Microbial Ecology

, Volume 64, Issue 3, pp 605–616 | Cite as

Alkane Biodegradation Genes from Chronically Polluted Subantarctic Coastal Sediments and Their Shifts in Response to Oil Exposure

  • Lilian M. Guibert
  • Claudia L. Loviso
  • Magalí S. Marcos
  • Marta G. Commendatore
  • Hebe M. Dionisi
  • Mariana Lozada
Microbiology of Aquatic Systems


Although sediments are the natural hydrocarbon sink in the marine environment, the ecology of hydrocarbon-degrading bacteria in sediments is poorly understood, especially in cold regions. We studied the diversity of alkane-degrading bacterial populations and their response to oil exposure in sediments of a chronically polluted Subantarctic coastal environment, by analyzing alkane monooxygenase (alkB) gene libraries. Sequences from the sediment clone libraries were affiliated with genes described in Proteobacteria and Actinobacteria, with 67 % amino acid identity in average to sequences from isolated microorganisms. The majority of the sequences were most closely related to uncultured microorganisms from cold marine sediments or soils from high latitude regions, highlighting the role of temperature in the structuring of this bacterial guild. The distribution of alkB sequences among samples of different sites and years, and selection after experimental oil exposure allowed us to identify ecologically relevant alkB genes in Subantarctic sediments, which could be used as biomarkers for alkane biodegradation in this environment. 16 S rRNA amplicon pyrosequencing indicated the abundance of several genera for which no alkB genes have yet been described (Oleispira, Thalassospira) or that have not been previously associated with oil biodegradation (Spongiibacter—formerly Melitea—, Maribius, Robiginitomaculum, Bizionia and Gillisia). These genera constitute candidates for future work involving identification of hydrocarbon biodegradation pathway genes.


Rhodococcus Marinobacter Unresolved Complex Mixture Nocardioides Hydrocarbon Biodegradation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



LMG, CLL and MSM are recipients of graduate student fellowships from the National Research Council of Argentina (CONICET). ML, HMD and MGC are staff members from CONICET. Grants from CONICET, National Agency for the Promotion of Science and Technology (ANPCyT, Argentina) and Secretary of Science, Technology and Innovation of the Chubut Province (Argentina) supported this research.

We would like to thank M. Gil, J. L. Esteves, H. Ocariz, A. Torres and R. Vera for their help during sample collection.

Supplementary material

248_2012_51_MOESM1_ESM.pdf (225 kb)
Online Resource 1 Hydrocarbon content and alkB PCR clone library information of coastal sediment samples from Ushuaia Bay. (PDF 225 kb)
248_2012_51_MOESM2_ESM.pdf (103 kb)
Online Resource 2 Alignment of deduced AlkB sequences from clones obtained in this study and related sequences from public databases. Only one representative sequence per OTU is shown. The conserved histidine box II [72, 73] is indicated. The beginning of histidine box II in the sequences from this study is not included, as it was included in the forward primer [54]. Residues ≥50% identical and similar are shaded in black and gray, respectively. CLUSTAL, MEGA5 and BioEdit softwares were used to build and shade the alignment. (PDF 102 kb)
248_2012_51_MOESM3_ESM.pdf (68 kb)
Online Resource 3 BLAST results of the alkB gene OTUs identified in this study. OTUs are ordered by relative abundances. For each OTU, the first BLAST match and the sequence from the closest isolated microorganism is indicated, with GenBank accession numbers in parentheses. Percent identity at the amino acid level is shown. N: number of sequences in the OTU; n: number of samples where the OTU was detected; samples correspond to: S (sediment), O (oil-exposed slurry), ON (oil-plus-nutrient amended slurry). (PDF 67 kb)
248_2012_51_MOESM4_ESM.pdf (90 kb)
Online Resource 4 Profiles obtained by high resolution gas chromatography of the aliphatic hydrocarbon fraction of sediments and experimental systems. a. OR08 sediment sample from Ushuaia Bay. b. crude oil added to the experimental systems. c. oil-exposed slurry (expOR08-O) after twenty days of exposure. d. oil-plus-nutrient amended slurry (expOR08-ON) after twenty days of exposure. e. control slurry (expOR08-c, neither oil nor nutrients added) after twenty days. Representative compound abbreviations are indicated above the corresponding peaks. UCM: unresolved complex mixture. (PDF 90 kb)


  1. 1.
