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Bacterial metabolism of long-chain n-alkanes

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Abstract

Degradation of alkanes is a widespread phenomenon in nature, and numerous microorganisms, both prokaryotic and eukaryotic, capable of utilizing these substrates as a carbon and energy source have been isolated and characterized. In this review, we summarize recent advances in the understanding of bacterial metabolism of long-chain n-alkanes. Bacterial strategies for accessing these highly hydrophobic substrates are presented, along with systems for their enzymatic degradation and conversion into products of potential industrial value. We further summarize the current knowledge on the regulation of bacterial long-chain n-alkane metabolism and survey progress in understanding bacterial pathways for utilization of n-alkanes under anaerobic conditions.

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References

  • Aeckersberg F, Bak F, Widdel F (1991) Anaerobic oxidation of saturated hydrocarbons to CO2 by a new type of sulfate-reducing bacterium. Arch Microbiol 156:5–14

    Article  CAS  Google Scholar 

  • Aeckersberg F, Rainey FA, Widdel F (1998) Growth, natural relationships, cellular fatty acids and metabolic adaptation of sulfate-reducing bacteria that utilize long-chain alkanes under anoxic conditions. Arch Microbiol 170:361–369

    Article  CAS  PubMed  Google Scholar 

  • Alain K, Holler T, Musat F, Elvert M, Treude T, Kruger M (2006) Microbiological investigation of methane- and hydrocarbon-discharging mud volcanoes in the Carpathian Mountains, Romania. Environ Microbiol 8:574–590

    Article  CAS  PubMed  Google Scholar 

  • Alvarez HM, Steinbüchel A (2002) Triacylglycerols in prokaryotic microorganisms. Appl Microbiol Biotechnol 60:367–376

    Article  CAS  PubMed  Google Scholar 

  • Amund OO, Higgins IJ (1985) The degradation of 1-phenylalkanes by an oil-degrading strain of Acinetobacter lwoffii. Antonie Van Leeuwenhoek 51:45–56

    Article  CAS  PubMed  Google Scholar 

  • Andreoni V, Bernasconi S, Colombo M, van Beilen JB, Cavalca L (2000) Detection of genes for alkane and naphthalene catabolism in Rhodococcus sp. strain 1BN. Environ Microbiol 2:572–577

    Article  CAS  PubMed  Google Scholar 

  • Antic MP, Jovancicevic BS, Ilic M, Vrvic MM, Schwarzbauer J (2006) Petroleum pollutant degradation by surface water microorganisms. Environ Sci Pollut Res 13:320–327

    Article  CAS  Google Scholar 

  • Ashraf W, Mihdhir A, Murrell JC (1994) Bacterial oxidation of propane. FEMS Microbiol Lett 122:1–6

    Article  CAS  PubMed  Google Scholar 

  • Azevedo LFA, Teixeira AM (2003) A critical review of the modeling of wax deposition mechanisms. Petrol Sci Technol 21:393–408

    Article  CAS  Google Scholar 

  • Baptist JN, Gholson RK, Coon MJ (1963) Hydrocarbon oxidation by a bacterial enzyme system. I. Products of octane oxidation. Biochim Biophys Acta 69:40–47

    Article  CAS  PubMed  Google Scholar 

  • Bonin P, Cravo-Laureau C, Michotey V, Hirschler-Rea A (2004) The anaerobic hydrocarbon biodegrading bacteria: an overview. Ophelia 58:243–254

    Article  Google Scholar 

  • Bouchez-Naitali M, Rakatozafy H, Marchal R, Leveau JY, Vandecasteele JP (1999) Diversity of bacterial strains degrading hexadecane in relation to the mode of substrate uptake. J Appl Microbiol 86:421–428

    Article  CAS  PubMed  Google Scholar 

  • Boulton CA, Ratledge C (1984) The physiology of hydrocarbon-utilizing microorganisms. In: Wiesemann A (eds) Enzyme and fermentation biotechnology. Halstead Press, Wiley, New York, pp 11–77

    Google Scholar 

  • Britton LN (1984) Microbial degradation of aliphatic hydrocarbons. In: Gibson DT (ed) Microbial degradation of organic compounds. Marcel Dekker, New York

    Google Scholar 

  • Burger ED, Perkins TK, Striegler JH (1981) Studies of wax deposition in the trans Alaska pipeline. J Petrol Technol 33:1075–1086

    Article  CAS  Google Scholar 

  • Callaghan AV, Gieg LM, Kropp KG, Suflita JM, Young LY (2006) Comparison of mechanisms of alkane metabolism under sulfate-reducing conditions among two bacterial isolates and a bacterial consortium. Appl Environ Microbiol 72:4274–4282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Canosa I, Yuste L, Rojo F (1999) Role of the alternative sigma factor sigmaS in expression of the AlkS regulator of the Pseudomonas oleovorans alkane degradation pathway. J Bacteriol 181:1748–1754

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Canosa I, Sanchez-Romero JM, Yuste L, Rojo F (2000) A positive feedback mechanism controls expression of AlkS, the transcriptional regulator of the Pseudomonas oleovorans alkane degradation pathway. Mol Microbiol 35:791–799

    Article  CAS  PubMed  Google Scholar 

  • Chaerun SK, Tazaki K, Asada R, Kogure K (2004) Bioremediation of coastal areas 5 years after the Nakhodka oil spill in the Sea of Japan: isolation and characterization of hydrocarbon-degrading bacteria. Environ Int 30:911–922

