Applied Microbiology and Biotechnology

, Volume 74, Issue 1, pp 13–21 | Cite as

Alkane hydroxylases involved in microbial alkane degradation

Mini-Review

Abstract

This review focuses on the role and distribution in the environment of alkane hydroxylases and their (potential) applications in bioremediation and biocatalysis. Alkane hydroxylases play an important role in the microbial degradation of oil, chlorinated hydrocarbons, fuel additives, and many other compounds. Environmental studies demonstrate the abundance of alkane degraders and have lead to the identification of many new species, including some that are (near)-obligate alkanotrophs. The availability of a growing collection of alkane hydroxylase gene sequences now allows estimations of the relative abundance of the different enzyme systems and the distribution of the host organisms.

References

  1. Austin RN et al (2006) The new diagnostic substrate bicyclohexane reveals a radical mechanism for bacterial cytochrome P450 in whole cells. Angew Chem Int Ed (in press) DOI 10.1002/anie.200603282
  2. Ayala M, Torres E (2004) Enzymatic activation of alkanes: constraints and prospective. Appl Catal A Gen 272:1–13CrossRefGoogle Scholar
  3. Baker PW, Futamata H, Harayama S, Watanabe K (2001) Molecular diversity of pMMO and sMMO in a TCE-contaminated aquifer during bioremediation. FEMS Microbiol Ecol 38:161–167CrossRefGoogle Scholar
  4. Bernhardt R (2006) Cytochromes P450 as versatile biocatalysts. J Biotechnol 124:128–145CrossRefGoogle Scholar
  5. Bertrand E et al (2005) Reaction mechanisms of non-heme diiron hydroxylases characterized in whole cells. J Inorg Biochem 99:1998–2006CrossRefGoogle Scholar
  6. Brakstad OG, Lodeng AGG (2005) Microbial diversity during biodegradation of crude oil in seawater from the North Sea. Microb Ecol 49:94–103CrossRefGoogle Scholar
  7. Colby J, Stirling DI, Dalton H (1977) Soluble methane mono-oxygenase of Methylococcus capsulatus (Bath)—its ability to oxygenate n-alkanes, n-alkenes, ethers, and alicyclic, aromatic and heterocyclic compounds. Biochem J 165:395–402Google Scholar
  8. Coleman NV, Bui NB, Holmes AJ (2006) Soluble di-iron monooxygenase gene diversity in soils, sediments and ethene enrichments. Environ Microbiol 8:1228–1239CrossRefGoogle Scholar
  9. Connon SA, Tovanabootr A, Dolan M, Vergin K, Giovannoni SJ, Semprini L (2005) Bacterial community composition determined by culture-independent and -dependent methods during propane-stimulated bioremediation in trichloroethene-contaminated groundwater. Environ Microbiol 7:165–178CrossRefGoogle Scholar
  10. Coon MJ (2005) Omega oxygenases: nonheme-iron enzymes and P450 cytochromes. Biochem Biophys Res Commun 338:378–385CrossRefGoogle Scholar
  11. Doughty DM, Sayavedra-Soto LA, Arp DJ, Bottomley PJ (2006) Product repression of alkane monooxygenase expression in ‘Pseudomonas butanovora’. J Bacteriol 188:2586–2592CrossRefGoogle Scholar
  12. Elliott SJ, Zhu M, Tso L, Nguyen HHT, Yip JHK, Chan SI (1997) Regio- and stereoselectivity of particulate methane monooxygenase from Methylococcus capsulatus (Bath). J Am Chem Soc 119:9949–9955CrossRefGoogle Scholar
  13. Fujii T, Narikawa T, Sumisa F, Arisawa A, Takeda K, Kato J (2006) Production of α, ω-alkanediols using Escherichia coli expressing a cytochrome P450 from Acinetobacter sp. OC4. Biosci Biotechnol Biochem 70:1379–1385CrossRefGoogle Scholar