    Marshall AG, Rodgers RP (2008) Petroleomics: chemistry of the underworld. Proc Natl Acad Sci 105:18090–18095PubMedCrossRefGoogle Scholar
  2. 2.
    NRC National Research Council (2003) Oil in the sea III: inputs, fates and effects. National Academies Press, Washington, D.CGoogle Scholar
  3. 3.
    Peterson CH, Rice SD, Short JW, Esler D, Bodkin JL, Ballachey BE, Irons DB (2003) Long-term ecosystem response to the Exxon Valdez oil spill. Science 302:2082–2086PubMedCrossRefGoogle Scholar
  4. 4.
    Short JW, Maselko JM, Lindeberg MR, Harris PM, Rice SD (2006) Vertical distribution and probability of encountering intertidal Exxon Valdez oil on shorelines of three embayments within Prince William Sound, Alaska. Environ Sci Technol 40:3723–3729PubMedCrossRefGoogle Scholar
  5. 5.
    Short JW, Irvine GV, Mann DH, Maselko JM, Pella JJ, Lindeberg MR, Payne JR, Driskell WB, Rice SD (2007) Slightly weathered Exxon Valdez oil persists in Gulf of Alaska beach sediments after 16 years. Environ Sci Technol 41:1245–1250PubMedCrossRefGoogle Scholar
  6. 6.
    Irvine GV, Mann DH, Short JW (2006) Persistence of 10-year old Exxon Valdez oil on Gulf of Alaska beaches: the importance of boulder-armoring. Mar Pollut Bull 52:1011–1022PubMedCrossRefGoogle Scholar
  7. 7.
    Atlas RM (2010) Microbial bioremediation in polar environments: current status and future directions. In: Bej AK, Aislabie J, Atlas RM (eds) Polar microbiology: the ecology, biodiversity and bioremediation potential of microorganisms in extremely cold environments. CRC Press, Boca Raton, pp 373–391Google Scholar
  8. 8.
    Coulon F, Chronopoulou P-M, Fahy A, Paissé S, Goñi-Urriza M, Peperzak L, Acuña Alvarez L, McKew BA, Brussaard CPD, Underwood GJC, Timmis KN, Duran R, McGenity TJ (2012) Hydrocarbon biodegradation in coastal mudflats: the central role of dynamic tidal biofilms dominated by aerobic hydrocarbonoclastic bacteria and diatoms. Appl Environ Microbiol in press. doi: 10.1128/aem.00072-12
  9. 9.
    Prince RC, Gramain A, McGenity TJ (2010) Prokaryotic hydrocarbon degraders. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology, vol 3. Springer-Verlag, Berlin Heidelberg, pp 1671–1692Google Scholar
  10. 10.
    Röling WF, Milner MG, Jones DM, Lee K, Daniel F, Swannell RJ, Head IM (2002) Robust hydrocarbon degradation and dynamics of bacterial communities during nutrient-enhanced oil spill bioremediation. Appl Environ Microbiol 68:5537–5548PubMedCrossRefGoogle Scholar
  11. 11.
    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 7:1426–1441PubMedCrossRefGoogle Scholar
  12. 12.
    Paisse S, Coulon F, Goñi-Urriza M, Peperzak L, McGenity TJ, Duran R (2008) Structure of bacterial communities along a hydrocarbon contamination gradient in a coastal sediment. FEMS Microbiol Ecol 66:295–305PubMedCrossRefGoogle Scholar
  13. 13.
    Alonso-Gutiérrez J, Figueras A, Albaigés J, Jiménez N, Viñas M, Solanas AM, Novoa B (2009) Bacterial communities from shoreline environments (Costa da Morte, Northwestern Spain) affected by the Prestige oil spill. Appl Environ Microbiol 75:3407–3418PubMedCrossRefGoogle Scholar
  14. 14.
    Paisse 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 60:394–405PubMedCrossRefGoogle Scholar
  15. 15.
    Zhou HW, Guo CL, Wong YS, Tam NF (2006) Genetic diversity of dioxygenase genes in polycyclic aromatic hydrocarbon-degrading bacteria isolated from mangrove sediments. FEMS Microbiol Lett 262:148–157PubMedCrossRefGoogle Scholar
  16. 16.
