Distribution of Hydrocarbon Degradation Pathways in the Sea

  • Rafael Bargiela
  • Michail M. Yakimov
  • Peter N. Golyshin
  • Manuel Ferrer
Reference work entry
Part of the Handbook of Hydrocarbon and Lipid Microbiology book series (HHLM)

Abstract

Petroleum hydrocarbons are one of the most persistent and complex pollutants discharged to environment as a consequence of the human activity, significantly affecting marine and coastal habitats. Some members of microbial communities inhabiting marine ecosystems show the ability to use these hydrocarbons as a preferential carbon source. These compounds are metabolized through different catabolic pathways , leading to their total or partial degradation. Microorganisms are the first responsive component of marine ecosystem after an oil spill. Their contribution may be different depending on the environmental conditions, baseline community setup, and oil composition. Here, we describe how these hydrocarbon-degrading bacteria behave in the marine environment after an oil spill and report on main pathways involved in the degradation of the different hydrocarbons, with a particular focus in the Mediterranean and Red Sea and the Gulf of Mexico as examples.

Notes

Acknowledgments

The authors gratefully acknowledge the financial support provided by the European Community projects KILL-SPILL (FP7-KBBE-2012-312139), MAGICPAH (FP7-KBBE-2009-245226), and ULIXES (FP7-KBBE-2010-266473). This project has received funding from the European Union’s Horizon 2020 research and innovation program [Blue Growth: Unlocking the potential of Seas and Oceans] under grant agreement No [634486]. This work was further funded by grants BIO2011-25012, PCIN-2014-107 (within the ERA NET-IB2 program), and BIO2014-54494-R from the Spanish Ministry of Economy, Industry and Competitiveness. The authors gratefully acknowledge the financial support provided by the European Regional Development Fund (ERDF).

References

  1. Abbasian F, Lockington R, Mallavarapu M, Naidu R (2015) A comprehensive review of aliphatic hydrocarbon biodegradation by bacteria. Appl Biochem Biotechnol 176(3):670–699CrossRefPubMedGoogle Scholar
  2. Acosta-González A, Rosselló-Móra R, Marqués S (2013) Characterization of the anaerobic microbial community in oil-polluted subtidal sediments: aromatic biodegradation potential after the Prestige oil spill. Environ Microbiol 15(1):77–92CrossRefPubMedGoogle Scholar
  3. Al-Awadhi H, Dashti N, Kansour M, Sorkhoh N, Radwan S (2012) Hydrocarbon-utilizing bacteria associated with biofouling materials from offshore waters of the Arabian Gulf. Int Biodeterior Biodegrad 69:10–16CrossRefGoogle Scholar
  4. Awal MR (2009) Environmentally conscious petroleum engineering. In: Kutz M, Elkamel A (eds) Environmentally conscious fossil energy production. Wiley, Hoboken, pp 1–86Google Scholar
  5. Bælum J, Borglin S, Chakraborty R, Fortney JL, Lamendella R, Mason OU, Manfred A, Marcin Z, Markus B, Conrad ME, Malfatti SA, Tringe SG, Hoi-Ying H, Hazen TC, Jansson JK (2012) Deep-sea bacteria enriched by oil and dispersant from the Deepwater Horizon spill. Environ Microbiol 14(9):2405–2416CrossRefPubMedGoogle Scholar
  6. Bargiela R, Mapelli F, Rojo D, Chouaia B, Tornés J, Borin S, Richter M, Del Pozo MV, Cappello S, Gertler C, Genovese M, Denaro R, Martínez-Martínez M, Fodelianakis S, Amer RA, Bigazzi D, Han X, Chen J, Chernikova TN, Golyshina OV, Mahjoubi M, Jaouanil A, Benzha F, Magagnini M, Hussein E, Al-Horani F, Cherif A, Blaghen M, Abdel-Fattah YR, Kalogerakis N, Barbas C, Malkawi HI, Golyshin PN, Yakimov MM, Daffonchio D, Ferrer M (2015) Bacterial population and biodegradation potential in chronically crude oil-contaminated marine sediments are strongly linked to temperature. Sci Rep 5:11651CrossRefPubMedPubMedCentralGoogle Scholar
