Diversity, Function, and Biocatalytic Applications of Alkane Oxygenases

Jan B. van Beilen; Berhard Witholt

doi:10.1128/9781555817589.ch13

Chapter 13 : Diversity, Function, and Biocatalytic Applications of Alkane Oxygenases

Authors: Jan B. van Beilen¹, Berhard Witholt²

VIEW AFFILIATIONS HIDE AFFILIATIONS

Affiliations: 1: Institute of Biotechnology, ETH Zürich, Wolfgang Pauli Strasse 16, ETH Hönggerberg HPT, CH-8093 Zürich, Switzerland; 2: Institute of Biotechnology, ETH Zürich, Wolfgang Pauli Strasse 16, ETH Hönggerberg HPT, CH-8093 Zürich, Switzerland

Content Type: Monograph

Publication Year: 2005

Category: Applied and Industrial Microbiology; Environmental Microbiology

Book DOI: 10.1128/9781555817589

Chapter DOI: 10.1128/9781555817589.ch13

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:

Diversity, Function, and Biocatalytic Applications of Alkane Oxygenases, Page 1 of 2

< Previous page | Next page > /docserver/preview/fulltext/10.1128/9781555817589/9781555813277_Chap13-1.gif /docserver/preview/fulltext/10.1128/9781555817589/9781555813277_Chap13-2.gif

Abstract:

This chapter focuses on the aerobic degradation of hydrocarbons, with an emphasis on alkanes, and the applications of enzymes involved in these processes for biocatalysis. Yeasts and fungi are often mentioned as alkane degraders, for example in connection with the production of single-cell proteins or organic acids and amino acids from hydrocarbons. Soluble and particulate mono-oxygenases are known to oxidize the same compounds, and some of the gene diversity detected with primers that amplify membrane-bound methane mono-oxygenase (pMMO) and soluble MMO (sMMO) genes may well be due to short-chain alkane-degrading bacteria instead of methanotrophs. The application of oxygenases in biocatalytic processes is more complicated than that of enzymes such as hydrolases, because of cofactor and oxygen requirements, the sensitive nature of many oxygenases, the toxicity of substrates and products to the biocatalyst, and the uptake of the lipophilic substrates. The best strain in this study was a hexane-degrading Sphingomonas sp. strain HXN-200, isolated from a trickling-bed bioreactor. The oxygenases that are required for the initial activation of alkanes belong to several different enzyme classes, some of which act on medium- and long-chain alkanes, while others oxidize only short-chain alkanes. Studies of alkane hydroxylase (AH) gene diversity, coupled with information on substrate range, induction, enzyme kinetics, and host properties, should help in understanding and optimizing the biodegradative activity of indigenous hydrocarbon-degrading strains, benefit biocatalytic applications, and promote fundamental research on the activation of oxygen by enzymes and biomimetic catalysts.

Citation: van Beilen J, Witholt B. 2005. Diversity, Function, and Biocatalytic Applications of Alkane Oxygenases, p 259-276. In Ollivier B, Magot M (ed), Petroleum Microbiology. ASM Press, Washington, DC. doi: 10.1128/9781555817589.ch13

Highlighted Text: Show | Hide

Full text loading...

Figures

Diversity, Function, and Biocatalytic Applications of Alkane Oxygenases

[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555817589.chap13-1,webId=/content/author/10.1128/9781555817589.chap13-1,properties={foaf_givenname=Jan B., foaf_name=Jan B. van Beilen, foaf_surname=van Beilen, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555817589.chap13-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555817589.chap13-2,webId=/content/author/10.1128/9781555817589.chap13-2,properties={foaf_givenname=Berhard, foaf_name=Berhard Witholt, foaf_surname=Witholt, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555817589.chap13-aff2]]}]]

/content/10.1128/9781555817589.chap13.fig13-1

FIGURE 1

Pathways for the degradation of alkanes by terminal, subterminal, and biterminal oxidation. Terminal oxidation leads to the formation of fatty acids, which enter the β-oxidation pathway. Alternatively, ω-hydroxylation by a fatty acid mono-oxygenase or AH may take place, leading to dicarboxylic acids. Subterminal oxidation gives rise to secondary alcohols, which are oxidized to a ketone. A Baeyer-Villiger mono-oxygenase converts the ketone to an ester, which is subsequently cleaved by an esterase. (Reprinted from Oil and Gas Science and Technology [ van Beilen et al, 2003b ] with permission of the publisher.)

