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Genetic Features and Regulation of n-Alkane Metabolism in Bacteria

  • Renata Moreno
  • Fernando RojoEmail author
Reference work entry
Part of the Handbook of Hydrocarbon and Lipid Microbiology book series (HHLM)

Abstract

Expression of the bacterial genes involved in the assimilation of alkanes is usually tightly regulated. Regulators responding to the presence of alkanes ensure that the alkane-degradation genes are induced only when these hydrocarbons are available to the cell. In microorganisms containing several sets of alkane degradation genes (each dealing with a particular kind of alkane), these regulators ensure their differential induction. In addition, the expression of alkane degradation pathways is commonly down-modulated via complex global regulation control systems that ensure that the corresponding genes are expressed only under appropriate physiological conditions or when no other preferred compound is available. Examples illustrating these specific and global regulation processes are presented.

Notes

Acknowledgments

Work in the author’s laboratory is funded by the Spanish Ministry of Economy and Competitiveness (grant BIO2015-66203-P; MINECO/FEDER) and the European Commission VII Framework Program (grant number 312139).

References

  1. Anraku Y, Gennis RB (1987) The aerobic respiratory chain of Escherichia coli. Trends Biochem Sci 12:262–266CrossRefGoogle Scholar
  2. Aranda-Olmedo I, Ramos JL, Marques S (2005) Integration of signals through Crc and PtsN in catabolite repression of Pseudomonas putida TOL plasmid pWW0. Appl Environ Microbiol 71:4191–4198CrossRefGoogle Scholar
  3. Arp DJ (1999) Butane metabolism by butane-grown “ Pseudomonas butanovora”. Microbiology 145:1173–1180CrossRefGoogle Scholar
  4. Brussaard CP, Peperzak L, Beggah S, Wick LY, Wuerz B, Weber J, Samuel Arey J, van der Burg B, Jonas A, Huisman J, van der Meer JR (2016) Immediate ecotoxicological effects of short-lived oil spills on marine biota. Nat Commun 7:11206CrossRefGoogle Scholar
  5. Canosa I, Sánchez-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 35:791–799CrossRefGoogle Scholar
  6. 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 181:1748–1754PubMedPubMedCentralGoogle Scholar
  7. Chen Q, Janssen DB, Witholt B (1995) Growth on octane alters the membrane lipid fatty acids of Pseudomonas oleovorans due to the induction of alkB and synthesis of octanol. J Bacteriol 177:6894–6901CrossRefGoogle Scholar
  8. 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 178:5508–5512CrossRefGoogle Scholar
  9. Dinamarca MA, Aranda-Olmedo I, Puyet A, Rojo F (2003) Expression of the Pseudomonas putida OCT plasmid alkane degradation pathway is modulated by two different global control signals: evidence from continuous cultures. J Bacteriol 185:4772–4778CrossRefGoogle Scholar
  10. Dinamarca MA, Ruiz-Manzano A, Rojo F (2002) Inactivation of cytochrome o ubiquinol oxidase relieves catabolic repression of the Pseudomonas putida GPo1 alkane degradation pathway. J Bacteriol 184:3785–3793CrossRefGoogle Scholar
  11. Doughty DM, Halsey KH, Vieville CJ, Sayavedra-Soto LA, Arp DJ, Bottomley PJ (2007) Propionate inactivation of butane monooxygenase activity in “ Pseudomonas butanovora”: biochemical and physiological implications. Microbiology 153:3722–3729CrossRefGoogle Scholar
  12. 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
  13. Dubbels BL, Sayavedra-Soto LA, Bottomley PJ, Arp DJ (2009) Thauera butanivorans sp. nov., a C2-C9 alkane-oxidizing bacterium previously referred to as 'Pseudomonas butanovora'. Int J Syst Evol Microbiol 59:1576–1578CrossRefGoogle Scholar
