeley, CA (United States); Univ. of Duisburg-Essen (Germany)
  2. Univ. of Bremen (Germany); Harvard Univ., Cambridge, MA (United States)
  3. Univ. of California, Berkeley, CA (United States); Univ. of Bremen (Germany)
  4. Univ. of Bremen (Germany)
  5. Elettra-Sincrotrone Treiste (Italy); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  6. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  7. Univ. of California, Berkeley, CA (United States)
  8. Univ. of British Columbia, Vancouver, BC (Canada); Univ. of Calgary, AB (Canada)
  9. Univ. of Calgary, AB (Canada)
  10. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); Sloan Foundation; German Research Foundation (DFG); Canadian National Science and Engineering Research Council
OSTI Identifier:
1634086
Grant/Contract Number:  
AC02-05CH11231; G-2016-20166041; DFG PR 1603/1-1; 06509-2016
Resource Type:
Accepted Manuscript
Journal Name:
The ISME Journal
Additional Journal Information:
Journal Volume: 14; Journal Issue: 6; Journal ID: ISSN 1751-7362
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; environmental microbiology; microbial ecology

Citation Formats

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, and Banfield, Jillian F. Lipid analysis of CO2-rich subsurface aquifers suggests an autotrophy-based deep biosphere with lysolipids enriched in CPR bacteria. United States: N. p., 2020. Web. https://doi.org/10.1038/s41396-020-0624-4.
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. Lipid analysis of CO2-rich subsurface aquifers suggests an autotrophy-based deep biosphere with lysolipids enriched in CPR bacteria. United States. https://doi.org/10.1038/s41396-020-0624-4
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, and Banfield, Jillian F. Fri . "Lipid analysis of CO2-rich subsurface aquifers suggests an autotrophy-based deep biosphere with lysolipids enriched in CPR bacteria". United States. https://doi.org/10.1038/s41396-020-0624-4. https://www.osti.gov/servlets/purl/1634086.
@article{osti_1634086,
title = {Lipid analysis of CO2-rich subsurface aquifers suggests an autotrophy-based deep biosphere with lysolipids enriched in CPR bacteria},
author = {Probst, Alexander J. and Elling, Felix J. and Castelle, Cindy J. and Zhu, Qingzeng and Elvert, Marcus and Birarda, Giovanni and Holman, Hoi-Ying N. and Lane, Katherine R. and Ladd, Bethany and Ryan, M. Cathryn and Woyke, Tanja and Hinrichs, Kai-Uwe and Banfield, Jillian F.},
abstractNote = {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.},
doi = {10.1038/s41396-020-0624-4},
journal = {The ISME Journal},
number = 6,
volume = 14,
place = {United States},
year = {2020},
month = {3}
}

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