10.1128/9781555817589/fig13-1_thmb.gif

10.1128/9781555817589/fig13-1.gif

FIGURE 1

/content/10.1128/9781555817589.chap13.fig13-2

FIGURE 2

Oxidation reactions catalyzed by AHs. See the text for details and references.

10.1128/9781555817589/fig13-2_thmb.gif

10.1128/9781555817589/fig13-2.gif

FIGURE 2

Oxidation reactions catalyzed by AHs. See the text for details and references.

References

/content/book/10.1128/9781555817589.chap13

1. Abbott, B. J.,, and C. T. Hou. 1973. Oxidation of 1-alkenes to 1,2-epoxyalkanes by Pseudomonas oleovorans. Appl. Microbiol. 26: 86– 91.

2. Al-Hasan, R. H.,, M. Khanafer,, M. Eliyas,, and S. S. Radwan. 2001. Hydrocarbon accumulation by picocyanobacteria from the Arabian Gulf. J. Appl. Microbiol. 91: 533– 540.

3. Angelova, B.,, and H. P. Schmauder. 1999. Lipophilic compounds in biotechnology—interactions with cells and technological problems. J. Biotechnol. 67: 13– 32.

4. Anzai, Y.,, H. Kim,, J. Y. Park,, H. Wakabayashi,, and H. Oyaizu. 2000. Phylogenetic affiliation of the pseudomonads based on 16S rRNA sequence. Int. J. Syst. Evol. Microbiol. 50: 1563– 1589.

5. April, T. M.,, J. M. Foght,, and R. S. Currah. 2000. Hydrocarbon-degrading filamentous fungi isolated from flare pit soils in northern and western Canada. Can. J. Microbiol. 46: 38– 49.

6. Ashraf, W.,, A. Mihdhir,, and J. C. Murrell. 1994. Bacterial oxidation of propane. FEMS Microbiol. Lett. 122: 1– 6.

7. Asperger, O.,, K. Wirkner,, M. Schmidt,, and E. Flechsig. 1994. Detection of diverse cytochrome P450-dependent biooxygenation catalysts in microorganisms using a multipurpose inducer. Biocatalysis 10: 233– 246.

8. Atlas, R. M.,, and R. Bartha. 1992. Hydrocarbon biodegradation and oil spill bioremediation. Adv. Microb. Ecol. 12: 287– 338.

9. Baptist, J. N.,, R. K. Gholson,, and M. J. Coon. 1963. Hydrocarbon oxidation by a bacterial enzyme system. I. Products of octane oxidation. Biochim. Biophys. Acta 69: 40– 47.

10. Baumann, P.,, M. Doudoroff,, and R. Y. Stanier. 1968. A study of the Moraxella group. II. Oxidative- negative species (genus Acinetobacter). J. Bacteriol. 95: 1520– 1541.

11. Bell, S. G.,, E. Orton,, H. Boyd,, J. A. Stevenson,, A. Riddle,, S. Campbell,, and L. L. Wong. 2003. Engineering cytochrome P450cam into an alkane hydroxylase. Dalton Trans. 2003: 2133– 2140.

12. Berekaa, M. M.,, and A. Steinbuchel. 2000. Microbial degradation of the multiply branched alkane 2,6,10,15,19,23-hexamethyltetracosane (squalane) by Mycobacterium fortuitum and Mycobacterium ratisbonense. Appl. Environ. Microbiol. 66: 4462– 4467.

13. Bogan, B. W.,, W. R. Sullivan,, K. J. Kayser,, K. D. Derr,, H. C. Aldrich,, and J. R. Peterek. 2003. Alkanindiges illinoisensis gen. nov., sp. nov., an obligately hydrocarbonoclastic, aerobic squalane- degrading bacterium isolated from oilfield soils. Int. J. Syst. Evol. Microbiol. 53: 1389– 1395.

14. Bosetti, A.,, J. B. van Beilen,, H. Preusting,, R. G. Lageveen,, and B. Witholt. 1992. Production of primary aliphatic alcohols with a recombinant Pseudomonas strain, encoding the alkane hydroxylase enzyme system. Enzyme Microb. Technol. 14: 702– 708.

15. Bourre, J. M.,, C. Cassagne,, S. Larrouquerre- Regnier,, and D. Darriet. 1977. Occurence of alkanes in brain myelin. Comparison between normal and quaking mouse. J. Neurochem. 29: 645– 648.

