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

Baruch Marine Field Laboratory, Belle W. Baruch Institute for Marine and Coastal Sciences, University of South Carolina Georgetown, SC, USA.
Frontiers in Microbiology (Impact Factor: 3.99). 03/2013; 4:50. DOI: 10.3389/fmicb.2013.00050
Source: PubMed


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.

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    • "It is a recurrent observation that most 16S rRNA gene sequences of uncultured organisms retrieved from oil polluted sediments are closely related to organisms detected in similar polluted sites, which suggests a common trend in the structuring of communities in the presence of oil. The enrichment of members of the Deltaproteobacteria is consistent with sulphate reduction being the prevailing respiratory metabolism in marine sediments which agrees with the observation that the abundance of sulphate-reducing Deltaproteobacteria also increased in deep-sea sediments near the DWH Macondo wellhead[39](reviewed in[21 ]). Deltaproteobacteria also constituted the prevailing group in the anoxic layer of subtidal sediments affected by the Prestige spill, dominated by the Desulfobacteraceae[33 ]. "
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    ABSTRACT: Marine environments harbour a persistent microbial seed which can be shaped by changes of the environmental conditions such as contamination by petroleum components. Oil spills, together with small but continuous discharges of oil from transportation and recreational activities, are important sources of hydrocarbon pollution within the marine realm. Consequently, prokaryotic communities have become well pre-adapted toward oil pollution, and many microorganisms that are exposed to its presence develop an active degradative response. The natural attenuation of oil pollutants, as has been demonstrated in many sites, is modulated according to the intrinsic environmental properties such as the availability of terminal electron acceptors and elemental nutrients, together with the degree of pollution and the type of hydrocarbon fractions present. Whilst dynamics in the bacterial communities in the aerobic zones of coastal sediments are well characterized and the key players in hydrocarbon biodegradation have been identified, the subtidal ecology of the anaerobic community is still not well understood. However, current data suggest common patterns of response in these ecosystems.
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    • "Given that these primers do not recover the full diversity of masD/assA genes, the environmental diversity and distribution of anaerobic alkane degraders remains poorly characterized. In particular, only marginal information is available on anaerobic alkane degraders in pristine sediments, i.e., sediments that are not influenced by thermogenic oil and gas formations and are not exposed to high loads of hydrocarbons from anthropogenic sources (Acosta-González et al., 2013; Kimes et al., 2013). The presence of short-chain alkanes (SCA, C 2 –C 5 ) in the pore water of marine sediments is generally considered a result of vertical migration from subsurface accumulation of hydrocarbons or reservoirs to the sediment surface and results in the release of SCA via macroseeps (focused/diffusive flow, e.g., oil and gas seeps, mud volcanoes, pockmarks) and microseepage (diffusive flow) (Etiope, 2015). "
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    ABSTRACT: Alkanes are major constituents of crude oil and are released to the marine environment by natural seepage and from anthropogenic sources. Due to their chemical inertness, their removal from anoxic marine sediments is primarily controlled by the activity of anaerobic alkane-degrading microorganisms. To facilitate comprehensive cultivation-independent surveys of the diversity and distribution of anaerobic alkane degraders, we designed novel PCR primers that cover all known diversity of the 1-methylalkyl succinate synthase gene (masD/assA), which catalyzes the initial activation of alkanes. We studied masD/assA gene diversity in pristine and seepage-impacted Danish coastal sediments, as well as in sediments and alkane-degrading enrichment cultures from the Middle Valley (MV) hydrothermal vent system in the Pacific Northwest. MasD/assA genes were ubiquitously present, and the primers captured the diversity of both known and previously undiscovered masD/assA gene diversity. Seepage sediments were dominated by a single masD/assA gene cluster, which is presumably indicative of a substrate-adapted community, while pristine sediments harbored a diverse range of masD/assA phylotypes including those present in seepage sediments. This rare biosphere of anaerobic alkane degraders will likely increase in abundance in the event of seepage or accidental oil spillage. Nanomolar concentrations of short-chain alkanes (SCA) were detected in pristine and seepage sediments. Interestingly, anaerobic alkane degraders closely related to strain BuS5, the only SCA degrader in pure culture, were found in mesophilic MV enrichments, but not in cold sediments from Danish waters. We propose that the new masD/assA gene lineages in these sediments represent novel phylotypes that are either fueled by naturally occurring low levels of SCA or that metabolize medium- to long-chain alkanes. Our study highlights that masD/assA genes are a relevant diagnostic marker to identify seepage and microseepage, e.g., during prospecting for oil and gas, and may act as an indicator of anthropogenic oil spills in marine sediments.
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    • "d washing ) , including populations with potential oil degradation capability ( Engel and Gupta , 2014 ) . Oil plumes have been shown to have an impact on microbial communities in marine sediments and other beach areas , with NGS detecting genes and transcripts indicative of pollutant ( monoaromatics and alkanes ) degradation in marine sediments ( Kimes et al . , 2013 ; Mason et al . , 2014 ) and areas along the shorelines ( Lamendella et al . , 2014 ) ."
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