  14. Funhoff EG, van Beilen JB (2006) Alkane activation by P450 oxygenases. Biocat Biotrans (in press)Google Scholar
  15. Funhoff EG, Bauer U, García-Rubio I, Witholt B, van Beilen JB (2006a) CYP153A6, a soluble P450 oxygenase catalyzing terminal-alkane-hydroxylation. J Bacteriol 188:5220–5227CrossRefGoogle Scholar
  16. Funhoff EG, Salzmann J, Bauer U, Witholt B, van Beilen JB (2006b) Hydroxylation and epoxidation reactions catalyzed by CYP153 enzymes. Enzyme Microb Technol (in press) DOI 10.1016/j.enzmictec.2006.06.014
  17. Groves JT (2006) High-valent iron in chemical and biological oxidations. J Inorg Biochem 100:434–447CrossRefGoogle Scholar
  18. Halsey KH, Sayavedra-Soto LA, Bottomley PJ, Arp DJ (2005) Trichloroethylene degradation by butane-oxidizing bacteria causes a spectrum of toxic effects. Appl Microbiol Biotechnol 68:794–801CrossRefGoogle Scholar
  19. Halsey KH, Sayavedra-Soto LA, Bottomley PJ, Arp DJ (2006) Site-directed amino acid substitutions in the hydroxylase a subunit of butane monooxygenase from Pseudomonas butanovora: implications for substrates knocking at the gate. J Bacteriol 188:4962–4969CrossRefGoogle Scholar
  20. Hamamura N, Storfa RT, Semprini L, Arp DJ (1999) Diversity in butane monooxygenases among butane-grown bacteria. Appl Environ Microbiol 65:4586–4593Google Scholar
  21. Hamamura N, Olson SH, Ward DM, Inskeep WP (2005) Diversity and functional analysis of bacterial communities associated with natural hydrocarbon seeps in acidic soils at Rainbow Springs, Yellowstone National Park. App Environ Microbiol 71:5943–5950CrossRefGoogle Scholar
  22. Harayama S, Kasai Y, Hara A (2004) Microbial communities in oil-contaminated seawater. Curr Opin Biotechnol 15:205–214CrossRefGoogle Scholar
  23. Head IM, Jones DM, Roling WFM (2006) Marine microorganisms make a meal of oil. Nature Rev Microbiol 4:173–182CrossRefGoogle Scholar
  24. Heiss-Blanquet S, Benoit Y, Marechaux C, Monot F (2005) Assessing the role of alkane hydroxylase genotypes in environmental samples by competitive PCR. J Appl Microbiol 99:1392–1403CrossRefGoogle Scholar
  25. Iida T, Sumita T, Ohta A, Takagi M (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 16:1077–1087CrossRefGoogle Scholar
  26. Johnson EL, Hyman MR (2006) Propane and n-butane oxidation by Pseudomonas putida GPo1. Appl Environ Microbiol 72:950–952CrossRefGoogle Scholar
  27. Johnson EL, Smith CA, O’Reilly KT, Hyman MR (2004) Induction of methyl tertiary butyl ether (MTBE)-oxidizing activity in Mycobacterium vaccae JOB5 by MTBE. Appl Environ Microbiol 70:1023–1030CrossRefGoogle Scholar
  28. Kim Y, Istok JD, Semprini L (2006) Push–pull tests evaluating in situ aerobic cometabolism of ethylene, propylene, and cis-1,2-dichloroethylene. J Contam Hydrol 82:165–181CrossRefGoogle Scholar
  29. Kitmitto A, Myronova N, Basu P, Dalton H (2005) Characterization and structural analysis of an active particulate methane monooxygenase trimer from Methylococcus capsulatus (Bath). Biochemistry 44:10954–10965CrossRefGoogle Scholar
  30. 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 185:7120–7128CrossRefGoogle Scholar
  31. Kubota M et al (2005) Isolation and functional analysis of cytochrome P450 CYP153A genes from various environments. Biosci Biotechnol Biochem 69:2421–2430CrossRefGoogle Scholar
  32. Leahy JG, Batchelor PJ, Morcomb SM (2003) Evolution of the soluble diiron monooxygenases. FEMS Microbiol Rev 27:449–479CrossRefGoogle Scholar