16. Bredholt, H.,, P. Bruheim,, M. Potocky,, and K. Eimhjellen. 2002. Hydrophobicity development, alkane oxidation, and crude-oil emulsification in a Rhodococcus species. Can. J. Microbiol. 48: 295– 304.

17. Britton, L. N., 1984. Microbial degradation of aliphatic hydrocarbons, p. 89– 129. In D. T. Gibson (ed.), Microbial Degradation of Organic Compounds, vol. 13. Marcel Dekker, New York, N.Y.

18. Broadway, N. M.,, F. M. Dickinson,, and C. Ratledge. 1993. The enzymology of dicarboxylic acid formation by Corynebacterium sp. strain 7E1C grown on n-alkanes. J. Gen. Microbiol. 139: 1337– 1344.

19. Bühler, M.,, and J. Schindler,. 1984. Aliphatic hydrocarbons, p. 329– 385. In K. Kieslich (ed.), Biotransformations, vol. 6a. Verlag Chemie Weinheim, Weinheim, Germany.

20. Cardini, G.,, and P. Jurtshuk. 1970. The enzymatic hydroxylation of n-octane by Corynebacterium sp. strain 7E1C. J. Biol. Chem. 245: 2789– 2796.

21. Chang, D. 2003. Regio- and Stereoselective Hydroxylations with Sphingomonas sp. HXN-200. Swiss Federal Institute of Technology, Zürich, Switzerland.

22. Chang, D.,, B. Witholt,, and Z. Li. 2000. Preparation of (S)-N-substituted 4-hydroxy-pyrrolidine- 2-ones by regio- and stereoselective hydroxylation with Sphingomonas sp. HXN-200. Org. Lett. 2: 3949– 3952.

23. Chang, D.,, H.-J. Feiten,, K.-H. Engesser,, J. B. van Beilen,, B. Witholt,, and Z. Li. 2002. Practical syntheses of N-substituted 3-hydroxyazetidines and 4-hydroxypiperidines by hydroxylation with Sphingomonas sp. HXN-200. Org. Lett. 4: 1859– 1862.

24. Chang, H. S.,, and L. Alvarez Cohen. 1995. Transformation capacities of chlorinated organics by mixed cultures enriched on methane, propane, toluene, or phenol. Biotechnol. Bioeng. 45: 440– 449.

25. Clifford, K. H.,, G. T. Phillips,, and A. F. Marx. August 1991. Process for the preparation of substituted phenoxy propanoic acids. U.S. patent 5,037,759.

26. Crespo, R.,, M. P. Juarez,, G. M. Dal Bello,, S. Padin,, G. C. Fernandez,, and N. Pedrini. 2002. Increased mortality of Acanthoscelides obtectus by alkane-grown Beauveria bassiana. Biocontrol 47: 685– 696.

27. Davies, H. G.,, R. H. Green,, D. R. Kelly,, and S. M. Roberts. 1989. Biotransformations in Preparative Organic Chemistry. Academic Press, London, United Kingdom.

28. de Smet, M.-J.,, H. Wijnberg,, and B. Witholt. 1981. Synthesis of 1,2-epoxyoctane by Pseudomonas oleovorans during growth in a two-phase system containing high concentrations of 1-octene. Appl. Environ. Microbiol. 42: 811– 816.

29. Duetz, W. A.,, J. B. van Beilen,, and B. Witholt. 2001. Using proteins in their natural environment: potential and limitations of microbial whole-cell hydroxylations in applied biocatalysis. Curr. Opin. Biotechnol. 12: 419– 425.

30. Ehrlich, H. L. 2002. Geomicrobiology, 4th ed. Marcel Dekker, Inc., Basel, Switzerland.

31. Engelhardt, M. A.,, K. Daly,, R. P. J. Swannell,, and I. M. Head. 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.

32. Feitkenhauer, H.,, R. Müller,, and H. Ma¨rkl. 2003. Degradation of polycyclic aromatic hydrocarbons and long chain alkanes at 60-70°C by Thermus and Bacillus spp. Biodegradation 14: 367– 372.

33. Flitsch, S. L.,, S. J. Aitken,, C. S.-Y. Chow,, G. Grogan,, and A. Staines. 1999. Biohydroxylation reactions catalyzed by enzymes and whole-cell systems. Bioorg. Chem. 27: 81– 90.

