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Title: Methane-Oxidizing Bacteria Shunt Carbon to Microbial Mats at a Marine Hydrocarbon Seep

Abstract

The marine subsurface is a reservoir of the greenhouse gas methane. While microorganisms living in water column and seafloor ecosystems are known to be a major sink limiting net methane transport from the marine subsurface to the atmosphere, few studies have assessed the flow of methane-derived carbon through the benthic mat communities that line the seafloor on the continental shelf where methane is emitted. We analyzed the abundance and isotope composition of fatty acids in microbial mats grown in the shallow Coal Oil Point seep field off Santa Barbara, CA, USA, where seep gas is a mixture of methane and CO2. We further used stable isotope probing (SIP) to track methane incorporation into mat biomass. We found evidence that multiple allochthonous substrates supported the rich growth of these mats, with notable contributions from bacterial methanotrophs and sulfur-oxidizers as well as eukaryotic phototrophs. Fatty acids characteristic of methanotrophs were shown to be abundant and 13C-enriched in SIP samples, and DNA-SIP identified members of the methanotrophic family Methylococcaceae as major 13CH4 consumers. Members of Sulfuricurvaceae, Sulfurospirillaceae, and Sulfurovumaceae are implicated in fixation of seep CO2. The mats’ autotrophs support a diverse assemblage of co-occurring bacteria and protozoa, with Methylophaga as key consumersmore » of methane-derived organic matter. This study identifies the taxa contributing to the flow of seep-derived carbon through microbial mat biomass, revealing the bacterial and eukaryotic diversity of these remarkable ecosystems.« less

Authors:
 [1];  [2];  [3];  [4];  [5];  [6];  [1]
  1. Univ. of California, Santa Barbara, CA (United States)
  2. Ocean Univ. of China, Qingdao (China)
  3. Univ. of California, Santa Barbara, CA (United States); Case Western Reserve Univ., Cleveland, OH (United States)
  4. Univ. of California, Santa Barbara, CA (United States); Carl von Ossietzky Univ., Wilhelmshaven (Germany)
  5. Univ. of California, Santa Barbara, CA (United States); Univ. of North Carolina, Charlotte, NC (United States)
  6. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1379742
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 8; Journal Issue: FEB; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; microbial mats; methanotrophs; sulfide-oxidizing bacteria; stable isotope probing; intact polar lipids (IPL); 16S rRNA gene