  14. Fuqua WC, Winans SC, Greenberg EP (1994) Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176:269–275CrossRefGoogle Scholar
  15. Gallegos MT, Schleif R, Bairoch A, Hofmann K, Ramos JL (1997) Arac/XylS family of transcriptional regulators. Microbiol Mol Biol Rev 61:393–410PubMedPubMedCentralGoogle Scholar
  16. García-Mauriño SM, Pérez-Martínez I, Amador CI, Canosa I, Santero E (2013) Transcriptional activation of the CrcZ and CrcY regulatory RNAs by the CbrB response regulator in Pseudomonas putida. Mol Microbiol 89:189–205CrossRefGoogle Scholar
  17. 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 181:4292–4298PubMedPubMedCentralGoogle Scholar
  18. 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 123:546–556PubMedPubMedCentralGoogle Scholar
  19. Hara A, Baik SH, Syutsubo K, Misawa N, Smits TH, Beilen JB, van Harayama S (2004) Cloning and functional analysis of alkB genes in Alcanivorax borkumensis SK2. Environ Microbiol 6:191–197CrossRefGoogle Scholar
  20. Hernández-Arranz S, Moreno R, Rojo F (2013) The translational repressor Crc controls the Pseudomonas putida benzoate and alkane catabolic pathways using a multi-tier regulation strategy. Environ Microbiol 15:227–241CrossRefGoogle Scholar
  21. Hester KL, Lehman J, Najar F, Song L, Roe BA, MacGregor CH, Hager PW, Phibbs PV Jr, Sokatch JR (2000a) Crc is involved in catabolite repression control of the bkd operons of Pseudomonas putida and Pseudomonas aeruginosa. J Bacteriol 182:1144–1149CrossRefGoogle Scholar
  22. Hester KL, Madhusudhan KT, Sokatch JR (2000b) Catabolite repression control by crc in 2xYT medium is mediated by posttranscriptional regulation of bkdR expression in Pseudomonas putida. J Bacteriol 182:1150–1153CrossRefGoogle Scholar
  23. Johnson EL, Hyman MR (2006) Propane and n-butane oxidation by Pseudomonas putida GPo1. Appl Environ Microbiol 72:950–952CrossRefGoogle Scholar
  24. Kok M, Oldenhuis R, Linden MP, van der Raatjes P, Kingma J, Lelyveld PH, van Witholt B (1989) The Pseudomonas oleovorans alkane hydroxylase gene. Sequence and expression. J Biol Chem 264:5435–5441PubMedGoogle Scholar
  25. Kumari R, Tecon R, Beggah S, Rutler R, Arey JS, van der Meer JR (2011) Development of bioreporter assays for the detection of bioavailability of long-chain alkanes based on the marine bacterium Alcanivorax borkumensis strain SK2. Environ Microbiol 13:2808–2819CrossRefGoogle Scholar
  26. Kurth EG, Doughty DM, Bottomley PJ, Arp DJ, Sayavedra-Soto LA (2008) Involvement of BmoR and BmoG in n-alkane metabolism in “Pseudomonas butanovora”. Microbiology 154:139–147CrossRefGoogle Scholar
  27. Lea-Smith DJ, Biller SJ, Davey MP, Cotton CA, Perez Sepulveda BM, Turchyn AV, Scanlan DJ, Smith AG, Chisholm SW, Howe CJ (2015) Contribution of cyanobacterial alkane production to the ocean hydrocarbon cycle. Proc Natl Acad Sci USA 112:13591–11356CrossRefGoogle Scholar
  28. Liang JL, JiangYang JH, Nie Y, XL W (2016a) Regulation of the alkane hydroxylase CYP153 gene in a gram-positive alkane-degrading bacterium, Dietzia sp. strain DQ12-45-1b. Appl Environ Microbiol 82:608–619CrossRefGoogle Scholar
  29. Liang JL, Nie Y, Wang M, Xiong G, Wang YP, Maser E, XL W (2016b) Regulation of alkane degradation pathway by a TetR family repressor via an autoregulation positive feedback mechanism in a gram-positive Dietzia bacterium. Mol Microbiol 99:338–359CrossRefGoogle Scholar
  30. Liu C, Wang W, Wu Y, Zhou Z, Lai Q, Shao Z (2011) Multiple alkane hydroxylase systems in a marine alkane degrader, Alcanivorax dieselolei B-5. Environ Microbiol 13:1168–1178CrossRefGoogle Scholar