    Marcial Gomes NC, Borges LR, Paranhos R, Pinto FN, Mendonça-Hagler LC, Smalla K (2008) Exploring the diversity of bacterial communities in sediments of urban mangrove forests. FEMS Microbiol Ecol 66:96–109PubMedCrossRefGoogle Scholar
  17. 17.
    Zhou HW, Wong AH, Yu RM, Park YD, Wong YS, Tam NF (2009) Polycyclic aromatic hydrocarbon-induced structural shift of bacterial communities in mangrove sediment. Microb Ecol 58:153–160PubMedCrossRefGoogle Scholar
  18. 18.
    Gomes NC, Flocco CG, Costa R, Junca H, Vilchez R, Pieper DH, Krögerrecklenfort E, Paranhos R, Mendonça-Hagler LC, Smalla K (2010) Mangrove microniches determine the structural and functional diversity of enriched petroleum hydrocarbon-degrading consortia. FEMS Microbiol Ecol 74:276–290PubMedCrossRefGoogle Scholar
  19. 19.
    dos Santos HF, Cury JC, do Carmo FL, dos Santos AL, Tiedje J, van Elsas JD, Rosado AS, Peixoto RS (2011) Mangrove bacterial diversity and the impact of oil contamination revealed by pyrosequencing: bacterial proxies for oil pollution. PLoS One 6:e16943PubMedCrossRefGoogle Scholar
  20. 20.
    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 77:7962–7974PubMedCrossRefGoogle Scholar
  21. 21.
    Peixoto R, Chaer GM, Carmo FL, Araújo FV, Paes JE, Volpon A, Santiago G, Rosado A (2011) Bacterial communities reflect the spatial variation in pollutant levels in Brazilian mangrove sediment. Antonie Van Leeuwenhoek 99:341–354PubMedCrossRefGoogle Scholar
  22. 22.
    Rosano-Hernández M, Ramírez-Saad H, Fernández-Linares L (2011) Petroleum-influenced beach sediments of the Campeche Bank, Mexico: diversity and bacterial community structure assessment. J Environ Manage in pressGoogle Scholar
  23. 23.
    Cui Z, Lai Q, Dong C, Shao Z (2008) Biodiversity of polycyclic aromatic hydrocarbon-degrading bacteria from deep sea sediments of the Middle Atlantic Ridge. Environ Microbiol 10:2138–2149PubMedCrossRefGoogle Scholar
  24. 24.
    Wasmund K, Burns KA, Kurtböke DI, Bourne DG (2009) Novel alkane hydroxylase gene (alkB) diversity in sediments associated with hydrocarbon seeps in the Timor Sea, Australia. Appl Environ Microbiol 75:7391–7398PubMedCrossRefGoogle Scholar
  25. 25.
    Kuhn E, Bellicanta GS, Pellizari VH (2009) New alk genes detected in Antarctic marine sediments. Environ Microbiol 11:669–673PubMedCrossRefGoogle Scholar
  26. 26.
    Marcos M, Lozada M, di Marzio WD, Dionisi H (2012) Abundance, dynamics and biogeographic distribution of seven polycyclic aromatic hydrocarbon dioxygenase gene variants in coastal sediments of Patagonia. Appl Environ Microbiol 78:1589–1592PubMedCrossRefGoogle Scholar
  27. 27.
    Head IM, Jones DM, Röling WF (2006) Marine microorganisms make a meal of oil. Nat Rev Microbiol 4:173–182PubMedCrossRefGoogle Scholar
  28. 28.
    Harayama S, Kishira H, Kasai Y, Shutsubo K (1999) Petroleum biodegradation in marine environments. J Mol Microbiol Biotechnol 1:63–70PubMedGoogle Scholar
  29. 29.
    Kuhad RC, Gupta R (2009) Biological remediation of petroleum contaminants. In: Singh A, Kuhad RC, Ward OP (eds) Advances in applied bioremediation, vol 17. Springer-Verlag, Berlin Heidelberg, pp 173–187CrossRefGoogle Scholar
  30. 30.
