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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 10 10 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 successionmore » following 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 Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1408445
Grant/Contract Number:
AC02-05CH11231
Resource Type:
Journal Article: 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. 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., and Andersen, Gary L. 2017. "Simulation of Deepwater Horizon oil plume reveals substrate specialization within a complex community of hydrocarbon degraders". United States. doi: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 = 2017,
month = 6
}

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  • The Deepwater Horizon (DWH) oil spill in the spring of 2010 resulted in an input of ~4.1 million barrels of oil to the Gulf of Mexico; >22% of this oil is unaccounted for, with unknown environmental consequences. Here we investigated the impact of oil deposition on microbial communities in surface sediments collected at 64 sites by targeted sequencing of 16S rRNA genes, shotgun metagenomic sequencing of 14 of these samples and mineralization experiments using 14C-labeled model substrates. The 16S rRNA gene data indicated that the most heavily oil-impacted sediments were enriched in an uncultured Gammaproteobacterium and a Colwellia species, bothmore » of which were highly similar to sequences in the DWH deep-sea hydrocarbon plume. The primary drivers in structuring the microbial community were nitrogen and hydrocarbons. Annotation of unassembled metagenomic data revealed the most abundant hydrocarbon degradation pathway encoded genes involved in degrading aliphatic and simple aromatics via butane monooxygenase. The activity of key hydrocarbon degradation pathways by sediment microbes was confirmed by determining the mineralization of 14C-labeled model substrates in the following order: propylene glycol, dodecane, toluene and phenanthrene. Further, analysis of metagenomic sequence data revealed an increase in abundance of genes involved in denitrification pathways in samples that exceeded the Environmental Protection Agency (EPA)’s benchmarks for polycyclic aromatic hydrocarbons (PAHs) compared with those that did not. Importantly, these data demonstrate that the indigenous sediment microbiota contributed an important ecosystem service for remediation of oil in the Gulf. However, PAHs were more recalcitrant to degradation, and their persistence could have deleterious impacts on the sediment ecosystem.« less
  • The Deepwater Horizon oil spill in the Gulf of Mexico is the deepest and largest offshore spill in U.S. history and its impacts on marine ecosystems are largely unknown. Here, we showed that the microbial community functional composition and structure were dramatically altered in a deep-sea oil plume resulting from the spill. A variety of metabolic genes involved in both aerobic and anaerobic hydrocarbon degradation were highly enriched in the plume compared to outside the plume, indicating a great potential for intrinsic bioremediation or natural attenuation in the deep-sea. Various other microbial functional genes relevant to carbon, nitrogen, phosphorus, sulfurmore » and iron cycling, metal resistance, and bacteriophage replication were also enriched in the plume. Together, these results suggest that the indigenous marine microbial communities could play a significant role in biodegradation of oil spills in deep-sea environments.« less
  • We sequenced and annotated the genome of the filamentous fungus Fusarium graminearum, a major pathogen of cultivated cereals. Very few repetitive sequences were detected, and the process of repeat-induced point mutation, in which duplicated sequences are subject to extensive mutation, may partially account for the reduced repeat content and apparent low number of paralogous (ancestrally duplicated) genes. A second strain of F. graminearum contained more than 10,000 single-nucleotide polymorphisms, which were frequently located near telomeres and within other discrete chromosomal segments. Many highly polymorphic regions contained sets of genes implicated in plant-fungus interactions and were unusually divergent, with higher ratesmore » of recombination. These regions of genome innovation may result from selection due to interactions of F. graminearum with its plant hosts.« less
  • The structure of a complex of Torpedo californica acetylcholinesterase with the transition state analog inhibitor m-(N, N,N-trimethylammonio)-2,2,2-trifluoroacetophenone has been solved by X-ray crystallographic methods to 2.8 A resolution. Since the inhibitor binds to the enzyme about 10{sup 10}-fold more tightly than the substrate acetylcholine, this complex provides a visual accounting of the enzyme-ligand interactions that provide the molecular basis for the catalytic power of acetylcholinesterase. The acetyl ester hydrolytic specificity of the enzyme is revealed by the interaction of the CF{sub 3} function of the transition state analog with a concave binding site comprised of the residues G119, W233, F288,more » F290, and F331. The highly geometrically convergent array of enzyme-ligand interactions visualized in the complex described herein envelopes the acylation transition state and sequesters it from solvent, this being consistent with the location of the active site at the bottom of a deep and narrow gorge. 82 refs., 5 figs.« less