  31. Liu H, Xu J, Liang R, Liu J (2014) Characterization of the medium- and long-chain n-alkanes degrading Pseudomonas aeruginosa strain SJTD-1 and its alkane hydroxylase genes. PLoS One 9:e105506CrossRefGoogle Scholar
  32. MacGregor CH, Arora SK, Hager PW, Dail MB, Phibbs PV Jr (1996) The nucleotide sequence of the Pseudomonas aeruginosa pyrE-crc-rph region and the purification of the crc gene product. J Bacteriol 178:5627–5635CrossRefGoogle Scholar
  33. Madhushani A, del Peso-Santos T, Moreno R, Rojo F, Shingler V (2015) Transcriptional and translational control through the 5′-leader region of the dmpR master regulatory gene of phenol metabolism. Environ Microbiol 17:119–133CrossRefGoogle Scholar
  34. Magasanik B (1970) Glucose effects: inducer exclusion and repression. In: Beckwith J (ed) The lactose operon. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp 189–220Google Scholar
  35. Marín MM, Smits TH, Beilen JB, van Rojo F (2001) The alkane hydroxylase gene of Burkholderia cepacia RR10 is under catabolite repression control. J Bacteriol 183:4202–4209CrossRefGoogle Scholar
  36. Marín MM, Yuste L, Rojo F (2003) Differential expression of the components of the two alkane hydroxylases from Pseudomonas aeruginosa. J Bacteriol 185:3232–3237CrossRefGoogle Scholar
  37. Morales G, Linares JF, Beloso A, Albar JP, Martínez JL, Rojo F (2004) The Pseudomonas putida Crc global regulator controls the expression of genes from several chromosomal catabolic pathways for aromatic compounds. J Bacteriol 186:1337–1344CrossRefGoogle Scholar
  38. Morales G, Ugidos A, Rojo F (2006) Inactivation of the Pseudomonas putida cytochrome o ubiquinol oxidase leads to a significant change in the transcriptome and to increased expression of the CIO and cbb3-1 terminal oxidases. Environ Microbiol 8:1764–1774CrossRefGoogle Scholar
  39. Moreno R, Hernández-Arranz S, La Rosa R, Yuste L, Madhushani A, Shingler V, Rojo F (2015) The Crc and Hfq proteins of Pseudomonas putida co-operate in catabolite repression and formation of ribonucleic acid complexes with specific target motifs. Environ Microbiol 17:105–118CrossRefGoogle Scholar
  40. Moreno R, Martínez-Gomariz M, Yuste L, Gil C, Rojo F (2009) The Pseudomonas putida Crc global regulator controls the hierarchical assimilation of amino acids in a complete medium: evidence from proteomic and genomic analyses. Proteomics 9:2910–2928CrossRefGoogle Scholar
  41. Moreno R, Fonseca P, Rojo F (2012) Two small RNAs, CrcY and CrcZ, act in concert to sequester the Crc global regulator in Pseudomonas putida, modulating catabolite repression. Mol Microbiol 83:24–40.  https://doi.org/10.1111/j.1365-2958.2011.07912.xCrossRefPubMedGoogle Scholar
  42. Moreno R, Ruiz-Manzano A, Yuste L, Rojo F (2007) The Pseudomonas putida Crc global regulator is an RNA binding protein that inhibits translation of the AlkS transcriptional regulator. Mol Microbiol 64:665–675CrossRefGoogle Scholar
  43. Nakamura H, Saiki K, Mogi T, Anraku Y (1997) Assignment and functional roles of the cyoABCDE gene products required for the Escherichia coli bo-type quinol oxidase. J Biochem 122:415–421CrossRefGoogle Scholar
  44. Nie Y, Liang J, Fang H, Tang YQ, XL W (2011) Two novel alkane hydroxylase-rubredoxin fusion genes isolated from a Dietzia bacterium and the functions of fused rubredoxin domains in long-chain n-alkane degradation. Appl Environ Microbiol 77:7279–7288CrossRefGoogle Scholar
