Microbial gene functions enriched in the Deepwater Horizon deep-sea oil plume.
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ABSTRACT:
SUBMITTER: Lu Z
PROVIDER: S-EPMC3260509 | biostudies-literature | 2012 Feb
REPOSITORIES: biostudies-literature
Publications
Microbial gene functions enriched in the Deepwater Horizon deep-sea oil plume.
Lu Zhenmei Z Deng Ye Y Van Nostrand Joy D JD He Zhili Z Voordeckers James J Zhou Aifen A Lee Yong-Jin YJ Mason Olivia U OU Dubinsky Eric A EA Chavarria Krystle L KL Tom Lauren M LM Fortney Julian L JL Lamendella Regina R Jansson Janet K JK D'haeseleer Patrik P Hazen Terry C TC Zhou Jizhong J
The ISME journal 20110804 2
The Deepwater Horizon oil spill in the Gulf of Mexico is the deepest and largest offshore spill in the United State 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 with outside the plume, i ...[more]
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Project description:The Deepwater Horizon (DWH) oil well blowout generated an enormous plume of dispersed hydrocarbons that substantially altered the Gulf of Mexico's deep-sea microbial community. A significant enrichment of distinct microbial populations was observed, yet, little is known about the abundance and richness of specific microbial ecotypes involved in gas, oil and dispersant biodegradation in the wake of oil spills. Here, we document a previously unrecognized diversity of closely related taxa affiliating with Cycloclasticus, Colwellia and Oceanospirillaceae and describe their spatio-temporal distribution in the Gulf's deepwater, in close proximity to the discharge site and at increasing distance from it, before, during and after the discharge. A highly sensitive, computational method (oligotyping) applied to a data set generated from 454-tag pyrosequencing of bacterial 16S ribosomal RNA gene V4-V6 regions, enabled the detection of population dynamics at the sub-operational taxonomic unit level (0.2% sequence similarity). The biogeochemical signature of the deep-sea samples was assessed via total cell counts, concentrations of short-chain alkanes (C1-C5), nutrients, (colored) dissolved organic and inorganic carbon, as well as methane oxidation rates. Statistical analysis elucidated environmental factors that shaped ecologically relevant dynamics of oligotypes, which likely represent distinct ecotypes. Major hydrocarbon degraders, adapted to the slow-diffusive natural hydrocarbon seepage in the Gulf of Mexico, appeared unable to cope with the conditions encountered during the DWH spill or were outcompeted. In contrast, diverse, rare taxa increased rapidly in abundance, underscoring the importance of specialized sub-populations and potential ecotypes during massive deep-sea oil discharges and perhaps other large-scale perturbations.
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Project description:The sinking of the Deepwater Horizon in the Gulf of Mexico led to uncontrolled emission of oil to the ocean, with an official government estimate of ? 5.0 million barrels released. Among the pressing uncertainties surrounding this event is the fate of ? 2 million barrels of submerged oil thought to have been trapped in deep-ocean intrusion layers at depths of ? 1,000-1,300 m. Here we use chemical distributions of hydrocarbons in >3,000 sediment samples from 534 locations to describe a footprint of oil deposited on the deep-ocean floor. Using a recalcitrant biomarker of crude oil, 17?(H),21?(H)-hopane (hopane), we have identified a 3,200-km(2) region around the Macondo Well contaminated by ? 1.8 ± 1.0 × 10(6) g of excess hopane. Based on spatial, chemical, oceanographic, and mass balance considerations, we calculate that this contamination represents 4-31% of the oil sequestered in the deep ocean. The pattern of contamination points to deep-ocean intrusion layers as the source and is most consistent with dual modes of deposition: a "bathtub ring" formed from an oil-rich layer of water impinging laterally upon the continental slope (at a depth of ? 900-1,300 m) and a higher-flux "fallout plume" where suspended oil particles sank to underlying sediment (at a depth of ? 1,300-1,700 m). We also suggest that a significant quantity of oil was deposited on the ocean floor outside this area but so far has evaded detection because of its heterogeneous spatial distribution.
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Project description:The Deepwater Horizon spill is one of the largest environmental disasters with extensive impacts on the economic and ecological health of the Gulf of Mexico. Surface oil and coastal impacts received considerable attention, but the far larger oil spill in the deep ocean and its effects received considerably less examination. Based on 2017 ROV surveys within 500 m of the wellhead, we provide evidence of continued impacts on diversity, abundance and health of deep-sea megafauna. At locations proximal to the wellhead, megafaunal communities are more homogeneous than in unimpacted areas, lacking many taxonomic groups, and driven by high densities of arthropods. Degraded hydrocarbons at the site may be attracting arthropods. The scope of impacts may extend beyond the impacted sites with the potential for impacts to pelagic food webs and commercially important species. Overall, deep-sea ecosystem health, 7 years post spill, is recovering slowly and lingering effects may be extreme.
