Chemical dispersants can suppress the activity of natural oil-degrading microorganisms

Kleindienst, Sara; Seidel, Michael; Ziervogel, Kai; Grim, Sharon L.; Loftis, Kathy; Harrison, Sarah; Malkin, Sairah Y.; Perkins, Matthew J.; Field, Jennifer A.; Sogin, Mitchell L.; Dittmar, Thorsten; Passow, Uta; Medeiros, Patricia M.; Joye, Samantha B.

doi:10.1073/pnas.1507380112

Cited by 264 publications

(339 citation statements)

References 46 publications

(54 reference statements)

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“…A recent study questions the efficacy of the subsea dispersant application in modulating droplet size (55), and the variable impacts of dispersant on biodegradation are at the center of an ongoing debate (56,57). The effect of dispersant itself on the benthos is not well understood, but components of dispersant have been found to persist in sediments and in fragile deep-sea coral communities on a scale of years (4).…”

Section: Discussionmentioning

confidence: 99%

Persistence and biodegradation of oil at the ocean floor following Deepwater Horizon

Bagby

Reddy

Aeppli

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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The 2010 Deepwater Horizon disaster introduced an unprecedented discharge of oil into the deep Gulf of Mexico. Considerable uncertainty has persisted regarding the oil’s fate and effects in the deep ocean. In this work we assess the compound-specific rates of biodegradation for 125 aliphatic, aromatic, and biomarker petroleum hydrocarbons that settled to the deep ocean floor following release from the damaged Macondo Well. Based on a dataset comprising measurements of up to 168 distinct hydrocarbon analytes in 2,980 sediment samples collected within 4 y of the spill, we develop a Macondo oil “fingerprint” and conservatively identify a subset of 312 surficial samples consistent with contamination by Macondo oil. Three trends emerge from analysis of the biodegradation rates of 125 individual hydrocarbons in these samples. First, molecular structure served to modulate biodegradation in a predictable fashion, with the simplest structures subject to fastest loss, indicating that biodegradation in the deep ocean progresses similarly to other environments. Second, for many alkanes and polycyclic aromatic hydrocarbons biodegradation occurred in two distinct phases, consistent with rapid loss while oil particles remained suspended followed by slow loss after deposition to the seafloor. Third, the extent of biodegradation for any given sample was influenced by the hydrocarbon content, leading to substantially greater hydrocarbon persistence among the more highly contaminated samples. In addition, under some conditions we find strong evidence for extensive degradation of numerous petroleum biomarkers, notably including the native internal standard 17α(H),21β(H)-hopane, commonly used to calculate the extent of oil weathering.

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Section: Discussionmentioning

confidence: 99%

Persistence and biodegradation of oil at the ocean floor following Deepwater Horizon

Bagby

Reddy

Aeppli

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…promote microbes that are able to use dispersant for growth. Therefore, it was thought that the relative abundance of the natural hydrocarbon degraders, such as Marinobacter, was kept low (7). No study, to date, has been able to specify the relationship between hydrocarbon substrate availability and the metabolic capacities of the diverse group of organisms responsible for hydrocarbon degradation in the DWH plume.…”

Section: Significancementioning

confidence: 99%

“…Consequently, vast plumes of oil microdroplets containing not only soluble but also insoluble fractions of oil were retained at depth, largely between 900 and 1,300 m deep (1,2), and subject to biodegradation by the deep ocean microbial community (3)(4)(5)(6). Furthermore, the application of dispersants at the wellhead may have enhanced oil droplet formation, oil retention, and biodegradation at depth, although potential inhibitory effects of dispersants on biodegradation have been reported (7). There continues to be considerable uncertainty and disagreement about the rates of microbial biodegradation under these conditions and the factors controlling the fate of the complex mixture of crude oil compounds that were trapped deep in the water column (8-10).…”

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confidence: 99%

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

Dubinsky

Probst

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

114

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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

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“…Likewise, in coastal beach sands impacted by the oil spill (3.1-4,500 mg oil kg -1 sand), aerobic hydrocarbon degraders such as Acinetobacter, Alcanivorax, Hyphomonas, Marinobacter, Parvibaculum, and Pseudomonas were shown to vary over time in response to oil exposure (Kostka et al, 2011;Rodriguez-R et al, 2015). Recent oil enrichment experiments with deep water from the Gulf of Mexico also documented the enhanced response of Colwellia, Cycloclasticus, and Marinobacter within a few weeks of oil exposure (Kleindienst et al, 2015b).…”

Section: Minimal Impacts On Sediment Microbial Community Structure Frmentioning

confidence: 98%

Microbial response to oil enrichment in Gulf of Mexico sediment measured using a novel long-term benthic lander system

Orcutt

Lapham

Delaney

et al. 2017

Elementa: Science of the Anthropocene

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Weathered crude oil sank to the seafloor following the Deepwater Horizon disaster in 2010, removing this oil from further physical and photo-chemical degradation processes and leaving benthic processes as the mechanisms for altering and remediating this hydrocarbon source. To quantify potential microbial oil degradation rates at the seafloor, and associated changes in sediment microbial community structure and pore fluid composition, we used a benthic lander system to deploy novel sediment flow-through chambers at a natural hydrocarbon seep in the Gulf of Mexico (at a depth of 1226 m in lease block GC600) roughly 265 km southwest of the Deepwater Horizon wellhead (at 1500 m depth). Sediment amended with 20% unweathered crude oil had elevated rates of sulfate reduction over the course of the 5-month-long experiment as compared to an unamended control, yielding potential rates of sulfate reduction (600–800 mmol m–2 d–1) among the highest measured in hydrocarbon-influenced seafloor sediment. Oil amendment also stimulated methane production towards the end of the experiment, and led to slightly higher cell densities without significant changes in microbial community structure, based on 16S rRNA gene sequence libraries and fatty acid profiles. Assuming a link between sulfate reduction and hydrocarbon degradation, these results suggest that electron acceptor availability may become limiting in heavily oiled deep-sea environments, resulting in minimal degradation of deposited oil. This study provides unique data on seafloor sediment responses to oil deposition, and reveals the value of using observatories to fill the gap in understanding deep-sea microbial processes, especially for ephemeral and stochastic events such as oil spills.

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Chemical dispersants can suppress the activity of natural oil-degrading microorganisms

Cited by 264 publications

References 46 publications

Persistence and biodegradation of oil at the ocean floor following Deepwater Horizon

Persistence and biodegradation of oil at the ocean floor following Deepwater Horizon

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

Microbial response to oil enrichment in Gulf of Mexico sediment measured using a novel long-term benthic lander system

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