34. Foster, J. W. 1962. Hydrocarbons as substrates for microorganisms. Antonie Leeuwenhoek 28: 241– 274.

35. Fu, H.,, M. Newcomb,, and C. H. Wong. 1991. Pseudomonas oleovorans monooxygenase catalyzed asymmetric epoxidation of allyl alcohol derivatives and hydroxylation of a hypersensitive radical probe with the radical ring opening state exceeding the oxygen rebound state. J. Am. Chem. Soc 113: 5878– 5880.

36. Fukui, S.,, and A. Tanaka. 1980. Production of useful compounds from alkane media in Japan. Adv. Biochem. Eng. 17: 1– 35.

37. Glieder, A.,, E. T. Farinas,, and F. H. Arnold. 2002. Laboratory evolution of a soluble, selfsufficient, highly active alkane hydroxylase. Nat. Biotechnol. 20: 1135– 1139.

38. Golyshin, P. N.,, T. Chernikova,, W. R. Abraham,, H. Lünsdorf,, K. N. Timmis,, and M. M. Yakimov. 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– 911.

39. Hamamura, N.,, R. T. Storfa,, L. Semprini,, and D. J. Arp. 1999. Diversity in butane monooxygenases among butane-grown bacteria. Appl. Environ. Microbiol. 65: 4586– 4593.

40. Hamamura, N.,, C. M. Yeager,, and D. J. Arp. 2001. Two distinct monooxygenases for alkane oxidation in Nocardioides sp. strain CF8. Appl. Environ. Microbiol. 67: 4992– 4998.

41. Harayama, S.,, H. Kishira,, Y. Kasai,, and K. Shutsubo. 1999. Petroleum biodegradation in marine environments. J. Mol. Microbiol. Biotechnol. 1: 63– 70.

42. Hayaishi, O.,, M. Katagiri,, and S. Rothberg. 1955. Mechanism of the pyrocatechase reaction. J. Am. Chem. Soc. 77: 5450– 5451.

43. Holland, H. L. 1991. Organic Synthesis with Oxidative Enzymes. VCH Publishers, Inc., New York, N.Y.

44. Hou, C. T.,, M. A. Jackson,, M. O. Bagby,, and L. A. Becker. 1994. Microbial oxidation of cumene by octane-grown cells. Appl. Microbiol. Biotechnol. 41: 178– 182.

45. Huybregtse, R.,, and A. C. van der Linden. 1964. Oxidation of α-olefins by a Pseudomonas. Reactions involving the double bond. Antonie Leeuwenhoek 30: 185– 196.

46. Iida, T.,, T. Sumita,, A. Ohta,, and M. Takagi. 2000. The cytochrome P450ALK multigene family of an n-alkane-assimilating yeast, Yarrowia lipolytica: cloning and characterization of genes coding for new CYP52 family members. Yeast 16: 1077– 1087.

47. Johnstone, S. L.,, G. T. Phillips,, B. W. Robertson,, P. D. Watts,, M. A. Bertola,, H. S. Koger,, and A. F. Marx,. 1986. Stereoselective synthesis of S-(-)- β-blockers via microbially produced epoxide intermediates, p. 387– 392. In C. Laane,, J. Tramper,, and M. D. Lilly (ed.), Biocatalysis in Organic Media. Elsevier, Amsterdam, The Netherlands.

48. Kaserer, H. 1906. Ueber die Oxidation des Wasserstoffes und des Methans durch Mikroorganismen. Zentbl. Bakteriol. Abt. 2 15: 573– 576.

49. Katopodis, A. G.,, H. A. Smith,, and S. W. May. 1988. New oxyfunctionalization capabilities for ohydroxylases: asymmetric aliphatic sulfoxidation and branched ether demethylation. J. Am. Chem. Soc. 110: 897– 899.

50. Kiener, A. 1992. Enzymatic oxidation of methyl groups on aromatic heterocycles: a versatile method for the preparation of heteroaromatic carboxylic acids. Angew. Chem. Int. Ed. Engl. 31: 774– 775.

51. Kok, M.,, R. Oldenhuis,, M. P. G. van der Linden,, P. Raatjes,, J. Kingma,, P. H. van Lelyveld,, and B. Witholt. 1989. The Pseudomonas oleovorans alkane hydroxylase gene. Sequence and expression. J. Biol. Chem. 264: 5435– 5441.