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Project description:The 2010 Deepwater Horizon blowout off the coast of Louisiana caused the largest marine oil spill on record. Samples were collected 2-3 months after the Macondo well was capped to assess damage to macrofauna and meiofauna communities. An earlier analysis of 58 stations demonstrated severe and moderate damage to an area of 148 km2. An additional 58 archived stations have been analyzed to enhance the resolution of that assessment and determine if impacts occurred further afield. Impacts included high levels of total petroleum hydrocarbons (TPH) and polycyclic aromatic hydrocarbons (PAH) in the sediment, low diversity, low evenness, and low taxonomic richness of the infauna communities. High nematode to copepod ratios corroborated the severe disturbance of meiofauna communities. Additionally, barium levels near the wellhead were very high because of drilling activities prior to the accident. A principal component analysis (PCA) was used to summarize oil spill impacts at stations near the Macondo well, and the benthic footprint of the DWH oil spill was estimated using Empirical Bayesian Kriging (EBK) interpolation. An area of approximately 263 km2 around the wellhead was affected, which is 78% higher than the original estimate. Particularly severe damages to benthic communities were found in an area of 58 km2, which is 142% higher than the original estimate. The addition of the new stations extended the area of the benthic footprint map to about twice as large as originally thought and improved the resolution of the spatial interpolation. In the future, increasing the spatial extent of sampling should be a top priority for designing assessment studies.
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Project description:The Deepwater Horizon (DWH) oil spill led to rapid microbial community shifts in the Gulf of Mexico, including the formation of unprecedented quantities of marine oil snow (MOS) and of a massive subsurface oil plume. The major taxa that bloomed in sea surface oil slicks during the spill included Cycloclasticus, and to a lesser extent Halomonas, Alteromonas, and Pseudoalteromonas-organisms that grow and degrade oil hydrocarbons aerobically. Here, we show that sea surface oil slicks at DWH contained obligate and facultative anaerobic taxa, including members of the obligate anaerobic phylum Fusobacteria that are commonly found in marine sediment environments. Pyrosequencing analysis revealed that Fusobacteria were strongly selected for when sea surface oil slicks were allowed to develop anaerobically. These organisms have been found in oil-contaminated sediments in the Gulf of Mexico, in deep marine oil reservoirs, and other oil-contaminated sites, suggesting they have putative hydrocarbon-degrading qualities. The occurrence and strong selection for Fusobacteria in a lab-based incubation of a sea surface oil slick sample collected during the spill suggests that these organisms may have become enriched in anaerobic zones of suspended particulates, such as MOS. Whilst the formation and rapid sinking of MOS is recognised as an important mechanism by which a proportion of the Macondo oil had been transported to the sea floor, its role in potentially transporting microorganisms, including oil-degraders, from the upper reaches of the water column to the seafloor should be considered. The presence of Fusobacteria on the sea surface-a highly oxygenated environment-is intriguing, and may be explained by the vertical upsurge of oil that provided a carrier to transport these organisms from anaerobic/micro-aerophilic zones in the oil plume or seabed to the upper reaches of the water column. We also propose that the formation of rapidly-sinking MOS may have re-transported these, and other microbial taxa, to the sediment in the Gulf of Mexico.
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Project description: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 (14)C-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, both 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 (14)C-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.
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Project description: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.
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Project description:One of the major environmental concerns of the Deepwater Horizon oil spill in the Gulf of Mexico was the ecological impact of the oil that reached shorelines of the Gulf Coast. Here we investigated the impact of the oil on the microbial composition in beach samples collected in June 2010 along a heavily impacted shoreline near Grand Isle, Louisiana. Successional changes in the microbial community structure due to the oil contamination were determined by deep sequencing of 16S rRNA genes. Metatranscriptomics was used to determine expression of functional genes involved in hydrocarbon degradation processes. In addition, potential hydrocarbon-degrading Bacteria were obtained in culture. The 16S data revealed that highly contaminated samples had higher abundances of Alpha- and Gammaproteobacteria sequences. Successional changes in these classes were observed over time, during which the oil was partially degraded. The metatranscriptome data revealed that PAH, n-alkane, and toluene degradation genes were expressed in the contaminated samples, with high homology to genes from Alteromonadales, Rhodobacterales, and Pseudomonales. Notably, Marinobacter (Gammaproteobacteria) had the highest representation of expressed genes in the samples. A Marinobacter isolated from this beach was shown to have potential for transformation of hydrocarbons in incubation experiments with oil obtained from the Mississippi Canyon Block 252 (MC252) well; collected during the Deepwater Horizon spill. The combined data revealed a response of the beach microbial community to oil contaminants, including prevalence of Bacteria endowed with the functional capacity to degrade oil.
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