    Nava V, Morales M, Revah S (2007) Cometabolism of methyl tert-butyl ether (MTBE) with alkanes. Rev Environ Sci Biotechnol 6:339–352CrossRefGoogle Scholar
  31. 31.
    Yakimov MM, Golyshin PN, Lang S, Moore ER, Abraham WR, Lünsdorf H, Timmis KN (1998) Alcanivorax borkumensis gen. nov., sp. nov., a new, hydrocarbon-degrading and surfactant-producing marine bacterium. Int J Syst Bacteriol 48:339–348PubMedCrossRefGoogle Scholar
  32. 32.
    Yakimov MM, Giuliano L, Denaro R, Crisafi E, Chernikova TN, Abraham WR, Luensdorf 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 54:141–148PubMedCrossRefGoogle Scholar
  33. 33.
    Golyshin PN, Chernikova TN, Abraham WR, 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 52:901–911PubMedCrossRefGoogle Scholar
  34. 34.
    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 53:779–785PubMedCrossRefGoogle Scholar
  35. 35.
    Yakimov MM, Timmis KN, Golyshin PN (2007) Obligate oil-degrading bacteria. Curr Opin Biotechnol 18:257–266PubMedCrossRefGoogle Scholar
  36. 36.
    van Beilen JB, Funhoff EG (2007) Alkane hydroxylases involved in microbial alkane degradation. Appl Microbiol Biotechnol 74:13–21PubMedCrossRefGoogle Scholar
  37. 37.
    Wentzel A, Ellingsen TE, Kotlar HK, Zotchev SB, Throne-Holst M (2007) Bacterial metabolism of long-chain n-alkanes. Appl Microbiol Biotechnol 76:1209–1221PubMedCrossRefGoogle Scholar
  38. 38.
    Rojo F (2009) Degradation of alkanes by bacteria. Environ Microbiol 11:2477–2490PubMedCrossRefGoogle Scholar
  39. 39.
    Margesin R, Labbé D, Schinner F, Greer CW, Whyte LG (2003) Characterization of hydrocarbon-degrading microbial populations in contaminated and pristine Alpine soils. Appl Environ Microbiol 69:3085–3092PubMedCrossRefGoogle Scholar
  40. 40.
    Pérez-de-Mora A, Engel M, Schloter M (2010) Abundance and diversity of n-alkane-degrading bacteria in a forest soil co-contaminated with hydrocarbons and metals: a molecular study on alkB homologous genes. Microb Ecol 62:959–972CrossRefGoogle Scholar
  41. 41.
    Powell SM, Bowman JP, Ferguson SH, Snape I (2010) The importance of soil characteristics to the structure of alkane-degrading bacterial communities on sub-Antarctic Macquarie Island. Soil Biol Biochem 42:2012–2021CrossRefGoogle Scholar
  42. 42.
    Powell SM, Ferguson SH, Bowman JP, Snape I (2006) Using real-time PCR to assess changes in the hydrocarbon-degrading microbial community in Antarctic soil during bioremediation. Microb Ecol 52:523–532PubMedCrossRefGoogle Scholar
  43. 43.
    Salminen JM, Tuomi PM, Jørgensen KS (2008) Functional gene abundances (nahAc, alkB, xylE) in the assessment of the efficacy of bioremediation. Appl Biochem Biotechnol 151:638–652PubMedCrossRefGoogle Scholar
  44. 44.
    Hamamura N, Fukui M, Ward DM, Inskeep WP (2008) Assessing soil microbial populations responding to crude-oil amendment at different temperatures using phylogenetic, functional gene (alkB) and physiological analyses. Environ Sci Technol 42:7580–7586PubMedCrossRefGoogle Scholar
  45. 45.
    Commendatore MG, Esteves JL (2007) An assessment of oil pollution in the coastal zone of Patagonia, Argentina. Environ Manage 40:814–821PubMedCrossRefGoogle Scholar
  46. 46.
    Esteves JL, Commendatore MG, Nievas ML, Paletto VM, Amín O (2006) Hydrocarbon pollution in coastal sediments of Tierra del Fuego Islands, Patagonia Argentina. Mar Pollut Bull 52:582–590PubMedCrossRefGoogle Scholar
  47. 47.
