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Extremophiles

, Volume 14, Issue 2, pp 225–231 | Cite as

Isolation of hydrocarbon-degrading extremely halophilic archaea from an uncontaminated hypersaline pond (Camargue, France)

  • Yosmina H. Tapilatu
  • Vincent Grossi
  • Monique Acquaviva
  • Cécile Militon
  • Jean-Claude Bertrand
  • Philippe CunyEmail author
Original Paper

Abstract

Little information exists about the ability of halophilic archaea present in hypersaline environments to degrade hydrocarbons. In order to identify the potential actors of hydrocarbon degradation in these environments, enrichment cultures were prepared using samples collected from a shallow crystallizer pond with no known contamination history in Camargue, France, with n-alkanes provided as source of carbon and energy. Five alkane-degrading halophilic archaeal strains were isolated: one (strain MSNC 2) was closely related to Haloarcula and three (strains MSNC 4, MSNC 14, and MSNC 16) to Haloferax. Biodegradation assays showed that depending on the strain, 32 to 95% (0.5 g/l) of heptadecane was degraded after 30 days of incubation at 40°C in 225 g/l NaCl artificial medium. One of the strains (MSNC 14) was also able to degrade phenanthrene. This work clearly shows for the first time the potential role of halophilic archaea belonging to the genera Haloarcula and Haloferax in the degradation of hydrocarbons in both pristine and hydrocarbon-contaminated hypersaline environments.

Keywords

Halophilic Archaea n-Alkanes Phenantrene Biodegradation Hypersaline ponds 

Notes

Acknowledgments

The work was carried out as part of Yosmina Tapilatu’s PhD research and of the French National Program EC2CO “BIOHYDEX (BIOdégradation des HYDrocarbures dans les milieux EXtrêmes”). We thank the Centre National de la Recherche Scientifique (CNRS) and the Institut National des Sciences de l’Univers (INSU) for financial support. Y.T. was the recipient of a scholarship from the French Foreign Ministry.

