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Title: Simulation of Deepwater Horizon oil plume reveals substrate specialization within a complex community of hydrocarbon degraders

Abstract

The Deepwater Horizon (DWH) accident released an estimated 4.1 million barrels of oil and 1010 mol of natural gas into the Gulf of Mexico, forming deep-sea plumes of dispersed oil droplets and dissolved gases that were largely degraded by bacteria. During the course of this 3-mo disaster a series of different bacterial taxa were enriched in succession within deep plumes, but the metabolic capabilities of the different populations that controlled degradation rates of crude oil components are poorly understood. We experimentally reproduced dispersed plumes of fine oil droplets in Gulf of Mexico seawater and successfully replicated the enrichment and succession of the principal oil-degrading bacteria observed during the DWH event. We recovered near-complete genomes, whose phylogeny matched those of the principal biodegrading taxa observed in the field, including the DWH Oceanospirillales (now identified as a Bermanella species), multiple species of Colwellia, Cycloclasticus, and other members of Gammaproteobacteria, Flavobacteria, and Rhodobacteria. Metabolic pathway analysis, combined with hydrocarbon compositional analysis and species abundance data, revealed substrate specialization that explained the successional pattern of oil-degrading bacteria. The fastest-growing bacteria used short-chain alkanes. The analyses also uncovered potential cooperative and competitive relationships, even among close relatives. We conclude that patterns of microbial succession followingmore » deep ocean hydrocarbon blowouts are predictable and primarily driven by the availability of liquid petroleum hydrocarbons rather than natural gases.« less

Authors:
 [1]; ORCiD logo [2];  [3];  [4];  [5];  [1];  [4];  [3];  [6]; ORCiD logo [2]
  1. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Ecology Dept.
  2. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Ecology Dept.; Univ. of California, Berkeley, CA (United States). Dept. of Environmental Science, Policy and Managment
  3. Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science
  4. Florida Intl Univ., Miami, FL (United States). Dept. of Chemistry and Biochemistry
  5. Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science; USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  6. Univ. of Louisville, KY (United States). Dept. of Biology
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1408445
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 114; Journal Issue: 28; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; 60 APPLIED LIFE SCIENCES; hydrocarbon biodegradation; gulf of Mexic; microbial communities; macondo oil; genome succession

Citation Formats

Hu, Ping, Dubinsky, Eric A., Probst, Alexander J., Wang, Jian, Sieber, Christian M. K., Tom, Lauren M., Gardinali, Piero R., Banfield, Jillian F., Atlas, Ronald M., and Andersen, Gary L. Simulation of Deepwater Horizon oil plume reveals substrate specialization within a complex community of hydrocarbon degraders. United States: N. p., 2017. Web. doi:10.1073/pnas.1703424114.
Hu, Ping, Dubinsky, Eric A., Probst, Alexander J., Wang, Jian, Sieber, Christian M. K., Tom, Lauren M., Gardinali, Piero R., Banfield, Jillian F., Atlas, Ronald M., & Andersen, Gary L. Simulation of Deepwater Horizon oil plume reveals substrate specialization within a complex community of hydrocarbon degraders. United States. https://doi.org/10.1073/pnas.1703424114
Hu, Ping, Dubinsky, Eric A., Probst, Alexander J., Wang, Jian, Sieber, Christian M. K., Tom, Lauren M., Gardinali, Piero R., Banfield, Jillian F., Atlas, Ronald M., and Andersen, Gary L. Mon . "Simulation of Deepwater Horizon oil plume reveals substrate specialization within a complex community of hydrocarbon degraders". United States. https://doi.org/10.1073/pnas.1703424114. https://www.osti.gov/servlets/purl/1408445.
@article{osti_1408445,
title = {Simulation of Deepwater Horizon oil plume reveals substrate specialization within a complex community of hydrocarbon degraders},
author = {Hu, Ping and Dubinsky, Eric A. and Probst, Alexander J. and Wang, Jian and Sieber, Christian M. K. and Tom, Lauren M. and Gardinali, Piero R. and Banfield, Jillian F. and Atlas, Ronald M. and Andersen, Gary L.},
abstractNote = {The Deepwater Horizon (DWH) accident released an estimated 4.1 million barrels of oil and 1010 mol of natural gas into the Gulf of Mexico, forming deep-sea plumes of dispersed oil droplets and dissolved gases that were largely degraded by bacteria. During the course of this 3-mo disaster a series of different bacterial taxa were enriched in succession within deep plumes, but the metabolic capabilities of the different populations that controlled degradation rates of crude oil components are poorly understood. We experimentally reproduced dispersed plumes of fine oil droplets in Gulf of Mexico seawater and successfully replicated the enrichment and succession of the principal oil-degrading bacteria observed during the DWH event. We recovered near-complete genomes, whose phylogeny matched those of the principal biodegrading taxa observed in the field, including the DWH Oceanospirillales (now identified as a Bermanella species), multiple species of Colwellia, Cycloclasticus, and other members of Gammaproteobacteria, Flavobacteria, and Rhodobacteria. Metabolic pathway analysis, combined with hydrocarbon compositional analysis and species abundance data, revealed substrate specialization that explained the successional pattern of oil-degrading bacteria. The fastest-growing bacteria used short-chain alkanes. The analyses also uncovered potential cooperative and competitive relationships, even among close relatives. We conclude that patterns of microbial succession following deep ocean hydrocarbon blowouts are predictable and primarily driven by the availability of liquid petroleum hydrocarbons rather than natural gases.},
doi = {10.1073/pnas.1703424114},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 28,
volume = 114,
place = {United States},
year = {Mon Jun 26 00:00:00 EDT 2017},
month = {Mon Jun 26 00:00:00 EDT 2017}
}

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