    Lozada M, Riva Mercadal JP, Guerrero LD, Di Marzio WD, Ferrero MA, Dionisi HM (2008) Novel aromatic ring-hydroxylating dioxygenase genes from coastal marine sediments of Patagonia. BMC Microbiol 8:50PubMedCrossRefGoogle Scholar
  48. 48.
    Gil MN, Torres AI, Amín O, Esteves JL (2011) Assessment of recent sediment influence in an urban polluted Subantarctic coastal ecosystem. Beagle Channel (Southern Argentina). Mar Pollut Bull 6:201–207CrossRefGoogle Scholar
  49. 49.
    Commendatore MG, Nievas ML, Amin O, Esteves JL (2012) Sources and distribution of aliphatic and polyaromatic hydrocarbons in coastal sediments from the Ushuaia Bay (Tierra del Fuego, Patagonia, Argentina). Mar Environ Res 74:20–31PubMedCrossRefGoogle Scholar
  50. 50.
    Marcos MS, Lozada M, Dionisi HM (2009) Aromatic hydrocarbon degradation genes from chronically polluted Subantarctic marine sediments. Lett Appl Microbiol 49:602–608PubMedCrossRefGoogle Scholar
  51. 51.
    Dionisi HM, Lozada M, Marcos MS, Di Marzio WD (2011) Aromatic hydrocarbon degradation genes from chronically polluted Subantarctic marine sediments. In: Bruijn FJd (ed) Handbook of molecular microbial ecology II: metagenomics in different habitats. John Wiley & Sons, Inc., Hoboken, pp 461–473CrossRefGoogle Scholar
  52. 52.
    Commendatore MG, Esteves JL, Colombo JC (2000) Hydrocarbons in coastal sediments of Patagonia, Argentina: levels and probable sources. Mar Pollut Bull 40:989–998CrossRefGoogle Scholar
  53. 53.
    Commendatore MG, Esteves JL (2004) Natural and anthropogenic hydrocarbons in sediments from the Chubut River (Patagonia, Argentina). Mar Pollut Bull 48:910–918PubMedCrossRefGoogle Scholar
  54. 54.
    Olivera NL, Nievas ML, Lozada M, Del Prado G, Dionisi HM, Siñeriz F (2009) Isolation and characterization of biosurfactant-producing Alcanivorax strains: hydrocarbon accession strategies and alkane hydroxylase gene analysis. Res Microbiol 160:19–26PubMedCrossRefGoogle Scholar
  55. 55.
    Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98Google Scholar
  56. 56.
    Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410PubMedGoogle Scholar
  57. 57.
    Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541PubMedCrossRefGoogle Scholar
  58. 58.
    Chao A (1984) Nonparametric estimation of the number of classes in a population. Scand J Stat 11:265–270Google Scholar
  59. 59.
    Chao A, Ma M-C, Yang MCK (1993) Stopping rules and estimation for recapture debugging with unequal failure rates. Biometrika 80:193–201CrossRefGoogle Scholar
  60. 60.
    Good IJ (1953) The population frequencies of species and the estimation of population parameters. Biometrika 40:237–264Google Scholar
  61. 61.
    Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882PubMedCrossRefGoogle Scholar
  62. 62.
    Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedCrossRefGoogle Scholar
  63. 63.
    Schloss PD, Westcott SL (2011) Assessing and improving methods used in operational taxonomic unit-based approaches for 16S rRNA gene sequence analysis. Appl Environ Microbiol 77:3219–3226PubMedCrossRefGoogle Scholar
  64. 64.
    Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glöckner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196PubMedCrossRefGoogle Scholar
  65. 65.
    Schloss PD (2010) The effects of alignment quality, distance calculation method, sequence filtering, and region on the analysis of 16S rRNA gene-based studies. PLoS Comput Biol 6:e1000844PubMedCrossRefGoogle Scholar
  66. 66.
    Huse SM, Welch DM, Morrison HG, Sogin ML (2010) Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ Microbiol 12:1889–1898PubMedCrossRefGoogle Scholar
  67. 67.
    Simpson EH (1949) Measurement of diversity. Nature 163:688CrossRefGoogle Scholar
  68. 68.
    Bray JR, Curtis CT (1957) An ordination of the upland forest communities of Southern Wisconsin. Ecol Monogr 27:325–349CrossRefGoogle Scholar
  69. 69.
    Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267PubMedCrossRefGoogle Scholar
  70. 70.