References

  1. Abed RMM, Al-Thukair A, de Beer D (2006) Bacterial diversity of a cyanobacterial mat degrading petroleum compounds at elevated salinities and temperatures. FEMS Microbiol Ecol 57:290–301CrossRefPubMedGoogle Scholar
  2. Al-Mueini R, Al-Dalali M, Al-Amri IS, Patzelt H (2007) Hydrocarbon degradation at high salinity by a novel extremely halophilic actinomycete. Environ Chem 4:5–7CrossRefGoogle Scholar
  3. Bertrand JC, Almallah M, Acquaviva M, Mille G (1990) Biodegradation of hydrocarbons by an extremely halophilic archaebacterium. Lett Appl Microbiol 11:260–263CrossRefGoogle Scholar
  4. Bezalel L, Hadar Y, Fu PP, Freeman JP, Cerniglia (1996) Metabolism of phenanthrene by the white rot fungus Pleurotus ostreatus. Appl Environ Microbiol 62:2547–53Google Scholar
  5. Cuadros-Orellana S, Pohlschröder M, Durrant LR (2006) Isolation and characterization of halophilic archaea able to grow in aromatic compounds. Int Biodeterior Biodegradation 57:151–154CrossRefGoogle Scholar
  6. Efroymson RA, Alexander M (1991) Biodegradation by an Arthrobacter species of hydrocarbons partitioned into an organic solvent. Appl Environ Microbiol 57:1441–1447PubMedGoogle Scholar
  7. Emerson D, Chauhan S, Oriel P, Breznak JA (1994) Haloferax sp. D1227, a halophilic archaeon capable of growth on aromatic compounds. Arch Microbiol 161:445–452CrossRefGoogle Scholar
  8. Engelhardt MA, Daly K, Swannell RPJ, Head IM (2001) Isolation and characterization of a novel hydrocarbon-degrading, gram-positive bacterium, isolated from intertidal beach sediment, and description of Planococcus alkanoclasticus sp. nov. J Appl Microbiol 90:237–247CrossRefPubMedGoogle Scholar
  9. Fairley DJ, Boyd DR, Sharma ND, Allen CCR, Morgan P, Larkin MJ (2002) Aerobic metabolism of 4-hydroxybenzoic acid in archaea via an unusual pathway involving an intramolecular migration (NIH Shift). Appl Environ Microbiol 68:6246–6255CrossRefPubMedGoogle Scholar
  10. Grötzschel S, Köster J, Abed RMM, de Beer D (2002) Degradation of petroleum model compounds immobilized on clay by a hypersaline microbial mat. Biodegradation 13:273–283CrossRefPubMedGoogle Scholar
  11. Hadibarata T, Tachibana S (2009) Identification of phenanthrene metabolites produced by Polyporus sp. S133. In: Obayashi Y, Isobe T, Subramanian A, Suzuki S, Tanabe S (eds) Interdisciplinary studies on environmental chemistry-environmental research in Asia. Terrapub, Tokyo, pp 293–299Google Scholar
  12. Hammel KE, Gai WZ, Green B, Moen MA (1992) Oxidative degradation of phenanthrene by the ligninolytic fungus Phanerochaete chrysosporium. Appl Environ Microbiol 58:1832–1838PubMedGoogle Scholar
  13. Hashimoto Y, Tokura K, Kishi H, Strachan WMJ (1984) Prediction of seawater solubility of aromatic compounds. Chemosphere 13:881–888CrossRefGoogle Scholar
  14. Ihara K, Watanabe S, Tamura T (1997) Haloarcula argentinensis sp. nov. and Haloarcula mukohataei sp. nov., two new extremely halophilic archaea collected in Argentina. Int J Syst Bacteriol 47:73–77PubMedCrossRefGoogle Scholar
  15. Kim YH, Freeman JP (2005) Effects of pH on the degradation of phenanthrene and pyrene by Mycobacterium vanbaalenii PYR-1. Appl Microbiol Biotechnol 67:275–285CrossRefPubMedGoogle Scholar
  16. Kulichevskaya IS, Milekhina EI, Borzenkov IA, Zvyagintseva IS, Belyaev SS (1991) Oxidation of petroleum hydrocarbons by extremely halophilic archeobacteria. Microbiology 60:596–601Google Scholar
  17. Le Borgne S, Paniagua D, Vazquez-Duhalt R (2008) Biodegradation of organic pollutants by halophilic bacteria and archaea. J Mol Microbiol Biotechnol 15:74–92PubMedGoogle Scholar
  18. Lefebvre O (2005) Application des micro-organismes halophiles au traitement des effluents industriels hypersalins. Ph.D Thesis. Ecole Nationale Supérieure Agronomique de Montpellier, p. 12Google Scholar
  19. Lefebvre O, Moletta R (2006) Treatment of organic pollution in industrial saline wastewater: a literature review. Water Res 40:3671–3682CrossRefPubMedGoogle Scholar
  20. López Z, Vila J, Ortega-Calvo JJ, Griffoll M (2008) Simultaneous biodegradation of creosote-polycyclic aromatic hydrocarbons by a pyrene-degrading Mycobacterium. Appl Microbiol Biotechnol 78:165–172CrossRefPubMedGoogle Scholar