  45. Nie Y, Liang JL, Fang H, Tang YQ, XL W (2014) Characterization of a CYP153 alkane hydroxylase gene in a gram-positive Dietzia sp. DQ12-45-1b and its "team role" with alkW1 in alkane degradation. Appl Microbiol Biotechnol 98:163–173CrossRefGoogle Scholar
  46. Panke S, Meyer A, Huber CM, Witholt B, Wubbolts MG (1999) An alkane-responsive expression system for the production of fine chemicals. Appl Environ Microbiol 65:2324–2332PubMedPubMedCentralGoogle Scholar
  47. Petruschka L, Burchhardt G, Müller C, Weihe C, Herrmann H (2001) The cyo operon of Pseudomonas putida is involved in catabolic repression of phenol degradation. Mol Gen Genom 266:199–206CrossRefGoogle Scholar
  48. Ramos-González MI, Molin S (1998) Cloning, sequencing, and phenotypic characterization of the rpoS gene from Pseudomonas putida KT2440. J Bacteriol 180:3421–3431PubMedPubMedCentralGoogle Scholar
  49. Pedrini N, Ortiz-Urquiza A, Huarte-Bonnet C, Zhang S, Keyhani NO (2013) Targeting of insect epicuticular lipids by the entomopathogenic fungus Beauveria bassiana: hydrocarbon oxidation within the context of a host-pathogen interaction. Front Microbiol 4:24CrossRefGoogle Scholar
  50. Post-Beitenmiller D (1996) Biochemistry and molecular biology of wax production in plants. Annu Rev Plant Physiol Plant Mol Biol 47:405–430CrossRefGoogle Scholar
  51. 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 180:5822–5827PubMedPubMedCentralGoogle Scholar
  52. Rojo F (2010) Carbon catabolite repression in Pseudomonas: optimizing metabolic versatility and interactions with the environment. FEMS Microbiol Rev 34:658–684CrossRefGoogle Scholar
  53. Ruiz-Manzano A, Yuste L, Rojo F (2005) Levels and activity of the Pseudomonas putida global regulatory protein Crc vary according to growth conditions. J Bacteriol 187:3678–3686CrossRefGoogle Scholar
  54. 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
  55. Schirmer A, Rude MA, Li X, Popova E, del Cardayre SB (2010) Microbial biosynthesis of alkanes. Science 329:559CrossRefGoogle Scholar
  56. 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 24:997–1004CrossRefGoogle Scholar
  57. Schreiber V, Richet E (1999) Self-association of the Escherichia coli transcription activator MalT in the presence of maltotriose and ATP. J Biol Chem 274:33220–33226CrossRefGoogle Scholar
  58. Sevilla E, Alvarez-Ortega C, Krell T, Rojo F (2013a) The Pseudomonas putida HskA hybrid sensor kinase responds to redox signals and contributes to the adaptation of the electron transport chain composition in response to oxygen availability. Environ Microbiol Rep 5:825–834CrossRefGoogle Scholar
  59. Sevilla E, Silva-Jiménez H, Duque E, Krell T, Rojo F (2013b) The Pseudomonas putida HskA hybrid sensor kinase controls the composition of the electron transport chain. Environ Microbiol Rep 5:291–300.  https://doi.org/10.1111/1758-2229.12017CrossRefPubMedGoogle Scholar
  60. Sevilla E, Yuste L, Rojo F (2015) Marine hydrocarbonoclastic bacteria as whole-cell biosensors for n-alkanes. Microb Biotechnol 8:693–706CrossRefGoogle Scholar
  61. Sluis MK, Sayavedra-Soto LA, Arp DJ (2002) Molecular analysis of the soluble butane monooxygenase from “Pseudomonas butanovora”. Microbiology 148:3617–3629CrossRefGoogle Scholar
  62. Smits TH, Balada SB, Witholt B, van Beilen JB (2002) Functional analysis of alkane hydroxylases from gram-negative and gram-positive bacteria. J Bacteriol 184:1733–1742CrossRefGoogle Scholar
  63. Sonnleitner E, Abdou L, Haas D (2009) Small RNA as global regulator of carbon catabolite repression in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 106:21866–21871CrossRefGoogle Scholar
  64. Sonnleitner E, Bläsi U (2014) Regulation of Hfq by the RNA CrcZ in Pseudomonas aeruginosa carbon catabolite repression. PLoS Genet 10:e1004440CrossRefGoogle Scholar