    Article  CAS  PubMed  Google Scholar 

  • Chaillan F, Le Fleche A, Bury E, Phantavong YH, Grimont P, Saliot A, Oudot J (2004) Identification and biodegradation potential of tropical aerobic hydrocarbon-degrading microorganisms. Res Microbiol 155:587–595

    Article  CAS  PubMed  Google Scholar 

  • Chaineau CH, Morel J, Dupont J, Bury E, Oudot J (1999) Comparison of the fuel oil biodegradation potential of hydrocarbon-assimilating microorganisms isolated from a temperate agricultural soil. Sci Total Environ 227:237–247

    Article  CAS  PubMed  Google Scholar 

  • Chakrabarty AM, Chou G, Gunsalus IC (1973) Genetic regulation of octane dissimilation plasmid in Pseudomonas. Proc Natl Acad Sci USA 70:1137–1140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Q, Janssen DB, Witholt B (1996) Physiological changes and alk gene instability in Pseudomonas oleovorans during induction and expression of alk genes. J Bacteriol 178:5508–5512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Churchill SA, Harper JP, Churchill PF (1999) Isolation and characterization of a Mycobacterium species capable of degrading three- and four-ring aromatic and aliphatic hydrocarbons. Appl Environ Microbiol 65:549–552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Correra S, Fasano A, Fusi L, Merino-Garcia D (2007) Calculating deposit formation in the pipelining of waxy crude oils. Meccanica 42:149–165

    Article  Google Scholar 

  • 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 9:177–186

    Article  CAS  PubMed  Google Scholar 

  • Cravo-Laureau C, Matheron R, Cayol JL, Joulian C, Hirschler-Rea A (2004) Desulfatibacillum aliphaticivorans gen. nov., sp nov., an n-alkane- and n-alkene-degrading, sulfate-reducing bacterium. Int J Syst Evol Microbiol 54:77–83

    Article  CAS  PubMed  Google Scholar 

  • Cravo-Laureau C, Grossi V, Raphel D, Matheron R, Hirschler-Rea A (2005) Anaerobic n-alkane metabolism by a sulfate-reducing bacterium, Desulfatibacillum aliphaticivorans strain CV2803T. Appl Environ Microbiol 71:3458–3467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • da Cunha CD, Rosado AS, Sebastian GV, Seldin L, von der Weid I (2006) Oil biodegradation by Bacillus strains isolated from the rock of an oil reservoir located in a deep-water production basin in Brazil. Appl Microbiol Biotechnol 73:949–959

    Article  CAS  PubMed  Google Scholar 

  • Davidova IA, Gieg LM, Nanny M, Kropp KG, Suflita JM (2005) Stable isotopic studies of n-alkane metabolism by a sulfate-reducing bacterial enrichment culture. Appl Environ Microbiol 71:8174–8182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Desai JD, Banat IM (1997) Microbial production of surfactants and their commercial potential. Microbiol Mol Biol Rev 61:47–64

    CAS  PubMed  PubMed Central  Google Scholar 

  • DeWitt S, Ervin JL, Howes-Orchison D, Dalietos D, Neidleman SL, Geigert J (1982) Saturated and unsaturated wax ester production by Acinetobacter sp. H01-N grown on C16–C20 n-alkanes. J Am Oil Chem Soc 59:69–74

    Article  CAS  Google Scholar 

  • Doumenq P, Aries E, Asia L, Acquaviva M, Artaud J, Gilewicz M, Mille G, Bertrand JC (2001) Influence of n-alkanes and petroleum on fatty acid composition of a hydrocarbonoclastic bacterium: Marinobacter hydrocarbonoclasticus strain 617. Chemosphere 44:519–528

    Article  CAS  PubMed  Google Scholar 

  • Dunlap KR, Perry JJ (1968) Effect of substrate on the fatty acid composition of hydrocarbon- and ketone-utilizing microorganisms. J Bacteriol 96:318–321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eggink G, Engel H, Meijer WG, Otten J, Kingma J, Witholt B (1988) Alkane utilization in Pseudomonas oleovorans. Structure and function of the regulatory locus alkR. J Biol Chem 263:13400–13405

    Article  CAS  PubMed  Google Scholar 

  • Ehrenreich P, Behrends A, Harder J, Widdel F (2000) Anaerobic oxidation of alkanes by newly isolated denitrifying bacteria. Arch Microbiol 173:58–64

    Article  CAS  PubMed  Google Scholar 

  • Engelhardt MA, Daly K, Swannell RP, 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

    Article  CAS  PubMed  Google Scholar 

  • Ervin JL, Geigert J, Neidlerman SL, Wadsworth J (1984) Substrate-dependent and growth temperature-dependent changes in the wax ester compositions produced by Acinetobacter sp. strain H01-N. In: Ratledge C, Dawson P, Rattray L (eds) Biotechnology for the oils and fats industry. American Oil Chemists Society, Champaign, IL, pp 217–222

    Google Scholar 

  • Favre-Bulle O, Witholt B (1992) Biooxidation of n-octane by a recombinant Escherichia coli in a two-liquid-phase system: effect of medium components on cell growth and alkane oxidation activity. Enzyme Microb Technol 14: 931–937