52. Kolattukudy, P. E. (ed.). 1976. Chemistry and Biochemistry of Natural Waxes. Elsevier Scientific Publishing Co., Amsterdam, The Netherlands.

53. Labinger, J. A.,, and J. E. Bercaw. 2002. Understanding and exploiting C-H bond activation. Nature 417: 507– 514.

54. Lehman, L. R.,, and J. D. Stewart. 2001. Filamentous fungi: potentially useful catalysts for the biohydroxylations of non-activated carbon centers. Curr. Org. Chem. 5: 439– 470.

55. Li, Z.,, H.-J. Feiten,, J. B. van Beilen,, W. Duetz,, and B. Witholt. 1999. Preparation of optically active N-benzyl-3-hydroxypyrrolidine by enzymatic hydroxylation. Tetrahedron Asymmetry 10: 1323– 1333.

56. Li, Z.,, H.-J. Feiten,, D. Chang,, W. A. Duetz,, J. B. van Beilen,, and B. Witholt. 2001. Preparation of (R)- and (S)-N-protected-3-hydroxypyrrolidines by hydroxylation with Sphingomonas sp. HXN-200, a highly active, regio-and stereoselective, and easy to handle biocatalyst. J. Org. Chem. 66: 8424– 8430.

57. Lindley, N. D. 1995. Bioconversion and biodegradation of aliphatic hydrocarbons. Can. J. Bot. Rev. Can. Bot. 73: S1034– S1042.

58. Lukins, H. B.,, and J. W. Foster. 1963. Utilization of hydrocarbons and hydrogen by mycobacteria. Z. Allg. Mikrobiol. 3: 251– 264.

59. Macnaughton, S. J.,, J. R. Stephen,, A. D. Venosa,, G. A. Davis,, Y. J. Chang,, and D. C. White. 1999. Microbial population changes during bioremediation of an experimental oil spill. Appl. Environ. Microbiol. 65: 3566– 3574.

60. Maeng, J. H.,, Y. Sakai,, Y. Tani,, and N. Kato. 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.

61. Maier, T.,, H.-H. Foerster,, O. Asperger,, and U. Hahn. 2001. Molecular characterization of the 56-kDa CYP153 from Acinetobacter sp. EB104. Biochem. Biophys. Res. Commun. 286: 652– 658.

62. Margesin, R.,, S. Gander,, G. Zacke,, A. M. Gounot,, and F. Schinner. 2003a. Hydrocarbon degradation and enzyme activities of cold-adapted bacteria and yeasts. Extremophiles 7: 451– 458.

63. Margesin, R.,, D. Labbe,, F. Schinner,, C. W. Greer,, and L. G. Whyte. 2003b. Characterization of hydrocarbon-degrading microbial populations in contaminated and pristine alpine soils. Appl. Environ. Microbiol. 69: 3085– 3092.

64. Marin, M. M.,, T. H. M. Smits,, J. B. van Beilen,, and F. Rojo. 2001. The alkane hydroxylase gene of Burkholderia cepacia RR10 is under catabolite repression control. J. Bacteriol. 183: 4202– 4209.

65. Marin, M.,, L. Yuste,, and F. Rojo. 2003. Differential expression of the components of the two alkane hydroxylases from Pseudomonas aeruginosa. J. Bacteriol. 185: 3232– 3237.

66. Mathys, R. G.,, A. Schmid,, and B. Witholt. 1999. Integrated two-liquid phase bioconversion and product-recovery processes for the oxidation of alkanes: process design and economic evaluation. Biotechnol. Bioeng. 64: 459– 477.

67. Matsui, T.,, and K. Furuhashi. 1995. Asymmetric oxidation of isopropylmoieties of aliphatic and aromatic hydrocarbons by Rhodococcus sp. 11B. Biosci. Biotechnol. Biochem. 59: 1342– 1344.

68. May, S. W.,, and B. J. Abbott. 1972. Enzymatic epoxidation. I. Alkane epoxidation by the ohydroxylation system of Pseudomonas oleovorans. Biochem. Biophys. Res. Commun. 48: 1230– 1234.

69. Mikolasch, A.,, E. Hammer,, and F. Schauer. 2003. Synthesis of imidazol-2-yl amino acids by using cells from alkane-oxidizing bacteria. Appl. Environ. Microbiol. 69: 1670– 1679.