  7. Benassi M, Berisha A, Romão W, Babayev E, Römpp A, Spengler B (2013) Petroleum crude oil analysis using low-temperature plasma mass spectrometry. Rapid Commun Mass Spectrom 27(7):825–834CrossRefPubMedGoogle Scholar
  8. Boll M, Fuch G, Heider J (2002) Anaerobic oxidation of aromatic compounds and hydrocarbons. Curr Opin Chem Biol 6(5):604–611CrossRefPubMedGoogle Scholar
  9. Boll M, Löffler C, Morris BEL, Kung JW (2014) Anaerobic degradation of homocyclic aromatic compounds via arylcarboxyl-coenzyme A esters: organisms, strategies and key enzymes. Environ Microbiol 16(3):612–627CrossRefPubMedGoogle Scholar
  10. Cappello S, Caruso G, Zampino D, Monticelli LS, Maimone G, Denaro R, Tripodo B, Troussellier M, Yakimov MM, Giuliano L (2007a) Microbial community dynamics during assays of harbour oil spill bioremediation: a microscale simulation study. J Appl Microbiol 102(1):184–194CrossRefPubMedGoogle Scholar
  11. Cappello S, Denaro R, Genovese M, Giuliano L, Yakimov MM (2007b) Predominant growth of Alcanivorax during experiments on “oil spill bioremediation” in mesocosms. Microbiol Res 162(2):185–190CrossRefPubMedGoogle Scholar
  12. Carmona M, Zamarro MT, Blázquez B, Durante-Rodríguez G, Juárez JF, Valderrama JA, Barragán MJL, García JL, Díaz E (2009) Anaerobic catabolism of aromatic compounds: a genetic and genomic view. Microbiol Mol Biol Rev 73(1):71–133CrossRefPubMedPubMedCentralGoogle Scholar
  13. Cirera L, Cirarda F, Palència L, Estarlich M, Montes-Martínez A, Lorenzo P, Daponte-Codina A, López-Abente G (2012) Mortality due to haematological cancer in cities close to petroleum refineries in Spain. Environ Sci Pollut Res 20(1):591–596CrossRefGoogle Scholar
  14. Daffonchio D, Ferrer M, Mapelli F, Cherif A, Lafraya A, Malkawi HI, Yakimov MM, Abdel-Fattah YR, Blaghen M, Golyshin PN, Kalogerakis N, Boon N, Magagnini M, Fava F (2013) Bioremediation of Southern Mediterranean oil polluted sites comes of age. New Biotechnol 30(6):743–748CrossRefGoogle Scholar
  15. Das N, Chandran P (2011) Microbial degradation of petroleum hydrocarbon contaminants: an overview. Biotechnol Res Int 2011:941810Google Scholar
  16. Díaz E, Jiménez JI, Nogales J (2013) Aerobic degradation of aromatic compounds. Curr Opin Biotechnol 24(3):431–442CrossRefPubMedGoogle Scholar
  17. Duarte M, Jauregui R, Vilchez-Vargas R, Junca H, Pieper DH (2014) AromaDeg, a novel database for phylogenomics of aerobic bacterial degradation of aromatics. Database (Oxford) 2014:bau118Google Scholar
  18. Dyksterhouse SE, Gray JP, Herwig RP, Lara JC, Staley JT (1995) Cycloclasticus pugetii gen. nov., sp. nov., an aromatic hydrocarbon-degrading bacterium from marine sediments. Int J Syst Bacteriol 45(1):116–123CrossRefPubMedGoogle Scholar
  19. Fathepure BZ (2014) Recent studies in microbial degradation of petroleum hydrocarbons in hypersaline environments. Front Microbiol 5:173CrossRefPubMedPubMedCentralGoogle Scholar
  20. Fetzner S (2012) Ring-cleaving dioxygenases with a cupin fold. Appl Environ Microbiol 78(8):2505–2514CrossRefPubMedPubMedCentralGoogle Scholar
  21. Foght J (2008) Anaerobic biodegradation of aromatic hydrocarbons: pathways and prospects. J Mol Microbiol Biotechnol 15(2–3):93–120CrossRefPubMedGoogle Scholar
  22. Fuchs G (2008) Anaerobic metabolism of aromatic compounds. Ann N Y Acad Sci 1125(1):82–99CrossRefPubMedGoogle Scholar
  23. Fuchs G, Boll M, Heider J (2011) Microbial degradation of aromatic compounds – from one strategy to four. Nat Rev Microbiol 9(11):803–816CrossRefPubMedGoogle Scholar