  65. Staijen IE, Marcionelli R, Witholt B (1999) The PalkBFGHJKL promoter is under carbon catabolite repression control in Pseudomonas oleovorans but not in Escherichia coli alk + recombinants. J Bacteriol 181:1610–1616PubMedPubMedCentralGoogle Scholar
  66. Sticher P, Jaspers MC, Stemmler K, Harms H, Zehnder AJ, der MJR v (1997) Development and characterization of a whole-cell bioluminescent sensor for bioavailable middle-chain alkanes in contaminated groundwater samples. Appl Environ Microbiol 63:4053–4060PubMedPubMedCentralGoogle Scholar
  67. 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
  68. Ugidos A, Morales G, Rial E, Williams HD, Rojo F (2008) The coordinate regulation of multiple terminal oxidases by the Pseudomonas putida ANR global regulator. Environ Microbiol 10:1690–1702CrossRefGoogle Scholar
  69. Valentini M, García-Mauriño SM, Pérez-Martínez I, Santero E, Canosa I, Lapouge K (2014) Hierarchical management of carbon sources is regulated similarly by the CbrA/B systems in Pseudomonas aeruginosa and Pseudomonas putida. Microbiology 160:2243–2252CrossRefGoogle Scholar
  70. van Beilen JB, Funhoff EG (2007) Alkane hydroxylases involved in microbial alkane degradation. Appl Microbiol Biotechnol 74:13–21CrossRefGoogle Scholar
  71. van Beilen JB, Marín 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 6:264–273CrossRefGoogle Scholar
  72. 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 147:1621–1630CrossRefGoogle Scholar
  73. van Beilen JB, Smits TH, Roos FF, Brunner T, Balada SB, Röthlisberger M, Witholt B (2005) Identification of an amino acid position that determines the substrate range of integral membrane alkane hydroxylases. J Bacteriol 187:85–91CrossRefGoogle Scholar
  74. van Beilen JB, Wubbolts MG, Witholt B (1994) Genetics of alkane oxidation by Pseudomonas oleovorans. Biodegradation 5:161–174CrossRefGoogle Scholar
  75. Venturi V (2003) Control of rpoS transcription in Escherichia coli and Pseudomonas: why so different? Mol Microbiol 49:1–9CrossRefGoogle Scholar
  76. Wang W, Shao Z (2012) Genes involved in alkane degradation in the Alcanivorax hongdengensis strain A-11-3. Appl Microbiol Biotechnol 94:437–448CrossRefGoogle Scholar
  77. Wang W, Shao Z (2014) The long-chain alkane metabolism network of Alcanivorax dieselolei. Nat Commun 5:5755CrossRefGoogle Scholar
  78. Williams HD, Zlosnik JE, Ryall B (2007) Oxygen, cyanide and energy generation in the cystic fibrosis pathogen Pseudomonas aeruginosa. Adv Microb Physiol 52:1–71PubMedGoogle Scholar
  79. Yakimov MM, Timmis KN, Golyshin PN (2007) Obligate oil-degrading marine bacteria. Curr Opin Biotechnol 18:257–266CrossRefGoogle Scholar
  80. Yuste L, Canosa I, Rojo F (1998) Carbon-source-dependent expression of the PalkB promoter from the Pseudomonas oleovorans alkane degradation pathway. J Bacteriol 180:5218–5226PubMedPubMedCentralGoogle Scholar
  81. Yuste L, Hervás AB, Canosa I, Tobes R, Jiménez JI, Nogales J, Pérez-Pérez MM, Santero E, Díaz E, Ramos JL, de Lorenzo V, Rojo F (2006) Growth-phase dependent expression of the Pseudomonas putida KT2440 transcriptional machinery analyzed with a genome-wide DNA microarray. Environ Microbiol 8:165–177CrossRefGoogle Scholar
  82. Yuste L, Rojo F (2001) Role of the crc gene in catabolic repression of the Pseudomonas putida GPo1 alkane degradation pathway. J Bacteriol 183:6197–6206CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Centro Nacional de Biotecnología, CSICMadridSpain

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