Metagenomic analysis and metabolite profiling of deep–sea sediments from the Gulf of Mexico following the Deepwater Horizon oil spill

Abstract

Marine subsurface environments such as deep-sea sediments, house abundant and diverse microbial communities that are believed to influence large-scale geochemical processes. These processes include the biotransformation and mineralization of numerous petroleum constituents. Thus, microbial communities in the Gulf of Mexico are thought to be responsible for the intrinsic bioremediation of crude oil released by the Deepwater Horizon (DWH) oil spill. While hydrocarbon contamination is known to enrich for aerobic, oil-degrading bacteria in deep-seawater habitats, relatively little is known about the response of communities in deep-sea sediments, where low oxygen levels may hinder such a response. Here, we examined the hypothesis that increased hydrocarbon exposure results in an altered sediment microbial community structure that reflects the prospects for oil biodegradation under the prevailing conditions. We explore this hypothesis using metagenomic analysis and metabolite profiling of deep-sea sediment samples following the DWH oil spill. The presence of aerobic microbial communities and associated functional genes was consistent among all samples, whereas, a greater number of Deltaproteobacteria and anaerobic functional genes were found in sediments closest to the DWH blowout site. Metabolite profiling also revealed a greater number of putative metabolites in sediments surrounding the blowout zone relative to a background site located 127 km away. The mass spectral analysis of the putative metabolites revealed that alkylsuccinates remained below detection levels, but a homologous series of benzylsuccinates (with carbon chain lengths from 5 to 10) could be detected. Our findings suggest that increased exposure to hydrocarbons enriches for Deltaproteobacteria, which are known to be capable of anaerobic hydrocarbon metabolism. We also provide evidence for an active microbial community metabolizing aromatic hydrocarbons in deep-sea sediments of the Gulf of Mexico.

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

“…We tested the validity of these relationships for the seafloor by comparing the residual fraction for each hydrocarbon remaining in the sediment 4 y after the spill began. Among the compounds examined, carbon skeletons range from nine to 37 atoms (aliphatics, 9-37; aromatics, 9-22; biomarkers, [23][24][25][26][27][28][29][30][31][32][33][34][35] and vary in complexity from the straight-chain aliphatic n-C9 to the pentacyclic, multiply substituted biomarker pentakishomohopane. This analysis provides an unparalleled window into the disposition of oil following the DWH event, in that the extent of biodegradation is quantified simultaneously for 125 petroleum hydrocarbons across wide-ranging contamination levels.…”

“…These droplets remained concentrated close to the well's coordinates (2,11,12,15), but modeling suggests that droplet size drove further vertical partitioning, with droplets >50 μm mixing upwards by August 2010 and smaller droplets remaining suspended in the deep ocean (7,17,18). Some suspended oil was eventually deposited to the seafloor, likely via oilmineral aggregates or microbial flocs (8,19,20), with intense contamination within ∼5 km of the well (21)(22)(23)(24)(25)(26). Surficial sediments near the well were found to carry >1,000-fold-elevated concentrations of dioctyl sodium sulfosuccinate (4), an active ingredient of the chemical dispersant applied at the wellhead, and to exhibit a radiocarbon deficit consistent with oil deposition (27).…”

Comparative analysis of metagenomes from three methanogenic hydrocarbon-degrading enrichment cultures with 41 environmental samples

“…This grouping presumably reflects the process of enrichment compared with unenriched samples from tailings and other environmental samples. All three GoM metagenomes grouped more closely with marine samples and lagoon sediments than with hydrocarbon-impacted environments, despite the recent exposure of at least two of the GoM sediments to hydrocarbons during the Deepwater Horizon oil spill (Kimes et al, 2013).…”

“…The oil sands tailings ponds were found to share some functions with the methanogenic hydrocarbon-degrading cultures, particularly those associated with anaerobic or methanogenic metabolism (Functional Group I, Figure 4b). For example, previous analyses revealed the presence of genes associated with fumarate addition in TP6 and in clone libraries from GoM sediments (Kimes et al, 2013), suggesting that this is a widespread mechanism of hydrocarbon activation in anoxic environments. Comparison of metagenome groups from hydrocarbon-impacted communities: HC (TOLDC, SCADC and NAPDC); GM (three metagenomes from Gulf of Mexico deep marine sediments); and TP (two metagenomes from oil sands tailings ponds).…”

“…To investigate the effects of environmental selection on functional potential in methanogenic microbial communities, the three metagenomes from the hydrocarbon-degrading cultures were compared with 41 metagenomes available through MG-RAST including two oil sands tailings ponds (MLSB and TP6), three Gulf of Mexico (GoM) marine sediment samples collected from the Deepwater Horizon oil spill area (Kimes et al, 2013), three dechlorinating enrichment cultures (the only other anaerobic pollutant-degrading enrichment culture metagenomes available on MG-RAST at time of analysis), and 33 metagenomes from a range of environments with varying physiochemical properties (Supplementary Table S1). A comparison of this nature assumes that random shotgun sequencing has recovered the prevalent genetic composition of the microbial community in any given environmental sample, validated by the taxonomic composition expected in their respective niches (for example, Proteobacteria in GoM and Dehalococcoidetes in dechlorinating cultures).…”