  24. Fuentes S, Méndez V, Aguila P, Seeger M (2014) Bioremediation of petroleum hydrocarbons: catabolic genes, microbial communities, and applications. Appl Microbiol Biotechnol 98(11):4781–4794CrossRefPubMedGoogle Scholar
  25. Gallego S, Vila J, Tauler M, Nieto JM, Breugelmans P, Springael D, Grifoll M (2014) Community structure and PAH ring-hydroxylating dioxygenase genes of a marine pyrene-degrading microbial consortium. Biodegradation 25(4):543–556CrossRefPubMedGoogle Scholar
  26. Genovese M, Crisafi F, Denaro R, Cappello S, Russo D, Calogero R, Santisi S, Catalfamo M, Modica A, Smedile F, Genovese L, Golyshin PN, Giuliano L, Yakimov MM (2014) Effective bioremediation strategy for rapid in situ cleanup of anoxic marine sediments in mesocosm oil spill simulation. Front Microbiol 5:162CrossRefPubMedPubMedCentralGoogle Scholar
  27. Gertler C, Gerdts G, Timmis KN, Yakimov MM, Golyshin PN (2009) Populations of heavy fuel oil-degrading marine microbial community in presence of oil sorbent materials. J Appl Microbiol 107(2):590–605CrossRefPubMedGoogle Scholar
  28. Gillespie IMM, Philp JC (2013) Bioremediation, an environmental remediation technology for the bioeconomy. Trends Biotechnol 31(6):329–332CrossRefPubMedGoogle Scholar
  29. Golyshin PN, Chernikova TN, Abraham W-R, Lünsdorf H, Timmis KN, Yakimov MM (2002) Oleiphilaceae fam. nov., to include Oleiphilus messinensis gen. nov., sp. nov., a novel marine bacterium that obligately utilizes hydrocarbons. Int J Syst Evol Microbiol 52(3):901–911PubMedGoogle Scholar
  30. Golyshin PN, VAP MDS, Kaiser O, Ferrer M, Sabirova YS, Lünsdorf H, Chernikova TN, Golyshina OV, Yakimov MM, Pühler A, Timmis KN (2003) Genome sequence completed of Alcanivorax borkumensis, a hydrocarbon-degrading bacterium that plays a global role in oil removal from marine systems. J Biotechnol 106(2–3):215–220CrossRefPubMedGoogle Scholar
  31. Gutierrez T1, Green DH, Whitman WB, Nichols PD, Semple KT, Aitken MD (2012a). Algiphilus aromaticivorans gen. nov., sp. nov., an aromatic hydrocarbon-degrading bacterium isolated from a culture of the marine dinoflagellate Lingulodinium polyedrum, and proposal of Algiphilaceae fam. nov. Int J Syst Evol Microbiol, 62(Pt 11): 2743–2749.Google Scholar
  32. Gutierrez T, Nichols PD, Whitman WB, Aitken MD (2012b) Porticoccus hydrocarbonoclasticus sp. nov., an aromatic hydrocarbon-degrading bacterium identified in laboratory cultures of marine phytoplankton. Appl Environ Microbiol 78(3):628–637CrossRefPubMedPubMedCentralGoogle Scholar
  33. Gutierrez T, Green DH, Nichols PD, Whitman WB, Semple KT, Aitken MD (2013b) Polycyclovorans algicola gen. nov., sp. nov., an aromatic-hydrocarbon-degrading marine bacterium found associated with laboratory cultures of marine phytoplankton. Appl Environ Microbiol 79(1):205–214CrossRefPubMedPubMedCentralGoogle Scholar
  34. Gutierrez T, Singleton DR, Berry D, Yang T, Aitken MD, Teske A (2013a). Hydrocarbon-degrading bacteria enriched by the Deepwater Horizon oil spill identified by cultivation and DNA-SIP. ISME J 7(11): 2091–2104.Google Scholar
  35. Gutierrez T, Thompson HF, Angelova A, Whitman WB, Huntemann M, Copeland A, Chen A, Kyrpides N, Markowitz V, Palaniappan K, Ivanova N, Mikhailova N, Ovchinnikova G, Andersen E, Pati A, Stamatis D, Reddy TB, Ngan CY, Chovatia M, Daum C, Shapiro N, Cantor MN, Woyke T (2015a) Genome aequence of Polycyclovorans algicola strain TG408, an obligate polycyclic aromatic hydrocarbon-degrading bacterium associated with marine eukaryotic phytoplankton. Genome Announc 3(2) pii: e00207-15Google Scholar
