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

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 114; no. 28; pp. 7432 - 7437
• Main Authors: 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.
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 11.07.2017; National Academy of Sciences, Washington, DC (United States)
• Subjects: 60 APPLIED LIFE SCIENCES; Abundance; Alkanes; Bacteria; Bacteria - metabolism; Biodegradation; Biodegradation, Environmental; Biodiversity; Biological Sciences; Blowouts; Chemical analysis; Computer Simulation; Crude oil; Degradation; Dispersion; Dissolved gases; Droplets; Ecological succession; ENVIRONMENTAL SCIENCES; Gases; genome succession; Genome, Bacterial; Genomes; gulf of Mexic; Gulf of Mexico; hydrocarbon biodegradation; Hydrocarbon-degrading bacteria; Hydrocarbons; Hydrocarbons - metabolism; macondo oil; microbial communities; Microorganisms; Natural gas; Oil spills; Petroleum; Petroleum hydrocarbons; Petroleum Pollution; Phylogeny; Plumes; RNA, Ribosomal, 16S - analysis; Seawater; Simulation; Specialization; Species; Taxa; Time Factors; Water analysis; Water Microbiology; Gulf of Mexico; Gulf of Mexico; microbial communities; genome succession; hydrocarbon biodegradation; Macondo oil
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1703424114

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.