Citation Formats

Paul, Blair G., Ding, Haibing, Bagby, Sarah C., Kellermann, Matthias Y., Redmond, Molly C., Andersen, Gary L., and Valentine, David L. Methane-Oxidizing Bacteria Shunt Carbon to Microbial Mats at a Marine Hydrocarbon Seep. United States: N. p., 2017. Web. doi:10.3389/fmicb.2017.00186.
Paul, Blair G., Ding, Haibing, Bagby, Sarah C., Kellermann, Matthias Y., Redmond, Molly C., Andersen, Gary L., & Valentine, David L. Methane-Oxidizing Bacteria Shunt Carbon to Microbial Mats at a Marine Hydrocarbon Seep. United States. https://doi.org/10.3389/fmicb.2017.00186
Paul, Blair G., Ding, Haibing, Bagby, Sarah C., Kellermann, Matthias Y., Redmond, Molly C., Andersen, Gary L., and Valentine, David L. Mon . "Methane-Oxidizing Bacteria Shunt Carbon to Microbial Mats at a Marine Hydrocarbon Seep". United States. https://doi.org/10.3389/fmicb.2017.00186. https://www.osti.gov/servlets/purl/1379742.
@article{osti_1379742,
title = {Methane-Oxidizing Bacteria Shunt Carbon to Microbial Mats at a Marine Hydrocarbon Seep},
author = {Paul, Blair G. and Ding, Haibing and Bagby, Sarah C. and Kellermann, Matthias Y. and Redmond, Molly C. and Andersen, Gary L. and Valentine, David L.},
abstractNote = {The marine subsurface is a reservoir of the greenhouse gas methane. While microorganisms living in water column and seafloor ecosystems are known to be a major sink limiting net methane transport from the marine subsurface to the atmosphere, few studies have assessed the flow of methane-derived carbon through the benthic mat communities that line the seafloor on the continental shelf where methane is emitted. We analyzed the abundance and isotope composition of fatty acids in microbial mats grown in the shallow Coal Oil Point seep field off Santa Barbara, CA, USA, where seep gas is a mixture of methane and CO2. We further used stable isotope probing (SIP) to track methane incorporation into mat biomass. We found evidence that multiple allochthonous substrates supported the rich growth of these mats, with notable contributions from bacterial methanotrophs and sulfur-oxidizers as well as eukaryotic phototrophs. Fatty acids characteristic of methanotrophs were shown to be abundant and 13C-enriched in SIP samples, and DNA-SIP identified members of the methanotrophic family Methylococcaceae as major 13CH4 consumers. Members of Sulfuricurvaceae, Sulfurospirillaceae, and Sulfurovumaceae are implicated in fixation of seep CO2. The mats’ autotrophs support a diverse assemblage of co-occurring bacteria and protozoa, with Methylophaga as key consumers of methane-derived organic matter. This study identifies the taxa contributing to the flow of seep-derived carbon through microbial mat biomass, revealing the bacterial and eukaryotic diversity of these remarkable ecosystems.},
doi = {10.3389/fmicb.2017.00186},
journal = {Frontiers in Microbiology},
number = FEB,
volume = 8,
place = {United States},
year = {Mon Feb 27 00:00:00 EST 2017},
month = {Mon Feb 27 00:00:00 EST 2017}
}

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Cited by: 26 works
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journal, June 2011


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journal, September 2012


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journal, December 2002


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journal, November 2016

  • Tavormina, Patricia L.; Kellermann, Matthias Y.; Antony, Chakkiath Paul
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Deep-Sea Oil Plume Enriches Indigenous Oil-Degrading Bacteria
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A Persistent Oxygen Anomaly Reveals the Fate of Spilled Methane in the Deep Gulf of Mexico
journal, January 2011


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Microbial Iron Mats at the Mid-Atlantic Ridge and Evidence that Zetaproteobacteria May Be Restricted to Iron-Oxidizing Marine Systems
journal, March 2015


Role of microbial mats in Sulaibikhat Bay (Kuwait) mudflat food webs: evidence from δ13C analysis
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Exopolysaccharides produced by marine bacteria and their applications as glycosaminoglycan-like molecules
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Works referencing / citing this record:

Microbial megacities fueled by methane oxidation in a mineral spring cave
journal, September 2017

  • Karwautz, Clemens; Kus, Günter; Stöckl, Michael
  • The ISME Journal, Vol. 12, Issue 1
  • DOI: 10.1038/ismej.2017.146

Communal metabolism by Methylococcaceae and Methylophilaceae is driving rapid aerobic methane oxidation in sediments of a shallow seep near Elba, Italy
journal, July 2019

  • Taubert, Martin; Grob, Carolina; Crombie, Andrew
  • Environmental Microbiology, Vol. 21, Issue 10
  • DOI: 10.1111/1462-2920.14728

Novel facultative Methylocella strains are active methane consumers at terrestrial natural gas seeps
journal, October 2019

  • Farhan Ul Haque, Muhammad; Crombie, Andrew T.; Murrell, J. Colin
  • Microbiome, Vol. 7, Issue 1
  • DOI: 10.1186/s40168-019-0741-3

Microbial megacities fueled by methane oxidation in a mineral spring cave
journal, September 2017

  • Karwautz, Clemens; Kus, Günter; Stöckl, Michael
  • The ISME Journal, Vol. 12, Issue 1
  • DOI: 10.1038/ismej.2017.146

In situ development of a methanotrophic microbiome in deep-sea sediments
journal, August 2018