70. Murrell, J. C.,, B. Gilbert,, and I. R. McDonald. 2000. Molecular biology and regulation of methane monooxygenase. Arch. Microbiol. 173: 325– 332.

71. National Research Council. 2002. Oil in the Sea III: Inputs, Fates, and Effects. National Academies Press, Washington, D.C.

72. Nazina, T. N.,, T. P. Tourova,, A. B. Poltaraus,, E. V. Novikova,, A. A. Grigoryan,, A. E. Ivanova,, A. M. Lysenko,, V. V. Petrunyaka,, G. A. Osipov,, S. S. Belyaev,, and M. V. Ivanov. 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.

73. Ohkuma, M.,, T. Zimmer,, T. Iida,, W. H. Schunck,, A. Ohta,, and M. Takagi. 1998. Isozyme function of n-alkane-inducible cytochromes P450 in Candida maltosa revealed by sequential gene disruption. J. Biol. Chem. 273: 3948– 3953.

74. Ooyama, J.,, and J. W. Foster. 1965. Bacterial oxidation of cycloparaffinic hydrocarbons. Antonie Leeuwenhoek 31: 45– 65.

75. Padda, R. S.,, K. K. Pandey,, S. Kaul,, V. D. Nair,, R. K. Jain,, S. K. Basu,, and T. Chakrabarti. 2001. A novel gene encoding a 54 kDa polypeptide is essential for butane utilization by Pseudomonas sp. IMT37. Microbiology 147: 2479– 2491.

76. Park, M. O.,, M. Tanabe,, K. Hirata,, and K. Miyamoto. 2001. Isolation and characterization of a bacterium that produces hydrocarbons extra-cellularly which are equivalent to light oil. Appl. Microbiol. Biotechnol. 56: 448– 452.

77. Peñuelas, J.,, and J. Llusià. 2003. BVOCs: plant defense against climate warming. Trends Plant Sci. 8: 105– 109.

78. Rahn, O. 1906. Ein Paraffin zersetzender Schimmelpilz. Zentbl. Bakteriol. Abt. 2 16: 382– 384.

79. Ratajczak, A.,, W. Geiβdörfer, andW.Hillen. 1998. Alkane hydroxylase from Acinetobacter sp. strain ADP- 1 is encoded by alkM and belongs to a new family of bacterial integral-membrane hydrocarbon hydroxylases. Appl. Environ. Microbiol. 64: 1175– 1179.

80. Röling, W. F. M.,, M. G. Milner,, D. M. Jones,, K. Lee,, F. Daniel,, R. J. P. Swannell,, and I. M. Head. 2002. Robust hydrocarbon degradation and dynamics of bacterial communities during nutrient-enhanced oil spill bioremediation. Appl. Environ. Microbiol. 68: 5537– 5548.

81. Savage, T. J.,, B. S. Hamilton,, and R. Croteau. 1996. Biochemistry of short-chain alkanes. Tissuespecific biosynthesis of n-heptane in Pinus jeffreyi. Plant Physiol. 110: 179– 186.

82. Scheller, U.,, T. Zimmer,, D. Becher,, F. Schauer,, and W. H. Schunck. 1998. Oxygenation cascade in conversion of n-alkanes to α,ω-dioic acids catalyzed by cytochrome P450 52A3. J. Biol. Chem. 273: 32528– 32534.

83. Schiestl, F. P.,, M. Ayasse,, H. F. Paulus,, C. Löfstedt,, B. S. Hansson,, F. Ibarra,, and W. Francke. 1999. Orchid pollination by sexual swindle. Nature 399: 421– 422.

84. Schmitz, C.,, I. Goebel,, S. Wagner,, A. Vomberg,, and U. Klinner. 2000. Competition between n-alkane- assimilating yeasts and bacteria during colonization of sandy soil microcosms. Appl . Microbiol. Biotechnol. 54: 126– 132.

85. Sluis, M. K.,, L. A. Sayavedra Soto,, and D. J. Arp. 2002. Molecular analysis of the soluble butane monooxygenase from ‘Pseudomonas butanovora.’ Microbiology 148: 3617– 3629.

86. Smits, T. H. M.,, M. Röthlisberger,, B. Witholt,, and J. B. van Beilen. 1999. Molecular screening for alkane hydroxylase genes in gram-negative and gram-positive strains. Environ. Microbiol. 1: 307– 318.