  33. Lee SG, Goo JH, Kim HG, Oh J-I, Kim YM, Kim SW (2004) Optimization of methanol biosynthesis from methane using Methylosinus trichosporium OB3b. Biotechnol Lett 26:947–950CrossRefGoogle Scholar
  34. Li Z et al (2002) Oxidative biotransformations using oxygenases. Curr Opin Chem Biol 6:136–144CrossRefGoogle Scholar
  35. Lieberman RL, Rosenzweig AC (2005) Crystal structure of a membrane-bound metalloenzyme that catalyzes the biological oxidation of methane. Nature 434:177–182CrossRefGoogle Scholar
  36. 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 178:3695–3700Google Scholar
  37. Maier T, Foerster H-H, Asperger O, Hahn U (2001) Molecular characterization of the 56-kDa CYP153 from Acinetobacter sp. EB104. Biochem Biophys Res Commun 286:652–658CrossRefGoogle Scholar
  38. Marchant R, Sharkey FH, Banat IM, Rahman TJ, Perfumo A (2006) The degradation of n-hexadecane in soil by thermophilic geobacilli. FEMS Microbiol Ecol 56:44–54CrossRefGoogle Scholar
  39. McDonald IR et al (2006) Diversity of soluble methane monooxygenase-containing methanotrophs isolated from polluted environments. FEMS Microbiol Lett 255:225–232CrossRefGoogle Scholar
  40. Meinhold P, Peters MW, Hartwick A, Hernandez AR, Arnold FH (2006) Engineering cytochrome P450 BM3 for terminal alkane hydroxylation. Adv Synth Catal 348:763–772CrossRefGoogle Scholar
  41. Meintanis C, Chalkou KI, Kormas KA, Karagouni AD (2006) Biodegradation of crude oil by thermophilic bacteria isolated from a volcano island. Biodegradation 17:3–9CrossRefGoogle Scholar
  42. Merkx M, Kopp DA, Sazinsky MH, Blazyk JL, Muller J, Lippard SJ (2001) Dioxygen activation and methane hydroxylation by soluble methane monooxygenase: a tale of two irons and three proteins. Angew Chem Int Ed 40:2782–2807CrossRefGoogle Scholar
  43. Murrell JC, Gilbert B, McDonald IR (2000) Molecular biology and regulation of methane monooxygenase. Arch Microbiol 173:325–332CrossRefGoogle Scholar
  44. Myronova N, Kitmitto A, Collins RF, Miyaji A, Dalton H (2006) Three-dimensional structure determination of a protein supercomplex that oxidizes methane to formaldehyde in Methylococcus capsulatus (Bath). Biochemistry 45:11905–11914CrossRefGoogle Scholar
  45. Nodate M, Kubota M, Misawa N (2006) Functional expression system for cytochrome P450 genes using the reductase domain of self-sufficient P450RhF from Rhodococcus sp. NCIMB 9784. Appl Microbiol Biotechnol 71:455–462CrossRefGoogle Scholar
  46. Pacheco-Oliver M, McDonald IR, Groleau D, Murrell JC, Miguez CB (2002) Detection of methanotrophs with highly divergent pmoA genes from Arctic soils. FEMS Microbiol Lett 209:313–319CrossRefGoogle Scholar
  47. Park M-O (2005) New pathway for long-chain n-alkane synthesis via 1-alcohol in Vibrio furnissii M1. J Bacteriol 187:1426–1429CrossRefGoogle Scholar
  48. 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 188:3763–3773CrossRefGoogle Scholar
  49. Shanklin J, Whittle E (2003) Evidence linking the Pseudomonas oleovorans alkane omega-hydroxylase, an integral membrane diiron enzyme, and the fatty acid desaturase family. FEBS Lett 545:188–192CrossRefGoogle Scholar
  50. Shennan JL (2006) Utilisation of C-2–C-4 gaseous hydrocarbons and isoprene by microorganisms. J Chem Technol Biotechnol 81:237–256CrossRefGoogle Scholar
  51. Smits THM, Röthlisberger M, Witholt B, van Beilen JB (1999) Molecular screening for alkane hydroxylase genes in Gram-negative and Gram-positive strains. Environ Microbiol 1:307–318CrossRefGoogle Scholar
