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.
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References
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 57:290–301
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 4:5–7
Bertrand JC, Almallah M, Acquaviva M, Mille G (1990) Biodegradation of hydrocarbons by an extremely halophilic archaebacterium. Lett Appl Microbiol 11:260–263
Bezalel L, Hadar Y, Fu PP, Freeman JP, Cerniglia (1996) Metabolism of phenanthrene by the white rot fungus Pleurotus ostreatus. Appl Environ Microbiol 62:2547–53
Cuadros-Orellana S, Pohlschröder M, Durrant LR (2006) Isolation and characterization of halophilic archaea able to grow in aromatic compounds. Int Biodeterior Biodegradation 57:151–154
Efroymson RA, Alexander M (1991) Biodegradation by an Arthrobacter species of hydrocarbons partitioned into an organic solvent. Appl Environ Microbiol 57:1441–1447
Emerson D, Chauhan S, Oriel P, Breznak JA (1994) Haloferax sp. D1227, a halophilic archaeon capable of growth on aromatic compounds. Arch Microbiol 161:445–452
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 90:237–247
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 68:6246–6255
Grötzschel S, Köster J, Abed RMM, de Beer D (2002) Degradation of petroleum model compounds immobilized on clay by a hypersaline microbial mat. Biodegradation 13:273–283
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 293–299
Hammel KE, Gai WZ, Green B, Moen MA (1992) Oxidative degradation of phenanthrene by the ligninolytic fungus Phanerochaete chrysosporium. Appl Environ Microbiol 58:1832–1838
Hashimoto Y, Tokura K, Kishi H, Strachan WMJ (1984) Prediction of seawater solubility of aromatic compounds. Chemosphere 13:881–888
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 47:73–77
Kim YH, Freeman JP (2005) Effects of pH on the degradation of phenanthrene and pyrene by Mycobacterium vanbaalenii PYR-1. Appl Microbiol Biotechnol 67:275–285
Kulichevskaya IS, Milekhina EI, Borzenkov IA, Zvyagintseva IS, Belyaev SS (1991) Oxidation of petroleum hydrocarbons by extremely halophilic archeobacteria. Microbiology 60:596–601
Le Borgne S, Paniagua D, Vazquez-Duhalt R (2008) Biodegradation of organic pollutants by halophilic bacteria and archaea. J Mol Microbiol Biotechnol 15:74–92
Lefebvre O (2005) Application des micro-organismes halophiles au traitement des effluents industriels hypersalins. Ph.D Thesis. Ecole Nationale Supérieure Agronomique de Montpellier, p. 12
Lefebvre O, Moletta R (2006) Treatment of organic pollution in industrial saline wastewater: a literature review. Water Res 40:3671–3682
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 78:165–172
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 60:42–548
Marhuenda-Egea FC, Bonete MJ (2002) Extreme halophilic enzymes in organic solvents. Curr Opin Biotechnol 13:385–389
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 67:1476–1483
Nicholson CA, Fathepure BZ (2004) Biodegradation of benzene by halophilic and halotolerant bacteria under aerobic conditions. Appl Environ Microbiol 70:1222–1225
Nicholson CA, Fathepure BZ (2005) Aerobic biodegradation of benzene and toluene under hypersaline conditions at the Great Salt Plains, Oklahoma. FEMS Microbiol Lett 245:257–262
Oren A (2002) Diversity of halophilic microorganisms: environments, phylogeny, physiology, and applications. J Ind Microbiol Biotechnol 28:56–63
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 105–122
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 187:923–929
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 65:2388–2394
Speight JG (1998) The chemistry and technology of petroleum. Marcel Dekker, New York
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
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 8:89–99
Ward DM, Brock TD (1978) Hydrocarbon biodegradation in hypersaline environments. Appl Environ Microbiol 35:353–359
Whitehouse BG (1984) The effects of temperature and salinity on the aqueous solubility of polynuclear aromatic hydrocarbons. Mar Chem 14:319–332
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 63:3719–3723
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 57:103–106
Zeinali M, Vossoughi M, Ardestani SK (2008) Degradation of phenanthrene and anthracene by Nocardia otitidiscaviarum strain TSH1, a moderately thermophilic bacterium. J Appl Microbiol 105:398–406
Zvyagintseva I, Belyaev S, Borzenkov I, Kostrikina N, Milekhina E, Ivanov M (1995) Halophilic archaebacteria from the Kalamkass oil field. Microbiology 64:67–71
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.
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Communicated by A. Oren.
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Tapilatu, Y.H., Grossi, V., Acquaviva, M. et al. Isolation of hydrocarbon-degrading extremely halophilic archaea from an uncontaminated hypersaline pond (Camargue, France). Extremophiles 14, 225–231 (2010). https://doi.org/10.1007/s00792-010-0301-z
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DOI: https://doi.org/10.1007/s00792-010-0301-z