87. Smits, T. H. M.,, S. B. Balada,, B. Witholt,, and J. B. van Beilen. 2002. Functional analysis of alkane hydroxylases from gram-negative and gram-positive bacteria. J. Bacteriol. 184: 1733– 1742.

88. Smits, T. H. M.,, B. Witholt,, and J. B. van Beilen. 2003. Functional characterization of genes involved in alkane oxidation by Pseudomonas aeruginosa. Antonie Leeuwenhoek 84: 193– 200.

89. Söhngen, N. L. 1906. Ueber Bakterien, welche Methan als Kohlenstoffnahrung und Energiequelle gebrauchen. Zentbl. Bakteriol. Abt. 2 15: 513– 517.

90. Söhngen, N. L. 1913. Benzin, Petroleum, Paraffinöl und Paraffin als Kohlenstoff- und Energiequelle fu¨ r Mikroben. Zentbl. Bakteriol. Abt. 2 37: 595– 609.

91. Spigno, G.,, C. Pagella,, M. D. Fumi,, R. Molteni,, and D. M. De Faveri. 2003. VOCs removal from waste gases: gas-phase bioreactor for the abatement of hexane by Aspergillus niger. Chem. Eng. Sci. 58: 739– 746.

92. Sullivan, J. P.,, D. Dickinson,, and H. A. Chase. 1998. Methanotrophs, Methylosinus trichosporium OB3b, sMMO, and their application to bioremediation. Crit. Rev. Microbiol. 24: 335– 373.

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

94. Ueno, R.,, N. Urano,, S. Wada,, and S. Kimura. 2002. Optimization of heterotrophic culture conditions for n-alkane utilization and phylogenetic position based on the 18S rDNA sequence of a thermotolerant Prototheca zopfii strain. J. Biosci. Bioeng. 94: 160– 165.

95. van Beilen, J. B. 1994. Alkane oxidation by Pseudomonas oleovorans: genes and proteins. Ph.D. thesis. University of Groningen, Groningen, The Netherlands.

96. van Beilen, J. B.,, J. Kingma,, and B. Witholt. 1994a. Substrate specificity of the alkane hydroxylase of Pseudomonas oleovorans GPo1. Enzyme Microb. Technol. 16: 904– 911.

97. van Beilen, J. B.,, M. G. Wubbolts,, and B. Witholt. 1994b. Genetics of alkane oxidation by Pseudomonas oleovorans. Biodegradation 5: 161– 174.

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

99. van Beilen, J. B.,, T. H. M. Smits,, L. G. Whyte,, S. Schorcht,, M. Röthlisberger,, T. Plaggemeier,, K.-H. Engesser,, and B. Witholt. 2002. Alkane hydroxylase homologues in gram-positive strains. Environ. Microbiol. 4: 676– 682.

100. van Beilen, J. B.,, W. A. Duetz,, A. Schmid,, and B. Witholt. 2003a. Practical issues in the application of oxygenases. Trends Biotechnol. 21: 170– 177.

101. van Beilen, J. B.,, Z. Li,, W. A. Duetz,, T. H. M. Smits,, and B. Witholt. 2003b. Diversity of alkane hydroxylase systems in the environment. Oil Gas Sci. Technol. 58: 427– 440.

102. van Beilen, J. B.,, E. G. Funhoff,, A. van Loon,, A. Just,, L. Kaysser,, M. Bouza,, R. Holtackers,, M. Röthlisberger,, Z. Li,, and B. Witholt. Submitted for publication.

103. van Beilen, J. B.,, R. Holtackers,, D. Lu¨ scher,, U. Bauer,, B. Witholt,, and W. A. Duetz. 2005. Biocatalytic production of perillyl alcohol from limonene by using a novel Mycobacterium sp. cytochrome P450 alkane hydroxylase expressed in Pseudomonas putida. Appl. Environ. Microbiol. 71: 1737– 1744.

104. van Beilen, J. B.,, M. Marin,, T. H. M. Smits,, M. Röthlisberger,, A. Franchini,, B. Witholt,, and F. Rojo. 2004. Characterization of two alkane hydroxylase genes from the marine hydrocarbonoclastic bacterium Alcanivorax borkumensis. Environ. Microbiol. 6: 264– 273.

105. van Beilen, J. B.,, T. H. M. Smits,, S. B. Balada,, F. Roos,, T. Brunner,, and B. Witholt. 2005. Getting a hold on alkanes: identification of an amino acid position that determines the substrate range of integral-membrane alkane hydroxylases. J. Bacteriol. 187: 85– 91.