  36. Gutierrez T, Whitman WB, Huntemann M, Copeland A, Chen A, Kyrpides N, Markowitz V, Pillay M, Ivanova N, Mikhailova N, Ovchinnikova G, Andersen E, Pati A, Stamatis D, Reddy TB, Ngan CY, Chovatia M, Daum C, Shapiro N, Cantor MN, Woyke T (2015b). Genome sequence of Porticoccus hydrocarbonoclasticus strain MCTG13d, an obligate polycyclic aromatic hydrocarbon-degrading bacterium associated with Marine eukaryotic phytoplankton. Genome Announc 18;3(3) pii: e00672-15.Google Scholar
  37. Harayama S, Kasai Y, Hara A (2004) Microbial communities in oil-contaminated seawater. Curr Opin Biotechnol 15(3):205–214CrossRefPubMedGoogle Scholar
  38. Hawley ER, Piao H, Scott NM, Malfatti S, Pagani I, Huntemann M, Chen A, Glavina del Rio T, Foster B, Copeland A, Jansson J, Pati A, Tringe S, Gilbert JA, Lorenson TD, Hess M (2014) Metagenomic analysis of microbial consortium from natural crude oil that seeps into the marine ecosystem offshore Southern California. Stand Genomic Sci 9(3):1259–1274CrossRefPubMedPubMedCentralGoogle Scholar
  39. Head IM (1998) Bioremediation: towards a credible technology. Microbiology 144(3):599–608CrossRefGoogle Scholar
  40. Head IM, Jones DM, Röling WFM (2006) Marine microorganisms make a meal of oil. Nat Rev Microbiol 4(3):173–182CrossRefPubMedGoogle Scholar
  41. Hedlund BP, Geiselbrecht AD, Bair TJ, Staley JT (1999) Polycyclic aromatic hydrocarbon degradation by a new marine bacterium, Neptunomonas naphthovorans gen. nov., sp. nov. Appl Environ Microbiol 65(1):251–259PubMedPubMedCentralGoogle Scholar
  42. Heider J (2007) Adding handles to unhandy substrates: anaerobic hydrocarbon activation mechanisms. Curr Opin Chem Biol 11(2):188–194CrossRefPubMedGoogle Scholar
  43. Jiménez N, Viñas M, Guiu-Aragonés C, Bayona JM, Albaigés J, Solanas AM (2011) Polyphasic approach for assessing changes in an autochthonous marine bacterial community in the presence of Prestige fuel oil and its biodegradation potential. Appl Microbiol Biotechnol 91(3):823–834CrossRefPubMedGoogle Scholar
  44. Jones DM, Head IM, Gray ND, Adams JJ, Rowan AK, Aitken CM, Bennett B, Huang H, Brown A, Bowler BFJ, Oldenburg T, Erdmann M, Larter SR (2008) Crude-oil biodegradation via methanogenesis in subsurface petroleum reservoirs. Nature 451(7175):176–180CrossRefPubMedGoogle Scholar
  45. Jurelevicius D, Couto CRA, Alvarez VM, Vollú RE, FdA D, Seldin L (2014) Response of the archaeal community to simulated petroleum hydrocarbon contamination in marine and hypersaline ecosystems. Water Air Soil Pollut 225(2):1–12CrossRefGoogle Scholar
  46. Kasai Y1, Kishira H, Harayama S. Bacteria belonging to the genus Cycloclasticus play a primary role in the degradation of aromatic hydrocarbons released in a marine environment (2002). Appl Environ Microbiol, 68(11): 5625–5633.Google Scholar
  47. Khelifi N, Amin Ali O, Roche P, Grossi V, Brochier-Armanet C, Valette O, Ollivier B, Hirschler-Réa A (2014). Anaerobic oxidation of long-chain n-alkanes by the hyperthermophilic sulfate-reducing archaeon, Archaeoglobus fulgidus. ISME J 8(11): 2153–2166.Google Scholar
  48. Kimes NE, Callaghan AV, Aktas DF, Smith WL, Sunner J, Golding B, Drozdowska M, Morris PJ (2013) Metagenomic analysis and metabolite profiling of deep-sea sediments from the Gulf of Mexico following the Deepwater Horizon oil spill. Front Microbiol 4:50CrossRefPubMedPubMedCentralGoogle Scholar
  49. Kimes NE, Callaghan AV, Suflita JM, Morris PJ (2014) Microbial transformation of the Deepwater Horizon oil spill – past, present, and future perspectives. Front Microbiol 5:603CrossRefPubMedPubMedCentralGoogle Scholar