    United Nations Environment Programme (1992) Determination of petroleum hydrocarbons in sediments. In: UNEP (ed.) Reference methods for marine pollution studies, vol. 20. UNEP/IOC/IAEA, pp. 1-75.Google Scholar
  71. 71.
    Altschul SF (1991) Amino acid substitution matrices from an information theoretic perspective. J Mol Biol 219:555–565PubMedCrossRefGoogle Scholar
  72. 72.
    Smits TH, Rothlisberger M, Witholt B, van Beilen JB (1999) Molecular screening for alkane hydroxylase genes in Gram-negative and Gram-positive strains. Environ Microbiol 1:307–317PubMedCrossRefGoogle Scholar
  73. 73.
    Shanklin J, Whittle E (2003) Evidence linking the Pseudomonas oleovorans alkane ω-hydroxylase, an integral membrane diiron enzyme, and the fatty acid desaturase family. FEBS Lett 545:188–192PubMedCrossRefGoogle Scholar
  74. 74.
    Kim SJ, Kwon KK (2010) Marine, hydrocarbon-degrading Alphaproteobacteria. In: Timmis KN (ed) Handbook of hydrocarbon and lipid microbiology, vol 3. Springer-Verlag, Berlin Heidelberg, pp 1707–1714CrossRefGoogle Scholar
  75. 75.
    Bell TH, Yergeau E, Martineau C, Juck D, Whyte LG, Greer CW (2011) Identification of nitrogen-incorporating bacteria in petroleum-contaminated arctic soils using [15N]DNA-based stable isotope probing and pyrosequencing. Appl Environ Microbiol 12:4163–4171CrossRefGoogle Scholar
  76. 76.
    Greenwood PF, Wibrow S, George SJ, Tibbett M (2009) Hydrocarbon biodegradation and soil microbial community response to repeated oil exposure. Org Geochem 40:293–300CrossRefGoogle Scholar
  77. 77.
    Kauppi S, Romantschuk M, Strömmer R, Sinkkonen A (2010) Natural attenuation is enhanced in previously contaminated and coniferous forest soils. Environ Sci Pollut Res Int 19:53–63CrossRefGoogle Scholar
  78. 78.
    Paisse S, Duran R, Coulon F, Goñi-Urriza M (2011) Are alkane hydroxylase genes (alkB) relevant to assess petroleum bioremediation processes in chronically polluted coastal sediments? Appl Microbiol Biotechnol 92:835–844PubMedCrossRefGoogle Scholar
  79. 79.
    Graeber I, Kaesler I, Borchert MS, Dieckmann R, Pape T, Lurz R, Nielsen P, von Döhren H, Michaelis W, Szewzyk U (2008) Spongiibacter marinus gen. nov., sp. nov., a halophilic marine bacterium isolated from the boreal sponge Haliclona sp. 1. Int J Syst Evol Microbiol 58:585–590PubMedCrossRefGoogle Scholar
  80. 80.
    Jang Gl, Hwang CY, Choi H-G, Kang S-H, Cho BC (2011) Description of Spongiibacter borealis sp. nov., isolated from Arctic seawater, and reclassification of Melitea salexigens Urios et al. 2008 as a later heterotypic synonym of Spongiibacter marinus Graeber et al. 2008 with emended descriptions of the genus Spongiibacter and Spongiibacter marinus. Int J Syst Evol Microbiol 61:2895–2900PubMedCrossRefGoogle Scholar
  81. 81.
    Urios L, Agogué H, Intertaglia L, Lesongeur F, Lebaron P (2008) Melitea salexigens gen. nov., sp. nov., a gammaproteobacterium from the Mediterranean Sea. Int J Syst Evol Microbiol 58:2479–2483PubMedCrossRefGoogle Scholar
  82. 82.
    Gauthier MJ, Lafay B, Christen R, Fernandez L, Acquaviva M, Bonin P, Bertrand JC (1992) Marinobacter hydrocarbonoclasticus gen. nov., sp. nov., a new, extremely halotolerant, hydrocarbon-degrading marine bacterium. Int J Syst Bacteriol 42:568–576PubMedCrossRefGoogle Scholar
  83. 83.