    Article  CAS  Google Scholar 

  • Feitkenhauer H, Müller R, Märkl H (2003) Degradation of polycyclic aromatic hydrocarbons and long chain alkanes at 6070°C by Thermus and Bacillus spp. Biodegradation 14: 367–372

    Article  CAS  PubMed  Google Scholar 

  • Feng L, Wang W, Cheng J, Ren Y, Zhao G, Gao C, Tang Y, Liu X, Han W, Peng X, Liu R, Wang L (2007) Genome and proteome of long-chain alkane degrading Geobacillus thermodenitrificans NG80-2 isolated from a deep-subsurface oil reservoir. Proc Natl Acad Sci USA 104: 5602–5607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fennewald M, Benson S, Oppici M, Shapiro J (1979) Insertion element analysis and mapping of the Pseudomonas plasmid alk regulon. J Bacteriol 139:940–952

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fixter LM, Nagi MN, McCormack JG, Fewson CA (1986) Structure, distribution and function of wax esters in Acinetobacter calcoaceticus. J Gen Microbiol 132:3147–3157

    CAS  Google Scholar 

  • Fletcher M (1996) Bacterial attachment in aquatic environments: a diversity of surfaces and adhesion strategies. In: Fletcher M (ed) Bacterial adhesion: molecular and ecological diversity. Wiley-Liss, New York, pp 1–24

    Google Scholar 

  • Foght JM, Fedorak PM, A. PM, Gray MR (1997) Biocatalytic upgrading of petroleum distillates: ring cleavage of aromatic hydrocarbons and heterocycles commonly present in petroleum distillates. In: Joint meeting of The Petroleum Society (48th Annual Technical Meeting) and BIOMINET, Calgary, paper 97-13, pp 1–9

  • Foster JW (1962) Bacterial oxidation of hydrocarbons. In: Foster JW (ed) Oxygenases. Academic, New York, pp 241–261

    Chapter  Google Scholar 

  • Fox MG, Dickinson FM, Ratledge C (1992) Long-chain alcohol and aldehyde dehydrogenase activities in Acinetobacter calcoaceticus strain HO1-N. J Gen Microbiol 138:1963–1972

    Article  CAS  PubMed  Google Scholar 

  • Gallagher IH (1971) Occurrence of waxes in Acinetobacter. J Gen Microbiol 68:245–247

    Article  CAS  PubMed  Google Scholar 

  • Geissdorfer W, Kok RG, Ratajczak A, Hellingwerf KJ, Hillen W (1999) The genes rubA and rubB for alkane degradation in Acinetobacter sp. strain ADP1 are in an operon with estB, encoding an esterase, and oxyR. J Bacteriol 181:4292–4298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grund A, Shapiro J, Fennewald M, Bacha P, Leahy J, Markbreiter K, Nieder M, Toepfer M (1975) Regulation of alkane oxidation in Pseudomonas putida. J Bacteriol 123:546–556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haferburg D, Hommel R, Claus R, Kleber HP (1986) Extracellular microbial lipids as biosurfactants. Adv Biochem Eng Biotechnol 33:53–93

    CAS  Google Scholar 

  • Hao R, Lu A, Wang G (2004) Crude-oil-degrading thermophilic bacterium isolated from an oil field. Can J Microbiol 50:175–182

    Article  CAS  PubMed  Google Scholar 

  • Hills G (2003) Industrial use of lipases to produce fatty acid esters. Eur J Lipid Sci Technol 105:601–607

    Article  CAS  Google Scholar 

  • Hommel RK (1994) Formation and function of biosurfactants for degradation of water-insoluble substrates. In: Ratledge C (ed) Biochemistry of microbial biodegradation. Kluwer Academic Publishers, Dordrecht, pp 63–87

    Chapter  Google Scholar 

  • Ishige T, Tani A, Sakai Y, Kato N (2003) Wax ester production by bacteria. Curr Opin Microbiol 6:244–250

    Article  CAS  PubMed  Google Scholar 

  • Ishige T, Tani A, Takabe K, Kawasaki K, Sakai Y, Kato N (2002) Wax ester production from n-alkanes by Acinetobacter sp. strain M-1: ultrastructure of cellular inclusions and role of acyl coenzyme A reductase. Appl Environ Microbiol 68:1192–1195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Juni E, Janik A (1969) Transformation of Acinetobacter calco-aceticus (Bacterium anitratum). J Bacteriol 98:281–288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalscheuer R, Steinbüchel A (2003) A novel bifunctional wax ester synthase/acyl-CoA:diacylglycerol acyltransferase mediates wax ester and triacylglycerol biosynthesis in Acinetobacter calcoaceticus ADP1. J Biol Chem 278:8075–8082

    Article  CAS  PubMed  Google Scholar 

  • Kalscheuer R, Uthoff SHL, Steinbüchel A (2003) In vitro and in vivo biosynthesis of wax diesters by an unspecific bifunctional wax ester synthase/acyl-CoA:diacylglycerol acyltransferase from Acinetobacter calcoaceticus ADP1. Eur J Lipid Sci Technol 105:578–584