  21. Malachowsky KJ, Phelps TJ, Teboli AB, Minnikin DE, White DC (1994) Aerobic mineralization of trichloroethylene, vinyl chloride, and aromatic compounds by Rhodococcus species. Appl Environ Microbiol 60:42–548Google Scholar
  22. Marhuenda-Egea FC, Bonete MJ (2002) Extreme halophilic enzymes in organic solvents. Curr Opin Biotechnol 13:385–389CrossRefPubMedGoogle Scholar
  23. Moody JD, Freeman JP, Doerge DR, Cerniglia CE (2001) Degradation of phenanthrene and anthracene by cell suspensions of Mycobacterium sp. strain PYR-1. Appl Environ Microbiol 67:1476–1483CrossRefPubMedGoogle Scholar
  24. Nicholson CA, Fathepure BZ (2004) Biodegradation of benzene by halophilic and halotolerant bacteria under aerobic conditions. Appl Environ Microbiol 70:1222–1225CrossRefPubMedGoogle Scholar
  25. Nicholson CA, Fathepure BZ (2005) Aerobic biodegradation of benzene and toluene under hypersaline conditions at the Great Salt Plains, Oklahoma. FEMS Microbiol Lett 245:257–262CrossRefPubMedGoogle Scholar
  26. Oren A (2002) Diversity of halophilic microorganisms: environments, phylogeny, physiology, and applications. J Ind Microbiol Biotechnol 28:56–63PubMedGoogle Scholar
  27. Patzelt H (2005) Hydrocarbon degradation under hypersaline conditions––some facts, some experiments and many open questions. In: Gunde-Cimerman N, Oren A, Plemenitas A (eds) Adaptation to life at high salt concentrations in archaea bacteria and eukarya. Springer, Berlin, pp 105–122CrossRefGoogle Scholar
  28. Robinson JL, Pyzyna B, Atrasz RG, Henderson CA, Morrill KL, Burd AM, DeSoucy E, Fogleman RE III, Naylor JB, Steele SM, Elliott DR, Leyva KJ, Shand RF (2005) Growth kinetics of extremely halophilic Archaea (family Halobacteriaceae) as revealed by arrhenius plots. J Bacteriol 187:923–929CrossRefPubMedGoogle Scholar
  29. Seo J-S, Keum Y-S, Hu Y, Lee S-E, Li QX (2006) Phenanthrene degradation in Arthrobacter sp. P1-1: initial 1,2-, 3,4- and 9,10-dioxygenation, and meta- and ortho-cleavages of naphthalene-1, 2-diol after its formation from naphthalene-1,2-dicarboxylic acid and hydroxyl naphthoic acids. Chemosphere 65:2388–2394CrossRefPubMedGoogle Scholar
  30. Speight JG (1998) The chemistry and technology of petroleum. Marcel Dekker, New YorkGoogle Scholar
  31. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599CrossRefPubMedGoogle Scholar
  32. Torreblanca M, Rodriguez-Valera F, Juez G, Ventosa A, Kamekura M, Kates M (1986) Classification of non-alkaliphilic halobacteria based on numerical taxonomy and polar lipid composition, and description of Haloarcula gen nov. and Haloferax gen. nov. System Appl Microbiol 8:89–99Google Scholar
  33. Ward DM, Brock TD (1978) Hydrocarbon biodegradation in hypersaline environments. Appl Environ Microbiol 35:353–359PubMedGoogle Scholar
  34. Whitehouse BG (1984) The effects of temperature and salinity on the aqueous solubility of polynuclear aromatic hydrocarbons. Mar Chem 14:319–332CrossRefGoogle Scholar
  35. Whyte LG, Bourbonnière L, Greer CW (1997) Biodegradation of petroleum hydrocarbons by psychrotrophic Pseudomonas strains possessing both alkane (alk) and naphthalene (nah) catabolic pathways. Appl Environ Microbiol 63:3719–3723PubMedGoogle Scholar
  36. Yang Y, Cui H-L, Zhou P-J, Liu S-J (2007) Haloarcula amylolytica sp. nov., an extremely halophilic archaeon isolated from Aibi salt lake in Xin-Jiang, China. Int J Syst Evol Microbiol 57:103–106CrossRefPubMedGoogle Scholar
  37. Zeinali M, Vossoughi M, Ardestani SK (2008) Degradation of phenanthrene and anthracene by Nocardia otitidiscaviarum strain TSH1, a moderately thermophilic bacterium. J Appl Microbiol 105:398–406CrossRefPubMedGoogle Scholar
  38. Zvyagintseva I, Belyaev S, Borzenkov I, Kostrikina N, Milekhina E, Ivanov M (1995) Halophilic archaebacteria from the Kalamkass oil field. Microbiology 64:67–71Google Scholar

Copyright information

© Springer 2010

Authors and Affiliations

  • Yosmina H. Tapilatu
    • 1
  • Vincent Grossi
    • 2
  • Monique Acquaviva
    • 1
  • Cécile Militon
    • 1
  • Jean-Claude Bertrand
    • 1
  • Philippe Cuny
    • 1
    Email author
  1. 1.Laboratoire de Microbiologie Géochimie et Ecologie Marines, CNRS/INSU, UMR 6117, Centre d’Océanologie de MarseilleUniversité de la MéditerranéeMarseille Cedex 9France
  2. 2.Université Lyon 1, CNRS, UMR5125, Paléoenvironnements et PaléobiosphèreVilleurbanneFrance

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