  50. King GM, Kostka JE, Hazen TC, Sobecky PA (2015) Microbial responses to the Deepwater Horizon Oil Spill: from coastal wetlands to the deep sea. Annu Rev Mar Sci 7(1):377–401CrossRefGoogle Scholar
  51. Kniemeyer O, Musat F, Sievert SM, Knittel K, Wilkes H, Blumenberg M, Michaelis W, Classen A, Bolm C, Joye SB, Widdel F (2007) Anaerobic oxidation of short-chain hydrocarbons by marine sulphate-reducing bacteria. Nature 449(7164):898–901CrossRefPubMedGoogle Scholar
  52. Kostka JE, Prakash O, Overholt WA, Green SJ, Freyer G, Canion A, Delgardio J, Norton N, Hazen TC, Huettel M (2011) Hydrocarbon-degrading bacteria and the bacterial community response in Gulf of Mexico beach sands impacted by the Deepwater Horizon oil spill. Appl Environ Microbiol 77(22):7962–7974CrossRefPubMedPubMedCentralGoogle Scholar
  53. Lanfranconi MP, Bosch R, Nogales B (2010) Short-term changes in the composition of active marine bacterial assemblages in response to diesel oil pollution. Microb Biotechnol 3(5):607–621CrossRefPubMedPubMedCentralGoogle Scholar
  54. Li H, Liu YH, Luo N, Zhang XY, Luan TG, JM H, Wang ZY, PC W, Chen MJ, JQ L (2006) Biodegradation of benzene and its derivatives by a psychrotolerant and moderately haloalkaliphilic Planococcus sp. strain ZD22. Res Microbiol 157(7):629–636CrossRefPubMedGoogle Scholar
  55. Liu Z, Liu J (2013) Evaluating bacterial community structures in oil collected from the sea surface and sediment in the northern Gulf of Mexico after the Deepwater Horizon oil spill. Microbiologyopen 2(3):492–504CrossRefPubMedPubMedCentralGoogle Scholar
  56. Lu Z, Deng Y, Van Nostrand JD, He Z, Voordeckers J, Zhou A, Lee Y-J, Mason OU, Dubinky EA, Chavarria KL, Tom LM, Fortney JL, Lamendella R, Jansson JK, D’haeseller P, Hazen TC, Zhou J (2011) Microbial gene functions enriched in the Deepwater Horizon deep-sea oil plume. ISME J 6(2):451–460CrossRefPubMedPubMedCentralGoogle Scholar
  57. Luo Y-R, Tian Y, Huang X, Kwon K, Yang S-H, Seo H-S, Kim S-J, Zheng T-L (2012) Sphingomonas polyaromaticivorans sp. nov., a polycyclic aromatic hydrocarbon-degrading bacterium from an oil port water sample. Int J Syst Evol Microbiol 62(6):1223–1227CrossRefPubMedGoogle Scholar
  58. Luo F, Gitiafroz R, Devine CE, Gong Y, Hug LA, Raskin L, Edwards EA (2014) Metatranscriptome of an anaerobic benzene-degrading, nitrate-reducing enrichment culture reveals involvement of carboxylation in benzene ring activation. Appl Environ Microbiol 80(14):4095–4107CrossRefPubMedPubMedCentralGoogle Scholar
  59. Ma J, Deng Y, Yuan T, Zhou J, Alvarez PJJ (2015) Succession of microbial functional communities in response to a pilot-scale ethanol-blended fuel release throughout the plume life cycle. Environ Pollut 198:154–160CrossRefPubMedGoogle Scholar
  60. Manilla-Pérez E, Lange AB, Hetzler S, Steinbüchel A (2010) Occurrence, production, and export of lipophilic compounds by hydrocarbonoclastic marine bacteria and their potential use to produce bulk chemicals from hydrocarbons. Appl Microbiol Biotechnol 86(6):1693–1706CrossRefPubMedGoogle Scholar
  61. Marshall AG, Rodgers RP (2004) Petroleomics: the next grand challenge for chemical analysis. Acc Chem Res 37(1):53–59CrossRefPubMedGoogle Scholar
  62. Mason OU, Hazen TC, Borglin S, Chain PSG, Dubinsky EA, Fortney JL, Han J, Holman H-YN, Hultman J, Lamendella R, Mackelprag R, Malfatti S, Tom LM, Tringe SG, Woyke T, Zhou J, Rubin EM, Jansson JK (2012) Metagenome, metatranscriptome and single-cell sequencing reveal microbial response to Deepwater Horizon oil spill. ISME J 6(9):1715–1727CrossRefPubMedPubMedCentralGoogle Scholar