    Article  CAS  Google Scholar 

  • Kalscheuer R, Stöveken T, Luftmann H, Malkus U, Reichelt R, Steinbüchel A (2006) Neutral lipid biosynthesis in engineered Escherichia coli: jojoba oil-like wax esters and fatty acid butyl esters. Appl Environ Microbiol 72:1373–1379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kasai Y, Kishira H, Syutsubo K, Harayama S (2001) Molecular detection of marine bacterial populations on beaches contaminated by the Nakhodka tanker oil-spill accident. Environ Microbiol 3:246–255

    Article  CAS  PubMed  Google Scholar 

  • Kasai Y, Kishira H, Sasaki T, Syutsubo K, Watanabe K, Harayama S (2002) Predominant growth of Alcanivorax strains in oil-contaminated and nutrient-supplemented sea water. Environ Microbiol 4:141–147

    Article  CAS  PubMed  Google Scholar 

  • Kato T, Haruki M, Imanaka T, Morikawa M, Kanaya S (2001) Isolation and characterization of long-chain-alkane degrading Bacillus thermoleovorans from deep subterranean petroleum reservoirs. J Biosci Bioeng 91:64–70

    Article  CAS  PubMed  Google Scholar 

  • Kleber HP, Claus R, Asperger O (1983) Enzymologie der n-Alkanoxidation bei Acinetobacter. Acta Biotechnol 3:251–260

    Article  CAS  Google Scholar 

  • Kok M, Oldenhuis R, van der Linden MP, Meulenberg CH, Kingma J, Witholt B (1989a) The Pseudomonas oleovorans alkBAC operon encodes two structurally related rubredoxins and an aldehyde dehydrogenase. J Biol Chem 264:5442–5451

    Article  CAS  PubMed  Google Scholar 

  • Kok M, Oldenhuis R, van der Linden MP, Raatjes P, Kingma J, van Lelyveld PH, Witholt B (1989b) The Pseudomonas oleovorans alkane hydroxylase gene. Sequence and expression. J Biol Chem 264:5435–5441

    Article  CAS  PubMed  Google Scholar 

  • Koma D, Hasumi F, Yamamoto E, Ohta T, Chung SY, Kubo M (2001) Biodegradation of long-chain n-paraffins from waste oil of car engine by Acinetobacter sp. J Biosci Bioeng 91:94–96

    Article  CAS  PubMed  Google Scholar 

  • Kotani T, Yamamoto T, Yurimoto H, Sakai Y, Kato N (2003) Propane monooxygenase and NAD+-dependent secondary alcohol dehydrogenase in propane metabolism by Gordonia sp. strain TY-5. J Bacteriol 185:7120–7128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kotlar HK, Wentzel A, Throne-Holst M, Zotchev SB, Ellingsen TE (2007) Wax control by biocatalytic degradation in high-paraffinic crude oils. In: SPE international symposium on Oilfield Chemistry, Houston, TX, paper SPE 106420

  • Kropp KG, Davidova IA, Suflita JM (2000) Anaerobic oxidation of n-dodecane by an addition reaction in a sulfate-reducing bacterial enrichment culture. Appl Environ Microbiol 66:5393–5398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kunihiro N, Haruki M, Takano K, Morikawa M, Kanaya S (2005) Isolation and characterization of Rhodococcus sp. strains TMP2 and T12 that degrade 2,6,10,14-tetramethylpentadecane (pristane) at moderately low temperatures. J Biotechnol 115:129–136

    Article  CAS  PubMed  Google Scholar 

  • Lal B, Khanna S (1996) Degradation of crude oil by Acinetobacter calcoaceticus and Alcaligenes odorans. J Appl Bacteriol 81:355–362

    CAS  PubMed  Google Scholar 

  • Lazar I, Voicu A, Nicolescu C, Mucenica D, Dobrota S, Petrisor IG, Stefanescu M, Sandulescu L (1999) The use of naturally occurring selectively isolated bacteria for inhibiting paraffin deposition. J Pet Sci Eng 22:161–169

    Article  CAS  Google Scholar 

  • Lee M, Kim MK, Singleton I, Goodfellow M, Lee ST (2006) Enhanced biodegradation of diesel oil by a newly identified Rhodococcus baikonurensis EN3 in the presence of mycolic acid. J Appl Microbiol 100:325–333

    Article  CAS  PubMed  Google Scholar 

  • Leon V, Kumar M (2005) Biological upgrading of heavy crude oil. Biotechnol Bioprocess Eng 10:471–481

    Article  CAS  Google Scholar 

  • Maeng JH, Sakai Y, Tani Y, Kato N (1996) Isolation and characterization of a novel oxygenase that catalyzes the first step of n-alkane oxidation in Acinetobacter sp. strain M-1. J Bacteriol 178: 3695–3700

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maier RM (2003) Biosurfactants: evolution and diversity in bacteria. Adv Appl Microbiol 52:101–121

    Article  CAS  PubMed  Google Scholar 

  • Marchant R, Sharkey FH, Banat IM, Rahman TJ, Perfumo A (2006) The degradation of n-hexadecane in soil by thermophilic geobacilli. FEMS Microbiol Ecol 56:44–54

    Article  CAS  PubMed  Google Scholar 

  • Marin MM, Yuste L, Rojo F (2003) Differential expression of the components of the two alkane hydroxylases from Pseudomonas aeruginosa. J Bacteriol 185:3232–3237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marin MM, Smits TH, van Beilen JB, Rojo F (2001) The alkane hydroxylase gene of Burkholderia cepacia RR10 is under catabolite repression control. J Bacteriol 183:4202–4209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mateles RI, Baruah JN, Tannenbaum SR (1967) Growth of a thermophilic bacterium on hydrocarbons: a new source of single-cell protein. Science 157:1322–1323

