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

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.

[1]  David C. Smith,et al.  Global distribution of microbial abundance and biomass in subseafloor sediment , 2012, Proceedings of the National Academy of Sciences.

[2]  Christopher R. Marks,et al.  Field and laboratory studies on the bioconversion of coal to methane in the San Juan Basin. , 2012, FEMS microbiology ecology.

[3]  S. Tringe,et al.  Metagenome, metatranscriptome and single-cell sequencing reveal microbial response to Deepwater Horizon oil spill , 2012, The ISME Journal.

[4]  J. Groves,et al.  The genome sequence of Desulfatibacillum alkenivorans AK-01: a blueprint for anaerobic alkane oxidation. , 2012, Environmental microbiology.

[5]  Bo Barker Jørgensen,et al.  Deep subseafloor microbial cells on physiological standby , 2011, Proceedings of the National Academy of Sciences.

[6]  J. White,et al.  Metagenomics of the subsurface Brazos-Trinity Basin (IODP site 1320): comparison with other sediment and pyrosequenced metagenomes , 2011, The ISME Journal.

[7]  Folker Meyer,et al.  37. The Metagenomics RAST Server: A Public Resource for the Automatic Phylogenetic and Functional Analysis of Metagenomes , 2011 .

[8]  L. Young,et al.  Dual biomarkers of anaerobic hydrocarbon degradation in historically contaminated groundwater. , 2011, Environmental science & technology.

[9]  David L. Valentine,et al.  A Persistent Oxygen Anomaly Reveals the Fate of Spilled Methane in the Deep Gulf of Mexico , 2011, Science.

[10]  Jonathan L. Ramseur.  Deepwater Horizon Oil Spill: The Fate of the Oil , 2010 .

[11]  T. Treude,et al.  Impact of natural oil and higher hydrocarbons on microbial diversity, distribution, and activity in Gulf of Mexico cold-seep sediments , 2010 .

[12]  P. D’haeseleer,et al.  Deep-Sea Oil Plume Enriches Indigenous Oil-Degrading Bacteria , 2010, Science.

[13]  Yongfei Hu,et al.  Construction and Preliminary Analysis of a Deep-Sea Sediment Metagenomic Fosmid Library from Qiongdongnan Basin, South China Sea , 2010, Marine Biotechnology.

[14]  J. Suflita,et al.  Diversity of benzyl- and alkylsuccinate synthase genes in hydrocarbon-impacted environments and enrichment cultures. , 2010, Environmental science & technology.

[15]  B. Little,et al.  Anaerobic Metabolism of Biodiesel and Its Impact on Metal Corrosion , 2010 .

[16]  J. Suflita,et al.  Subsurface Cycling of Nitrogen and Anaerobic Aromatic Hydrocarbon Biodegradation Revealed by Nucleic Acid and Metabolic Biomarkers , 2010, Applied and Environmental Microbiology.

[17]  Oscar Pizarro,et al.  Spatial Structure and Activity of Sedimentary Microbial Communities Underlying a Beggiatoa spp. Mat in a Gulf of Mexico Hydrocarbon Seep , 2010, PloS one.

[18]  K. Kwon,et al.  Marine, Hydrocarbon-Degrading Alphaproteobacteria , 2010 .

[19]  K. Knittel,et al.  Anaerobic Hydrocarbon-Degrading Microorganisms: An Overview , 2010 .

[20]  F. Rojo.  Enzymes for Aerobic Degradation of Alkanes , 2010 .

[21]  J. Haddock.  18 Aerobic Degradation of Aromatic Hydrocarbons: Enzyme Structures and Catalytic Mechanisms , 2010 .

[22]  F. Widdel,et al.  Biochemistry of the Anaerobic Degradation of Non Methane Alkanes , 2010 .

[23]  K. Timmis.  Handbook of hydrocarbon and lipid microbiology , 2010 .

[24]  Kathleen E. Duncan,et al.  Biocorrosive thermophilic microbial communities in Alaskan North Slope oil facilities. , 2009, Environmental science & technology.

[25]  Franciszek Hasiuk,et al.  Subseafloor sedimentary life in the South Pacific Gyre , 2009, Proceedings of the National Academy of Sciences.

[26]  P. Alvarez,et al.  Field metabolomics and laboratory assessments of anaerobic intrinsic bioremediation of hydrocarbons at a petroleum‐contaminated site , 2009, Microbial biotechnology.

[27]  Andreas Wilke,et al.  phylogenetic and functional analysis of metagenomes , 2022 .

[28]  H. Beller,et al.  Comparative assessments of benzene, toluene, and xylene natural attenuation by quantitative polymerase chain reaction analysis of a catabolic gene, signature metabolites, and compound-specific isotope analysis. , 2008, Environmental science & technology.

[29]  Stephan C Schuster,et al.  Metagenomic signatures of the Peru Margin subseafloor biosphere show a genetically distinct environment , 2008, Proceedings of the National Academy of Sciences.

[30]  Joel Dudley,et al.  MEGA: A biologist-centric software for evolutionary analysis of DNA and protein sequences , 2008, Briefings Bioinform..