    Márquez MC, Ventosa A (2005) Marinobacter hydrocarbonoclasticus Gauthier et al. 1992 and Marinobacter aquaeolei Nguyen et al. 1999 are heterotypic synonyms. Int J Syst Evol Microbiol 55:1349–1351PubMedCrossRefGoogle Scholar
  84. 84.
    Schneiker S, Martins dos Santos VA, Bartels D, Bekel T, Brecht M, Buhrmester J, Chernikova TN, Denaro R, Ferrer M, Gertler C, Goesmann A, Golyshina OV, Kaminski F, Khachane AN, Lang S, Linke B, McHardy AC, Meyer F, Nechitaylo T, Puhler A, Regenhardt D, Rupp O, Sabirova JS, Selbitschka W, Yakimov MM, Timmis KN, Vorholter FJ, Weidner S, Kaiser O, Golyshin PN (2006) Genome sequence of the ubiquitous hydrocarbon-degrading marine bacterium Alcanivorax borkumensis. Nat Biotechnol 24:997–1004PubMedCrossRefGoogle Scholar
  85. 85.
    Zhao B, Wang H, Li R, Mao X (2010) Thalassospira xianhensis sp. nov., a polycyclic aromatic hydrocarbon-degrading marine bacterium. Int J Syst Evol Microbiol 60:1125–1129PubMedCrossRefGoogle Scholar
  86. 86.
    Kodama Y, Stiknowati LI, Ueki A, Ueki K, Watanabe K (2008) Thalassospira tepidiphila sp. nov., a polycyclic aromatic hydrocarbon-degrading bacterium isolated from seawater. Int J Syst Evol Microbiol 58:711–715PubMedCrossRefGoogle Scholar
  87. 87.
    Jiménez N, Viñas M, Guiu-Aragonés C, Bayona J, Albaigés J, Solanas A (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 91:823–834PubMedCrossRefGoogle Scholar
  88. 88.
    Wang F, Xu M, Xiao X (2011) Isolation and characterization of alkane hydroxylases from a metagenomic library of Pacific deep-sea sediment In: De Bruijn, F (ed.) Handbook of molecular microbial ecology II: metagenomics in different habitats, vol. 2. Wiley-Blackwell, pp. 475-479Google Scholar
  89. 89.
    Wang L, Wang W, Lai Q, Shao Z (2010) Gene diversity of CYP153A and AlkB alkane hydroxylases in oil degrading bacteria isolated from the Atlantic Ocean. Environ Microbiol 12:1230–1242PubMedCrossRefGoogle Scholar
  90. 90.
    Tourova T, Nazina T, Mikhailova E, Rodionova T, Ekimov A, Mashukova A, Poltaraus A (2008) alkB homologs in thermophilic bacteria of the genus Geobacillus. Mol Biol 42:217–226CrossRefGoogle Scholar
  91. 91.
    Yergeau E, Sanschagrin S, Beaumier D, Greer CW (2012) Metagenomic analysis of the bioremediation of diesel-contaminated Canadian high arctic soils. PLoS One 7:e30058PubMedCrossRefGoogle Scholar
  92. 92.
    Wang Y, Yu M, Austin B, Zhang X-H (2012) Oleispira lenta sp. nov., a novel marine bacterium isolated from Yellow sea coastal seawater in Qingdao, China. Antonie van Leeuwenhoek in pressGoogle Scholar
  93. 93.
    Coulon F, McKew BA, Osborn AM, McGenity TJ, Timmis KN (2007) Effects of temperature and biostimulation on oil-degrading microbial communities in temperate estuarine waters. Environ Microbiol 9:177–186PubMedCrossRefGoogle Scholar
  94. 94.
    Golyshin PN, Ferrer M, Chernokova TN, Golyshina OV, Yakimov MM (2010) Oleispira. In: Timmis, KN (ed.) Handbook of hydrocarbon and lipid microbiology, vol. 3. Springer-Verlag Berlin Heidelberg, pp. 1755-1764Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Lilian M. Guibert
    • 1
  • Claudia L. Loviso
    • 1
  • Magalí S. Marcos
    • 1
  • Marta G. Commendatore
    • 1
  • Hebe M. Dionisi
    • 1
  • Mariana Lozada
    • 1
  1. 1.Centro Nacional Patagónico (CENPAT - CONICET)Puerto MadrynArgentina

Personalised recommendations