    Article  CAS  PubMed  Google Scholar 

  • McKew BA, Coulon F, Osborn AM, Timmis KN, McGenity TJ (2007) Determining the identity and roles of oil-metabolizing marine bacteria from the Thames estuary, UK. Environ Microbiol 9:165–176

    Article  CAS  PubMed  Google Scholar 

  • Meintanis C, Chalkou KI, Kormas KA, Karagouni AD (2006) Biodegradation of crude oil by thermophilic bacteria isolated from a volcano island. Biodegradation 17:105–111

    Article  PubMed  CAS  Google Scholar 

  • Milekhina EI, Borzenkov IA, Zvyagintseva IS, Kostrikina NA, Belyaev SS (1998) Characterization of hydrocarbon-oxidizing Rhodococcus erythropolis strain isolated from an oil field. Microbiology (English translation of Mikrobiologiya) 67:328–332

    Google Scholar 

  • Mukherjee S, Das P, Sen R (2006) Towards commercial production of microbial surfactants. Trends Biotechnol 24:509–515

    Article  CAS  PubMed  Google Scholar 

  • Murphy DJ, Vance J (1999) Mechanisms of lipid-body formation. Trends Biochem Sci 24:109–115

    Article  CAS  PubMed  Google Scholar 

  • Naik PR, Sakthivel N (2006) Functional characterization of a novel hydrocarbonoclastic Pseudomonas sp. strain PUP6 with plant-growth-promoting traits and antifungal potential. Res Microbiol 157:538–546

    Article  CAS  PubMed  Google Scholar 

  • Nazina TN, Tourova TP, Poltaraus AB, Novikova EV, Grigoryan AA, Ivanova AE, Lysenko AM, Petrunyaka VV, Osipov GA, Belyaev SS, Ivanov MV (2001) Taxonomic study of aerobic thermophilic bacilli: descriptions of Geobacillus subterraneus gen. nov., sp. nov. and Geobacillus uzenensis sp. nov. from petroleum reservoirs and transfer of Bacillus stearothermophilus, Bacillus thermocatenulatus, Bacillus thermoleovorans, Bacillus kaustophilus, Bacillus thermoglucosidasius and Bacillus thermodenitrificans to Geobacillus as the new combinations G. stearothermophilus, G. thermocatenulatus, G. thermoleovorans, G. kaustophilus, G. thermoglucosidasius and G. thermodenitrificans. Int J Syst Evol Microbiol 51:433–446

    Article  CAS  PubMed  Google Scholar 

  • Neu TR (1996) Significance of bacterial surface-active compounds in interaction of bacteria with interfaces. Microbiol Rev 60:151–166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patel RN, Mazumdar S, Ornston LN (1975) Beta-ketoadipate enol-lactone hydrolases I and II from Acinetobacter calcoaceticus. J Biol Chem 250:6567

    Article  CAS  PubMed  Google Scholar 

  • Perry JJ, Scheld HW (1968) Oxidation of hydrocarbons by microorganisms isolated from soil. Can J Microbiol 14:403–407

    Article  CAS  PubMed  Google Scholar 

  • Perry JJ (1985) Isolation and characterization of thermophilic, hydrocarbon utilizing bacteria. Adv Aquat Microbiol 3:109–139

    Google Scholar 

  • Phillips WE, Perry JJ (1976) Thermomicrobium fosteri sp. nov., a hydrocarbon utilizing obligate thermophile. Int J System Bacteriol 26:220–225

    Article  Google Scholar 

  • Rabus R, Wilkes H, Behrends A, Armstroff A, Fischer T, Pierik AJ, Widdel F (2001) Anaerobic initial reaction of n-alkanes in a denitrifying bacterium: Evidence for (1-methylpentyl)succinate as initial product and for involvement of an organic radical in n-hexane metabolism. J Bacteriol 183:1707–1715

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Radwan SS, Sorkhoh NA, Felzmann H, El-Desouky AF (1996) Uptake and utilization of n-octacosane and n-nonacosane by Arthrobacter nicotianae KCC B35. J Appl Bacteriol 80:370–374

    Article  CAS  PubMed  Google Scholar 

  • Ratajczak A, Geissdorfer W, Hillen W (1998) Expression of alkane hydroxylase from Acinetobacter sp. Strain ADP1 is induced by a broad range of n-alkanes and requires the transcriptional activator AlkR. J Bacteriol 180:5822–5827

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reiser S, Somerville C (1997) Isolation of mutants of Acinetobacter calcoaceticus deficient in wax ester synthesis and complementation of one mutation with a gene encoding a fatty acyl coenzyme A reductase. J Bacteriol 179:2969–2975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reisfeld A, Rosenberg E, Gutnick D (1972) Microbial degradation of crude oil: factors affecting the dispersion in sea water by mixed and pure cultures. Appl Microbiol 24:363–368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rios-Hernandez LA, Gieg LM, Suflita JM (2003) Biodegradation of an alicyclic hydrocarbon by a sulfate-reducing enrichment from a gas condensate-contaminated aquifer. Appl Environ Microbiol 69:434–443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ron EZ, Rosenberg E (2002) Biosurfactants and oil bioremediation. Curr Opin Biotechnol 13:249–252