  52. Smits THM, Balada SB, Witholt B, van Beilen JB (2002) Functional analysis of alkane hydroxylases from Gram-negative and Gram-positive bacteria. J Bacteriol 184:1733–1742CrossRefGoogle Scholar
  53. Söhngen NL (1913) Benzin, Petroleum, Paraffinöl und Paraffin als Kohlenstoff- und Energiequelle für Mikroben. Zentr Bacteriol Parasitenk Abt II 37:595–609Google Scholar
  54. Steinkamp R, Zimmer W, Papen H (2001) Improved method for detection of methanotrophic bacteria in forest soils by PCR. Curr Microbiol 42:316–322CrossRefGoogle Scholar
  55. 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 183:1819–1823CrossRefGoogle Scholar
  56. Urlacher VB, Eiben S (2006) Cytochrome P450 monooxygenases: perspectives for synthetic application. Trends Biotechnol 24:324–330CrossRefGoogle Scholar
  57. van Beilen JB, Witholt B (2004) Alkane degradation by pseudomonads. In: Ramos JL (ed) The Pseudomonads. Kluwer, DordrechtGoogle Scholar
  58. van Beilen JB, Funhoff EG (2005) Expanding the alkane oxygenase toolbox: new enzymes and applications. Curr Opin Biotechnol 16:308–314CrossRefGoogle Scholar
  59. van Beilen JB, Wubbolts MG, Witholt B (1994) Genetics of alkane oxidation by Pseudomonas oleovorans. Biodegradation 5:161–174CrossRefGoogle Scholar
  60. van Beilen JB et al (2002) Alkane hydroxylase homologues in Gram-positive strains. Environ Microbiol 4:676–682CrossRefGoogle Scholar
  61. van Beilen JB, Duetz WA, Schmid A, Witholt B (2003a) Practical issues in the application of oxygenases. Trends Biotechnol 21:170–177CrossRefGoogle Scholar
  62. van Beilen JB, Li Z, Duetz WA, Smits THM, Witholt B (2003b) Diversity of alkane hydroxylase systems in the environment. Oil Gas Sci Technol 58:427–440CrossRefGoogle Scholar
  63. van Beilen JB, Lüscher D, Holtacker R, Bauer U, Witholt B, Duetz WA (2005a) Biocatalytic production of perillyl alcohol from limonene using a novel Mycobacterium cytochrome P450 alkane hydroxylase expressed in P. putida. Appl Environ Microbiol 71:1737–1744CrossRefGoogle Scholar
  64. van Beilen JB, Smits THM, Balada SB, Roos FF, Brunner T, Witholt B (2005b) Identification of an amino acid position that determines the substrate range of integral-membrane alkane hydroxylases. J Bacteriol 187:85–91CrossRefGoogle Scholar
  65. van Beilen JB et al (2006) Cytochrome P450 alkane hydroxylases of the CYP153 family are common in alkane-degrading eubacteria lacking integral membrane alkane hydroxylases. Appl Environ Microbiol 72:59–65CrossRefGoogle Scholar
  66. Venter JC et al (2004) Environmental genome shotgun sequencing of the Sargasso Sea. Science 304:66–74CrossRefGoogle Scholar
  67. Xin J-Y et al (2004) Production of methanol from methane by methanotrophic bacteria. Biocatal Biotransform 22:225–229CrossRefGoogle Scholar
  68. Yakimov MM et al (2004) Thalassolituus oleivorans gen. nov., sp nov., a novel marine bacterium that obligately utilizes hydrocarbons. Int J Syst Evol Microbiol 54:141–148CrossRefGoogle Scholar
  69. Zhang J, Zheng H, Groce SL, Lipscomb JD (2006) Basis for specificity in methane monooxygenase and related non-heme iron-containing biological oxidation catalysts. J Mol Catal A Chem 251:54–65CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.Département de Biologie Moléculaire Végétale, Le Biophore, Quartier SorgeUniversité de LausanneLausanneSwitzerland
  2. 2.Institute of BiotechnologySwiss Federal Institute of TechnologyZurichSwitzerland

Personalised recommendations