[31]  F. Widdel,et al.  Genes encoding the candidate enzyme for anaerobic activation of n-alkanes in the denitrifying bacterium, strain HxN1. , 2008, Environmental microbiology.

[32]  L. Young,et al.  Anaerobic alkane-degrading strain AK-01 contains two alkylsuccinate synthase genes. , 2008, Biochemical and biophysical research communications.

[33]  A. K. Rowan,et al.  Crude-oil biodegradation via methanogenesis in subsurface petroleum reservoirs , 2008, Nature.

[34]  K. Lloyd,et al.  An Anaerobic Methane-Oxidizing Community of ANME-1b Archaea in Hypersaline Gulf of Mexico Sediments , 2006, Applied and Environmental Microbiology.

[35]  K. Timmis,et al.  Genome sequence of the ubiquitous hydrocarbon-degrading marine bacterium Alcanivorax borkumensis , 2006, Nature Biotechnology.

[36]  W. Röling,et al.  Marine microorganisms make a meal of oil , 2006, Nature Reviews Microbiology.

[37]  J. Suflita,et al.  Stable Isotopic Studies of n-Alkane Metabolism by a Sulfate-Reducing Bacterial Enrichment Culture , 2005, Applied and Environmental Microbiology.

[38]  K. Timmis,et al.  Natural microbial diversity in superficial sediments of Milazzo Harbor (Sicily) and community successions during microcosm enrichment with various hydrocarbons. , 2005, Environmental microbiology.

[39]  J. Suflita,et al.  Metabolic Indicators of Anaerobic Hydrocarbon Biodegradation in Petroleum-Laden Environments , 2005 .

[40]  Gerald R. Dickens,et al.  Distributions of Microbial Activities in Deep Subseafloor Sediments , 2004, Science.

[41]  D. Jones,et al.  Anaerobic hydrocarbon biodegradation in deep subsurface oil reservoirs , 2004, Nature.

[42]  Antje Boetius,et al.  The anaerobic oxidation of methane and sulfate reduction in sediments from Gulf of Mexico cold seeps , 2004 .

[43]  S. Giovannoni,et al.  Geobacter metallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals , 2004, Archives of Microbiology.

[44]  S. Harayama,et al.  Alcanivorax which prevails in oil-contaminated seawater exhibits broad substrate specificity for alkane degradation. , 2003, Environmental microbiology.

[45]  M. Hofrichter,et al.  Aerobic Degradation by Microorganisms , 2001 .

[46]  S. Harayama,et al.  Molecular detection of marine bacterial populations on beaches contaminated by the Nakhodka tanker oil-spill accident. , 2001, Environmental microbiology.

[47]  J. Suflita,et al.  Signature metabolites attesting to the in situ attenuation of alkylbenzenes in anaerobic environments. , 2001, Environmental science & technology.

[48]  J. Suflita,et al.  Anaerobic Oxidation of n-Dodecane by an Addition Reaction in a Sulfate-Reducing Bacterial Enrichment Culture , 2000, Applied and Environmental Microbiology.

[49]  S. Harayama,et al.  Petroleum biodegradation in marine environments. , 1999, Journal of molecular microbiology and biotechnology.

[50]  L. Young,et al.  Isolation and Characterization of a Sulfate-Reducing Bacterium That Anaerobically Degrades Alkanes , 1999, Applied and Environmental Microbiology.

[51]  C. Leutwein,et al.  Biochemical and genetic characterization of benzylsuccinate synthase from Thauera aromatica: a new glycyl radical enzyme catalysing the first step in anaerobic toluene metabolism , 1998, Molecular microbiology.

[52]  K. Timmis,et al.  Alcanivorax borkumensis gen. nov., sp. nov., a new, hydrocarbon-degrading and surfactant-producing marine bacterium. , 1998, International journal of systematic bacteriology.

[53]  D. Pelletier,et al.  A cluster of bacterial genes for anaerobic benzene ring biodegradation. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[54]  A. Spormann,et al.  Anaerobic activation of toluene and o-xylene by addition to fumarate in denitrifying strain T , 1997, Journal of bacteriology.

[55]  J. Heider,et al.  Evidence that anaerobic oxidation of toluene in the denitrifying bacterium Thauera aromatica is initiated by formation of benzylsuccinate from toluene and fumarate. , 1996, European journal of biochemistry.

[56]  A. Uitterlinden,et al.  Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA , 1993, Applied and environmental microbiology.

[57]  R. Atlas.  Microbial degradation of petroleum hydrocarbons: an environmental perspective , 1981 .

[58]  R M Atlas,et al.  Microbial degradation of petroleum hydrocarbons: an environmental perspective , 1981, Microbiological reviews.

[59]  O. Lindén,et al.  Ixtoc I; a case study of the world's largest oil spill , 1981 .

[60]  Metagenomic analysis and metabolite profiling of deep-sea 1 sediments from the Gulf of Mexico following the Deepwater Horizon 2 oil spill 3 4 Contributors : , .