    Article  CAS  PubMed  Google Scholar 

  • Rosenberg E (1993) Exploiting microbial growth on hydrocarbons—new markets. Trends Biotechnol 11:419–424

    Article  Google Scholar 

  • Rosenberg E, Ron EZ (1999) High- and low-molecular-mass microbial surfactants. Appl Microbiol Biotechnol 52:154–162

    Article  CAS  PubMed  Google Scholar 

  • Rosenberg M, Bayer EA, Delarea J, Rosenberg E (1982) Role of thin fimbriae in adherence and growth of Acinetobacter calcoaceticus RAG-1 on hexadecane. Appl Environ Microbiol 44:929–937

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rueter P, Rabus R, Wilkes H, Aeckersberg F, Rainey FA, Jannasch HW, Widdel F (1994) Anaerobic oxidation of hydrocarbons in crude oil by new types of sulphate-reducing bacteria. Nature 372:455–458

    Article  CAS  PubMed  Google Scholar 

  • Sabirova JS, Ferrer M, Regenhardt D, Timmis KN, Golyshin PN (2006) Proteomic insights into metabolic adaptations in Alcanivorax borkumensis induced by alkane utilization. J Bacteriol 188:3763–3773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakai Y, Maeng JH, Tani Y, Kato N (1994) Use of long-chain n-alkanes (C13–C44) by an isolate, Acinetobacter sp. M-1. Biosci Biotechnol Biochem 58:2128–2130

    Article  CAS  Google Scholar 

  • Sayavedra-Soto LA, Doughty DM, Kurth EG, Bottomley PJ, Arp DJ (2005) Product and product-independent induction of butane oxidation in Pseudomonas butanovora. FEMS Microbiol Lett 250:111–116

    Article  CAS  PubMed  Google Scholar 

  • 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 24:997–1004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma SL, Pant A (2000) Biodegradation and conversion of alkanes and crude oil by a marine Rhodococcus. Biodegradation 11:289–294

    Article  CAS  PubMed  Google Scholar 

  • Singer ME, Finnerty WR (1984) Microbial metabolism of straight-chain and branched alkanes. In: Atlas RM (ed) Microbial metabolism of straight-chain and branched alkanes. Macmillan Publishing Company, New York, pp 1–60

    Google Scholar 

  • Singer ME, Finnerty WR (1985) Fatty aldehyde dehydrogenases in Acinetobacter sp. strain HO1-N: role in hexadecanol metabolism. J Bacteriol 164:1011–1016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh A, Van Hamme JD, Ward OP (2007) Surfactants in microbiology and biotechnology: part 2. Application aspects. Biotechnol Adv 25:99–121

    Article  CAS  PubMed  Google Scholar 

  • Singh P, Venkatesan R, Scott Fogler H, Nagarajan NR (2001) Morphological evolution of thick wax deposits during aging. AIChE J 47:6–18

    Article  Google Scholar 

  • Smits TH, Balada SB, Witholt B, van Beilen JB (2002) Functional analysis of alkane hydroxylases from gram-negative and gram-positive bacteria. J Bacteriol 184:1733–1742

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • So CM, Young LY (1999a) Initial reactions in anaerobic alkane degradation by a sulfate reducer, strain AK-01. Appl Environ Microbiol 65:5532–5540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • So CM, Young LY (1999b) Isolation and characterization of a sulfate-reducing bacterium that anaerobically degrades alkanes. Appl Environ Microbiol 65:2969–2976

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • So CM, Phelps CD, Young LY (2003) Anaerobic transformation of alkanes to fatty acids by a sulfate-reducing bacterium, strain Hxd3. Appl Environ Microbiol 69:3892–3900

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sorkhoh NA, Ghannoum MA, Ibrahim AS, Stretton RJ, Radwan SS (1990) Crude oil and hydrocarbon-degrading strains of Rhodococcus rhodochrous isolated from soil and marine environments in Kuwait. Environ Pollut 65:1–17

    Article  CAS  PubMed  Google Scholar 

  • Sorkhoh NA, Ibrahim AS, Ghannoum MA, Radwan SS (1993) High-temperature hydrocarbon degradation by Bacillus stearothermophilus from oil-polluted Kuwaiti desert. Appl Microbiol Biotechnol 39:123–126

    Article  CAS  Google Scholar 

  • Spormann AM, Widdel F (2000) Metabolism of alkylbenzenes, alkanes, and other hydrocarbons in anaerobic bacteria. Biodegradation 11:85–105

    Article  CAS  PubMed  Google Scholar 

  • Sullivan JP, Dickinson D, Chase HA (1998) Methanotrophs, Methylosinus trichosporium OB3b, sMMO, and their application to bioremediation. Crit Rev Microbiol 24:335–373

    Article  CAS  PubMed  Google Scholar 

  • Syutsubo K, Kishira H, Harayama S (2001) Development of specific oligonucleotide probes for the identification and in situ detection of hydrocarbon-degrading Alcanivorax strains. Environ Microbiol 3:371–379