  63. Mason OU, Scott NM, Gonzalez A, Robbins-Pianka A, Baelum J, Kimbrel J, Bouskill NJ, Prestat E, Borglin S, Joyner DC, Fortney JL, Jurelevicius D, Stringfellow WT, Álvarez-Cohen L, Hazen TC, Knight R, Gilbert JA, Jansson JK (2014) Metagenomics reveals sediment microbial community response to Deepwater Horizon oil spill. ISME J 8(7):1464–1475CrossRefPubMedPubMedCentralGoogle Scholar
  64. McGenity TJ, Folwell BD, McKew BA, Sanni GO (2012) Marine crude-oil biodegradation: a central role for interspecies interactions. Aquat Biosyst 8:10CrossRefPubMedPubMedCentralGoogle Scholar
  65. Meckenstock RU, Mouttaki H (2011) Anaerobic degradation of non-substituted aromatic hydrocarbons. Curr Opin Biotechnol 22(3):406–414CrossRefPubMedGoogle Scholar
  66. Meckenstock RU, Boll M, Mouttaki H, Koelschbach JS, Cunha Tarouco P, Weyrauch P, Dong X, Himmelberg AM (2016) Anaerobic degradation of benzene and polycyclic aromatic hydrocarbons. J Mol Microbiol Biotechnol 26(1–3):92–118CrossRefPubMedGoogle Scholar
  67. Messina E, Denaro R, Crisafi F, Smedile F, Cappello S, Genovese M, Genovese L, Giuliano L, Russo D, Ferrer M, Golyshin PN, Yakimov MM (2016) Genome sequence of obligate marine polycyclic aromatic hydrocarbons-degrading bacterium Cycloclasticus sp. 78-ME, isolated from petroleum deposits of the sunken tanker Amoco Milford Haven, Mediterranean Sea. Mar Genomics 25:11–13CrossRefPubMedGoogle Scholar
  68. Montagnolli RN, Lopes PRM, Bidoia ED (2014) Screening the toxicity and biodegradability of petroleum hydrocarbons by a rapid colorimetric method. Arch Environ Contam Toxicol 68(2):342–353CrossRefPubMedGoogle Scholar
  69. Nogales B, Lanfranconi MP, Piña-Villalonga JM, Bosch R (2011) Anthropogenic perturbations in marine microbial communities. FEMS Microbiol Rev 35(2):275–298CrossRefPubMedGoogle Scholar
  70. Oil in the Sea III: Inputs, Fates, and Effects (2003) The National Academy Press (ed). Washington, DCGoogle Scholar
  71. Omokoko B, Jäntges UK, Zimmermann M, Reiss M, Hartmeier W (2008) Isolation of the phe-operon from G. stearothermophilus comprising the phenol degradative meta-pathway genes and a novel transcriptional regulator. BMC Microbiol 8:197CrossRefPubMedPubMedCentralGoogle Scholar
  72. Païssé S, Goñi-Urriza M, Coulon F, Duran R (2010) How a bacterial community originating from a contaminated coastal sediment responds to an oil input. Microb Ecol 60(2):394–405CrossRefPubMedGoogle Scholar
  73. Paissé S, Goñi-Urriza M, Stadler T, Budzinski H, Duran R (2012) Ring-hydroxylating dioxygenase (RHD) expression in a microbial community during the early response to oil pollution. FEMS Microbiol Ecol 80(1):77–86CrossRefPubMedGoogle Scholar
  74. Peng R-H, Xiong A-S, Xue Y, X-Y F, Gao F, Zhao W, Tian Y-S, Yao Q-H (2008) Microbial biodegradation of polyaromatic hydrocarbons. FEMS Microbiol Rev 32(6):927–955CrossRefPubMedGoogle Scholar
  75. Philipp B, Schink B (2012) Different strategies in anaerobic biodegradation of aromatic compounds: nitrate reducers versus strict anaerobes. Environ Microbiol Rep 4(5):469–478CrossRefPubMedGoogle Scholar
  76. Prosser CM, Redman AD, Prince RC, Paumen ML, Letinski DJ, Butler JD (2016) Evaluating persistence of petroleum hydrocarbons in aerobic aqueous media. Chemosphere 155:542–549CrossRefPubMedGoogle Scholar
  77. Reddy CM, Eglinton TI, Hounshell A, White HK, Xu L, Gaines RB, Frysinger GS (2002) The West Falmouth oil spill after thirty years: the persistence of petroleum hydrocarbons in Marsh sediments. Environ Sci Technol 36(22):4754–4760CrossRefPubMedGoogle Scholar
  78. Redmond MC, Valentine DL (2012) Natural gas and temperature structured a microbial community response to the Deepwater Horizon oil spill. Proc Natl Acad Sci 109(50):20292–20297CrossRefPubMedGoogle Scholar
