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 oildegrading 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.hydrocarbon biodegradation | Gulf of Mexico | microbial communities | Macondo oil | genome succession

Major changes in the composition of a Southern Ocean bacterial community in response to diatom-derived dissolved organic matter

“…In an experimental study Colwellia became a dominant taxon at an intermediate stage of hydrocarbon degradation (Hu et al 2017). The increase in abundance of this group was concurrent with an increased number of aromatic degradation genes as shown by metagenomic analyses and the decrease in the concentration of one -to three -ring aromatic compounds (Hu et al 2017).…”

The Molecular Basis for Understanding the Impacts of Ocean Warming

“…For an example of lag times in an ocean microbial population sensing changing chemical energy opportunity, we can examine the elegant laboratory simulation of the Deepwater Horizon oil spill event by Hu et al (). Here the changes occurring over a 64‐day period in a series of stainless steel vessels containing sea water collected from the site and maintained at in situ temperature were followed both for the genomic patterns and the changing quantity of hydrocarbons present.…”

Simulations predict microbial responses in the environment? This environment disagrees retrospectively

“…However, the 16S rRNA gene of Candidatus B. macondoprimitus does not match perfectly to any amplicons from the oil plume (Fig. 1A), and Hu et al (1) present no evidence to link the simulation to the environment beyond genus-level taxonomic community profiles.…”

“…In their recent study, Hu et al (1) simulated in the laboratory the deep-sea oil plume of the Deepwater Horizon (DWH) disaster, and claim successful enrichment of the dominant oil-degrading bacteria found in the environment. Although the simulation offers valuable insights into microbial succession patterns following the addition of oil, our analysis revealed that the dominant hydrocarbon-degrading bacteria in the simulation was not in the environment, and the one in the environment was not in the simulation.…”

“…Cultivation efforts failed to isolate members from these early responders; however, a population genome reconstructed from the oil plume is available (5). In their simulation, Hu et al (1) reconstructed various population genomes, including an abundant Oceanospirillaceae population. The authors named this population genome "Candidatus Bermanella macondoprimitus," and claim that they were able to enrich "the dominant hydrocarbon-degrading organism that was detected in the initial stage of the DWH [oil] plume" (1), which was missing in previous simulations (6).…”