    Article  CAS  PubMed  Google Scholar 

  • Tani A, Ishige T, Sakai Y, Kato N (2001) Gene structures and regulation of the alkane hydroxylase complex in Acinetobacter sp. strain M-1. J Bacteriol 183:1819–1823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thijsse GJE, Linden ACvd (1958) n-Alkane oxidation by Pseudomonas. Antonie Van Leeuwenhoek 24:298–308

    Article  Google Scholar 

  • Throne-Holst M, Markussen S, Winnberg A, Ellingsen TE, Kotlar HK, Zotchev SB (2006) Utilization of n-alkanes by a newly isolated strain of Acinetobacter venetianus: the role of two AlkB-type alkane hydroxylases. Appl Microbiol Biotechnol 72:53–360

    Article  CAS  Google Scholar 

  • Throne-Holst M, Wentzel A, Ellingsen TE, Kotlar HK, Zotchev SB (2007) Identification of novel genes involved in long-chain n-alkane degradation by Acinetobacter sp. strain DSM 17874. Appl Environ Microbiol 73:3327–3332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uthoff S, Stöveken T, Weber N, Vosmann K, Klein E, Kalscheuer R, Steinbüchel A (2005) Thio wax ester biosynthesis utilizing the unspecific bifunctional wax ester synthase/acyl coenzyme A:diacylglycerol acyltransferase of Acinetobacter sp. strain ADP1. Appl Environ Microbiol 71:790–796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Beilen JB, Eggink G, Enequist H, Bos R, Witholt B (1992) DNA sequence determination and functional characterization of the OCT-plasmid-encoded alkJKL genes of Pseudomonas oleovorans. Mol Microbiol 6:3121–3136

    Article  PubMed  Google Scholar 

  • van Beilen JB, Funhoff EG (2007) Alkane hydroxylases involved in microbial alkane degradation. Appl Microbiol Biotechnol 74:13–21

    Article  CAS  PubMed  Google Scholar 

  • van Beilen JB, Funhoff EG, van Loon A, Just A, Kaysser L, Bouza M, Holtackers R, Röthlisberger M, Li Z, Witholt B (2006) Cytochrome P450 alkane hydroxylases of the CYP153 family are common in alkane-degrading eubacteria lacking integral membrane alkane hydroxylases. Appl Environ Microbiol 72:59–65

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • van Beilen JB, Li Z, Duetz WA, Smits TH, Witholt B (2003) Diversity of alkane hydroxylase systems in the environment. Oil Gas Sci Technol 58:427–440

    Article  Google Scholar 

  • van Beilen JB, Marin MM, Smits TH, Röthlisberger M, Franchini AG, Witholt B, Rojo F (2004) Characterization of two alkane hydroxylase genes from the marine hydrocarbonoclastic bacterium Alcanivorax borkumensis. Environ Microbiol 6:264–273

    Article  CAS  PubMed  Google Scholar 

  • van Beilen JB, Panke S, Lucchini S, Franchini AG, Röthlisberger M, Witholt B (2001) Analysis of Pseudomonas putida alkane-degradation gene clusters and flanking insertion sequences: evolution and regulation of the alk genes. Microbiology 147:1621–1630

    Article  PubMed  Google Scholar 

  • van Hamme JD, Singh A, Ward OP (2003) Recent advances in petroleum microbiology. Microbiol Mol Biol Rev 67:503–549

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • van Hamme JD, Singh A, Ward OP (2006) Physiological aspects: Part 1 in a series of papers devoted to surfactants in microbiology and biotechnology. Biotechnol Adv 24:604–620

    Article  PubMed  CAS  Google Scholar 

  • van Beilen JB, Smits TH, Whyte LG, Schorcht S, Röthlisberger M, Plaggemeier T, Engesser KH, Witholt B (2002) Alkane hydroxylase homologues in gram-positive strains. Environ Microbiol 4:676–682

    Article  PubMed  Google Scholar 

  • van Beilen JB, Wubbolts MG, Witholt B (1994a) Genetics of alkane oxidation by Pseudomonas oleovorans. Biodegradation 5:161–174

    Article  PubMed  Google Scholar 

  • van Beilen JB, Kingma J, Witholt B (1994b) Substrate specificity of the alkane hydroxylase system of Pseudomonas oleovorans GPo1. Enzyme Microb Technol 16:904–911

    Article  Google Scholar 

  • Vaneechoutte M, Young DM, Ornston LN, De Baere T, Nemec A, Van Der Reijden T, Carr E, Tjernberg I, Dijkshoorn L (2006) Naturally transformable Acinetobacter sp. strain ADP1 belongs to the newly described species Acinetobacter baylyi. Appl Environ Microbiol 72:932–936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • von der Weid I, Marques JM, Cunha CD, Lippi RK, Dos Santos SC, Rosado AS, Lins U, Seldin L (2006) Identification and biodegradation potential of a novel strain of Dietzia cinnamea isolated from a petroleum-contaminated tropical soil. Syst Appl Microbiol 30:331–339

    Article  PubMed  CAS  Google Scholar 

  • Wang L, Tang Y, Wang S, Liu RL, Liu MZ, Zhang Y, Liang FL, Feng L (2006) Isolation and characterization of a novel thermophilic Bacillus strain degrading long-chain n-alkanes. Extremophiles 10:347–356