  79. Reis I, Almeida CMR, Magalhães CM, Cochofel J, Guedes P, Basto MCP, Bordalo AA, Mucha AP (2013) Bioremediation potential of microorganisms from a sandy beach affected by a major oil spill. Environ Sci Pollut Res 21(5):3634–3645CrossRefGoogle Scholar
  80. Rodriguez-R LM, Overholt WA, Hagan C, Huettel M, Kostka JE, Konstantinidis KT (2015) Microbial community successional patterns in beach sands impacted by the Deepwater Horizon oil spill. ISME J 9(9):1928–1940CrossRefPubMedPubMedCentralGoogle Scholar
  81. Rojo F (2009) Degradation of alkanes by bacteria. Environ Microbiol 11(10):2477–2490CrossRefPubMedGoogle Scholar
  82. Ron EZ, Rosenberg E (2014) Enhanced bioremediation of oil spills in the sea. Curr Opin Biotechnol 27:191–194CrossRefPubMedGoogle Scholar
  83. Sammarco PW, Kolian SR, Warby RAF, Bouldin JL, Subra WA, Porter SA (2013) Distribution and concentrations of petroleum hydrocarbons associated with the BP/Deepwater Horizon oil spill, Gulf of Mexico. Mar Pollut Bull 73(1):129–143CrossRefPubMedGoogle Scholar
  84. Sauret C, Christaki U, Moutsaki P, Hatzianestis I, Gogou A, Ghiglione J-F (2012) Influence of pollution history on the response of coastal bacterial and nanoeukaryote communities to crude oil and biostimulation assays. Mar Environ Res 79:70–78CrossRefPubMedGoogle Scholar
  85. Sauret C, Séverin T, Vétion G, Guigue C, Goutx M, Pujo-Pay M, Conan P, Fagervold SK, Ghiglione J-F (2014) “Rare biosphere” bacteria as key phenanthrene degraders in coastal seawaters. Environ Pollut 194:246–253CrossRefPubMedGoogle Scholar
  86. Stout SA, Payne JR, Emsbo-Mattingly SD, Baker G (2016) Weathering of field-collected floating and stranded Macondo oils during and shortly after the Deepwater Horizon oil spill. Mar Pollut Bull 105(1):7–22CrossRefPubMedGoogle Scholar
  87. Szaleniec M, Dudzik A, Kozik B, Borowski T, Heider J, Witko M (2014) Mechanistic basis for the enantioselectivity of the anaerobic hydroxylation of alkylaromatic compounds by ethylbenzene dehydrogenase. J Inorg Biochem 139:9–20CrossRefPubMedGoogle Scholar
  88. Tapilatu Y, Acquaviva M, Guigue C, Miralles G, Bertrand J-C, Cuny P (2010) Isolation of alkane-degrading bacteria from deep-sea Mediterranean sediments. Lett Appl Microbiol 50(2):234–236CrossRefPubMedGoogle Scholar
  89. Tomás-Gallardo L, Gómez-Álvarez H, Santero E, Floriano B (2014) Combination of degradation pathways for naphthalene utilization in Rhodococcus sp. strain TFB. Microb Biotechnol 7(2):100–113CrossRefPubMedGoogle Scholar
  90. Torres Pazmiño DE, Winkler M, Glieder A, Fraaije MW (2010) Monooxygenases as biocatalysts: classification, mechanistic aspects and biotechnological applications. J Biotechnol 146(1–2):9–24CrossRefPubMedGoogle Scholar
  91. Townsend GT, Prince RC, Suflita JM (2003) Anaerobic oxidation of crude oil hydrocarbons by the resident microorganisms of a contaminated anoxic aquifer. Environ Sci Technol 37(22):5213–5218CrossRefPubMedGoogle Scholar
  92. Tsitou P, Heneweer M, Boogaard PJ (2015) Toxicogenomics in vitro as an alternative tool for safety evaluation of petroleum substances and PAHs with regard to prenatal developmental toxicity. Toxicol In Vitro 29(2):299–307CrossRefPubMedGoogle Scholar
  93. Vaillancourt FH, Bolin JT, Eltis LD (2006) The ins and outs of ring-cleaving dioxygenases. Crit Rev Biochem Mol Biol 41(4):241–267CrossRefPubMedGoogle Scholar
  94. Valderrama JA, Durante-Rodríguez G, Blázquez B, García JL, Carmona M, Díaz E (2012) Bacterial degradation of benzoate. J Biol Chem 287(13):10494–10508CrossRefPubMedPubMedCentralGoogle Scholar