106. van Beilen, J. B.,, and B. Witholt,. 2004. Alkane degradation by pseudomonads, p. 397– 423. In J. L. Ramos (ed.), The Pseudomonads, vol. 3. Kluwer Academic Publishers, Dordrecht, The Netherlands.

107. van der Linden, A. C. 1963. Epoxidation of aolefins by heptane-grown Pseudomonas cells. Biochim. Biophys. Acta 77: 157– 159.

108. vanHamme, J. D.,, A. Singh,, and O. P. Ward. 2003. Recent advances in petroleum microbiology. Microbiol. Mol. Biol. Rev. 67: 503– 549.

109. van Ravenswaay Claasen, J. C.,, and A. C. van der Linden. 1971. Substrate specificity of the paraffin hydroxylase of Pseudomonas aeruginosa. Antonie Leeuwenhoek 37: 339– 352.

110. Walker, J. D.,, and R. S. Pore. 1978. Growth of Prototheca isolates on n-hexadecane and mixed-hydrocarbon substrate. Appl. Environ. Microbiol. 35: 694– 697.

111. Whyte, L. G.,, J. Hawari,, E. Zhou,, L. Bourbonnière,, W. E. Inniss,, and C. W. Greer. 1998. Biodegradation of variable-chain-length alkanes at low temperatures by a psychrotrophic Rhodococcus sp. Appl. Environ. Microbiol. 64: 2578– 2584.

112. Whyte, L. G.,, A. Schultz,, J. B. van Beilen,, A. P. Luz,, D. Pellizari,, D. Labbé,, and C. W. Greer. 2002a. Prevalence of alkane monooxygenase genes in arctic and antarctic hydrocarbon-contaminated and pristine soils. FEMS Microbiol. Ecol. 41: 141– 150.

113. Whyte, L. G.,, T. H. M. Smits,, D. Labbé,, B. Witholt,, C. W. Greer,, and J. B. van Beilen. 2002b. Cloning and characterization of multiple alkane hydroxylase systems in Rhodococcus spp. strains Q15 and 16531. Appl. Environ. Microbiol. 68: 5933– 5942.

114. Widdel, F.,, and R. Rabus. 2001. Anaerobic biodegradation of saturated and aromatic hydrocarbons. Curr. Opin. Biotechnol. 12: 259– 276.

115. Witholt, B.,, M. J. de Smet,, J. Kingma,, J. B. van Beilen,, M. Kok,, R. G. Lageveen,, and G. Eggink. 1990. Bioconversions of aliphatic compounds by Pseudomonas oleovorans in multiphase biorectors: background and economic potential. Trends Biotechnol. 8: 46– 52.

116. Yadav, J. S.,, and J. C. Loper. 1999. Multiple P450alk (cytochrome P450 alkane hydroxylase) genes from the halotolerant yeast Debaryomyces hansenii. Gene 226: 139– 146.

117. Yakimov, M. M.,, P. N. Golyshin,, S. Lang,, E. R. B. Moore,, W.-R. Abraham,, H. Lünsdorf,, and K. N. Timmis. 1998. Alcanivorax borkumensis gen. nov., sp. nov., a new, hydrocarbon-degrading and surfactant-producing marine bacterium. Int. J. Syst. Bacteriol. 48: 339– 348.

118. Yakimov, M. M.,, H. Lünsdorf,, and P. N. Golyshin. 2003. Thermoleophilum album and Thermoleophilum minutum are culturable representatives of group 2 of the Rubrobacteridae (Actinobacteria). Int. J. Syst. Evol. Microbiol. 53: 377– 380.

119. ZoBell, C. E. 1950. Assimilation of hydrocarbons by microorganisms. Adv. Enzymol. 10: 443– 486.

Tables

Diversity, Function, and Biocatalytic Applications of Alkane Oxygenases

/content/10.1128/9781555817589.chap13.tab13-1

TABLE 1

Genera containing isolates that aerobically degrade aliphatic hydrocarbons a

TABLE 1

Genera containing isolates that aerobically degrade aliphatic hydrocarbons a

/content/10.1128/9781555817589.chap13.tab13-2

TABLE 2

Enzyme classes shown to be involved in the oxidation of alkanes a

TABLE 2

Enzyme classes shown to be involved in the oxidation of alkanes a