    Article  CAS  PubMed  Google Scholar 

  • Whyte LG, Hawari J, Zhou E, Bourbonniere L, Inniss WE, Greer CW (1998) Biodegradation of variable-chain-length alkanes at low temperatures by a psychrotrophic Rhodococcus sp. Appl Environ Microbiol 64:2578–2584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilkes H, Kuhner S, Bolm C, Fischer T, Classen A, Widdel F, Rabus R (2003) Formation of n-alkane- and cycloalkane-derived organic acids during anaerobic growth of a denitrifying bacterium with crude oil. Org Geochem 34:1313–1323

    Article  CAS  Google Scholar 

  • Wilkes H, Rabus R, Fischer T, Armstroff A, Behrends A, Widdel F (2002) Anaerobic degradation of n-hexane in a denitrifying bacterium: Further degradation of the initial intermediate (1-methylpentyl)succinate via C-skeleton rearrangement. Arch Microbiol 177:235–243

    Article  CAS  PubMed  Google Scholar 

  • Witholt B, de Smet MJ, Kingma J, van Beilen JB, Kok M, Lageveen RG, Eggink G (1990) Bioconversions of aliphatic compounds by Pseudomonas oleovorans in multiphase bioreactors: background and economic potential. Trends Biotechnol 8:46–52

    Article  CAS  PubMed  Google Scholar 

  • Wongsa P, Tanaka M, Ueno A, Hasanuzzaman M, Yumoto I, Okuyama H (2004) Isolation and characterization of novel strains of Pseudomonas aeruginosa and Serratia marcescens possessing high efficiency to degrade gasoline, kerosene, diesel oil, and lubricating oil. Curr Microbiol 49:415–422

    Article  CAS  PubMed  Google Scholar 

  • Wubbolts MG, Favre-Bulle O, Witholt B (1996) Biosynthesis of synthons in two-liquid-phase media. Biotechnol Bioeng 52:301–308

    Article  CAS  PubMed  Google Scholar 

  • 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 54:141–148

    Article  CAS  PubMed  Google Scholar 

  • Yan PL (2006) Alkane-degrading functional bacteria, its cultivation method and application. CN1789408, 2006–06–21, CN20041081505 20041217, CHENGDU BIOLOGY RES INST OF TH (CN)

  • Yumoto I, Nakamura A, Iwata H, Kojima K, Kusumoto K, Nodasaka Y, Matsuyama H (2002) Dietzia psychralcaliphila sp. nov., a novel, facultatively psychrophilic alkaliphile that grows on hydrocarbons. Int J Syst Evol Microbiol 52:85–90

    Article  CAS  PubMed  Google Scholar 

  • Yuste L, Canosa I, Rojo F (1998) Carbon-source-dependent expression of the PalkB promoter from the Pseudomonas oleovorans alkane degradation pathway. J Bacteriol 180:5218–5226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuste L, Corbella ME, Turiegano MJ, Karlson U, Puyet A, Rojo F (2000) Characterization of bacterial strains able to grow on high molecular mass residues from crude oil processing. FEMS Microbiol Ecol 32:69–75

    Article  CAS  PubMed  Google Scholar 

  • Zarilla KA, Perry JJ (1984) Thermoleophilum album gen. nov. and sp. nov., a bacterium obligate for thermophily and n-alkane substrates. Arch Microbiol 137:286–290

    Article  CAS  Google Scholar 

  • Zarilla K, Perry JJ (1987) Bacillus thermoleovorans, sp. nov., a species of obligately thermophilic hydrocarbon utilizing endospore forming bacteria. Syst Appl Microbiol 9:258–264

    Article  CAS  Google Scholar 

  • Zengler K, Richnow HH, Rossello-Mora R, Michaelis W, Widdel F (1999) Methane formation from long-chain alkanes by anaerobic microorganisms. Nature 401:266–269

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Kallimanis A, Koukkou AI, Drainas C (2004) Isolation and characterization of novel bacteria degrading polycyclic aromatic hydrocarbons from polluted Greek soils. Appl Microbiol Biotechnol 65:124–131

    Article  CAS  PubMed  Google Scholar 

  • Zhuang WQ, Tay JH, Maszenan AM, Krumholz LR, Tay ST (2003) Importance of gram-positive naphthalene-degrading bacteria in oil–contaminated tropical marine sediments. Lett Appl Microbiol 36:251–257

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Biotechnology, Norwegian University of Science and Technology, Sem Saelandsvei 6/8, 7491, Trondheim, Norway

    Alexander Wentzel & Sergey B. Zotchev

  2. Department of Biotechnology, SINTEF Materials and Chemistry, Sem Saelandsvei 2A, 7465, Trondheim, Norway

    Alexander Wentzel, Trond E. Ellingsen & Mimmi Throne-Holst

  3. Statoil ASA, R&D, Arkitekt Ebbellsvei 10, Rotvoll, 7005, Trondheim, Norway

    Hans-Kristian Kotlar

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  1. Alexander Wentzel
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  2. Trond E. Ellingsen
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  3. Hans-Kristian Kotlar
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  4. Sergey B. Zotchev
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  5. Mimmi Throne-Holst
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Correspondence to Alexander Wentzel.

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Wentzel, A., Ellingsen, T.E., Kotlar, HK. et al. Bacterial metabolism of long-chain n-alkanes. Appl Microbiol Biotechnol 76, 1209–1221 (2007). https://doi.org/10.1007/s00253-007-1119-1

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  • DOI: https://doi.org/10.1007/s00253-007-1119-1

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