  95. Vila J, Nieto JM, Mertens J, Springael D, Grifoll M (2010) Microbial community structure of a heavy fuel oil-degrading marine consortium: linking microbial dynamics with polycyclic aromatic hydrocarbon utilization. FEMS Microbiol Ecol 73(2):349–362PubMedGoogle Scholar
  96. Wang W, Zhong R, Shan D, Shao Z (2014) Indigenous oil-degrading bacteria in crude oil-contaminated seawater of the Yellow sea, China. Appl Microbiol Biotechnol 98(16):7253–7269CrossRefPubMedGoogle Scholar
  97. Wang H, Wang B, Dong W, Hu X (2016) Co-acclimation of bacterial communities under stresses of hydrocarbons with different structures. Sci Rep 6:34588CrossRefPubMedPubMedCentralGoogle Scholar
  98. Widdel F, Knittel K, Galushko (2010) Anaerobic hydrocarbon-degrading microorganisms: an overview. In: Eckey C, Fabiani S (eds) Handbook of hydrocarbon and lipid microbiology. Springer-Verlag, Heidelberg. Berlin Heidelberg, pp 1997–2023CrossRefGoogle Scholar
  99. Xue J, Yu Y, Bai Y, Wang L, Wu Y (2015) Marine oil-degrading microorganisms and biodegradation process of petroleum hydrocarbon in marine environments: a review. Curr Microbiol 71(2):220–228CrossRefPubMedGoogle Scholar
  100. Yakimov MM, Golyshin PN, Lang S, Moore ERB, Abraham W-R, Lünsdorf H, Timmis KN (1998) Alcanivorax borkumensis gen. nov., sp. nov., a new, hydrocarbon-degrading and surfactant-producing marine bacterium. Int J Syst Bacteriol 48(2):339–348CrossRefPubMedGoogle Scholar
  101. Yakimov MM, Giuliano L, Gentile G, Crisafi E, Chernikova TN, Abraham W-R, Lünsdorf H, Timmis KN, Golyshin PN (2003) Oleispira antarctica gen. nov., sp. nov., a novel hydrocarbonoclastic marine bacterium isolated from Antarctic coastal sea water. Int J Syst Evol Microbiol 53(3):779–785CrossRefPubMedGoogle Scholar
  102. Yakimov MM, Giuliano L, Denaro R, Crisafi E, Chernikova TN, Abraham W-R, Lünsdorf H, Timmis KN, Golyshin PN (2004) Thalassolituus oleivorans gen. nov., sp. nov., a novel marine bacterium that obligately utilizes hydrocarbons. Int J Syst Evol Microbiol 54(1):141–148CrossRefPubMedGoogle Scholar
  103. Yakimov MM, Denaro R, Genovese M, Cappello S, D’Auria G, Chernikova TN, Timmis KN, Golyshin PN, Giluliano L (2005) Natural microbial diversity in superficial sediments of Milazzo Harbor (Sicily) and community successions during microcosm enrichment with various hydrocarbons. Environ Microbiol 7(9):1426–1441CrossRefPubMedGoogle Scholar
  104. Yakimov MM, Timmis KN, Golyshin PN (2007) Obligate oil-degrading marine bacteria. Curr Opin Biotechnol 18(3):257–266CrossRefPubMedGoogle Scholar
  105. Yang H-Y, Jia R-B, Chen B, Li L (2014) Degradation of recalcitrant aliphatic and aromatic hydrocarbons by a dioxin-degrader Rhodococcus sp. strain p52. Environ Sci Pollut Res 21(18):11086–11093CrossRefGoogle Scholar
  106. Yim UH, Ha SY, An JG, Won JH, Han GM, Hong SH, Kim M, Jung J-H, Shim WJ (2011) Fingerprint and weathering characteristics of stranded oils after the Hebei Spirit oil spill. J Hazard Mater 197:60–69CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2017

Authors and Affiliations

  • Rafael Bargiela
    • 1
  • Michail M. Yakimov
    • 2
    • 3
  • Peter N. Golyshin
    • 3
    • 4
  • Manuel Ferrer
    • 5
  1. 1.Institute of Catalysis, Consejo Superior de Investigaciones Científicas (CSIC)MadridSpain
  2. 2.Institute for Coastal Marine Environment, CNRMessinaItaly
  3. 3.Immanuel Kant Baltic Federal UniversityKaliningradRussia
  4. 4.School of Biological SciencesUniversity of BangorBangor, GwyneddUK
  5. 5.CSIC, Institute of Catalysis, Dept. of Applied BiocatalysisMadridSpain

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