Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Molecular characteristics of xenobiotic-degrading sphingomonads

  • 1084 Accesses

  • 132 Citations


The genus Sphingomonas (sensu latu) belongs to the α-Proteobacteria and comprises strictly aerobic chemoheterotrophic bacteria that are widespread in various aquatic and terrestrial environments. The members of this genus are often isolated and studied because of their ability to degrade recalcitrant natural and anthropogenic compounds, such as (substituted) biphenyl(s) and naphthalene(s), fluorene, (substituted) phenanthrene(s), pyrene, (chlorinated) diphenylether(s), (chlorinated) furan(s), (chlorinated) dibenzo-p-dioxin(s), carbazole, estradiol, polyethylene glycols, chlorinated phenols, nonylphenols, and different herbicides and pesticides. The metabolic versatility of these organisms suggests that they have evolved mechanisms to adapt quicker and/or more efficiently to the degradation of novel compounds in the environment than members of other bacterial genera. Comparative analyses demonstrate that sphingomonads generally use similar degradative pathways as other groups of microorganisms but deviate from competing microorganisms by the existence of multiple hydroxylating oxygenases and the conservation of specific gene clusters. Furthermore, there is increasing evidence for the existence of plasmids that only can be disseminated among sphingomonads and which undergo after conjugative transfer pronounced rearrangements.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4


  1. Amato P, Parazols M, Sancelme M, Laj P, Mailhot G, Delort A-M (2007) Microorganisms isolated from the water phase of tropospheric clouds at the Puy de Dôme: major groups and growth abilities at low temperatures. FEMS Microbiol Ecol 59:242–254

  2. Armengaud J, Happe B, Timmis KN (1998) Genetic analysis of dioxin dioxygenase of Sphingomonas sp. RW1: catabolic genes dispersed on the genome. J Bacteriol 180:3954–3966

  3. Aso Y, Miyamoto Y, Harada KM, Momma K, Kawai S, Hashimoto W, Mikami B, Murata K (2006) Engineered membrane superchannel improves bioremediation potential of dioxin-degrading bacteria. Nat Biotechnol 24:188–189

  4. Balkwill DL, Drake GR, Reeves RH, Fredrickson JK, White DC, Ringelberg DB, Chandler DP, Romine MF, Kennedy DW, Spadoni CW (1997) Taxonomic study of aromatic-degrading bacteria from deep-terrestrial-subsurface sediments and description of Sphingomonas aromaticivorans sp. nov., Sphingomonas subterranea sp. nov., and Sphingomonas stygia sp. nov. Int J Syst Bacteriol 47:191–201

  5. Baraniecki CA, Aislabie J, Foght JM (2002) Characterization of Sphingomonas sp. Ant 17, an aromatic hydrocarbon-degrading bacterium isolated from Antarctic soil. Microb Ecol 43:44–54

  6. Basta T, Keck A, Klein J, Stolz A (2004) Detection and characterization of conjugative degradative plasmids in xenobiotics degrading Sphingomonas strains. J Bacteriol 186:3862–3872

  7. Basta T, Bürger S, Stolz A (2005) Structural and replicative diversity of large plasmids from polycyclic aromatic compounds and xenobiotics degrading Sphingomonas strains. Microbiology 151:2025–2037

  8. Bending GD, Lincoln SD, Sørensen SR, Morgan JA, Aamand J, Walker A (2003) In-field spatial variability in the degradation of the phenyl-urea herbicide isoproturon is the result of interaction between degradative Sphingomonas spp. and soil pH. Appl Environ Microbiol 69:827–834

  9. Boersma FG, McRoberts WC, Cobb SL, Murphy CD (2004) A 19F NMR study of fluorobenzoate biodegradation by Sphingomonas sp. HB-1. FEMS Microbiol Lett 237:355–361

  10. Bramucci M, Singh M, Nagarajan V (2002) Biotransformation of p-xylene and 2,6-dimethylnaphthalene by xylene monooxygenase cloned from a Sphingomonas isolate. Appl Microbiol Biotechnol 59:679–684

  11. Briglia M, Eggen RI, van Elsas DJ, de Vos WM (1994) Phylogenetic evidence for transfer of pentachlorophenol-mineralizing Rhodococcus chlorophenolicus PCP-I(T) to the genus Mycobacterium. Int J Syst Bacteriol 44:494–498

  12. Cai M, Xun L (2002) Organization and regulation of pentachlorophenol-degrading genes in Sphingobium chlorophenolicum ATCC 39723. J Bacteriol 184:4672–4680

  13. Cérémonie H, Boubakri H, Mavingui P, Simonet P, Vogel TM (2006) Plasmid-encoded γ-hexachlorocyclohexane degradation genes and insertion sequences in Sphingobium francense (ex-Sphingomonas paucimobilis Sp+). FEMS Microbiol Lett 257:243–252

  14. Chadhain SM, Moritz EM, Kim E, Zylstra GJ (2007) Identification, cloning, and characterization of a multicomponent dioxygenase from Sphingobium yanoikuyae B1. J Ind Microbiol Biotechnol 34:605–613

  15. Charity RM, Foukas AF (2005) Osteomyelitis and secondary septic arthritis caused by Sphingomonas paucimobilis. Infection 33:93–95

  16. Chen K, Hu H, Wang W, Zhang X, Xu Y (2008) Metabolic degradation of phenazine-1-carboxylic acid by the strain Sphingomonas sp. DP58: the identification of two metabolites. Biodegradation 19:659–667

  17. Cho J-C, Kim S-J (2001) Detection of mega plasmid from polycyclic aromatic hydrocarbon-degrading Sphingomonas sp. strain KS14. J Mol Microbiol Biotechnol 3:503–506

  18. Cho O, Choi KY, Zylstra GJ, Kim Y-S, Kim S-K, Lee JH, Sohn H-Y, Kwon G-S, Kim YM, Kim E (2005) Catabolic role of a three-component salicylate oxygenase from Sphingomonas yanoikuyae B1 in polycyclic aromatic hydrocarbon degradation. Biochem Biophys Res Comm 327:656–662

  19. Christner BC, Mosley-Thompson E, Thompson LG, Reeve JN (2001) Isolation of bacteria and 16S rDNAs from Lake Vostok accretion ice. Environ Microbiol 3:570–577

  20. Corvini PF, Hollender J, Ji R, Schumacher S, Prell J, Hommes G, Priefer U, Vinken R, Schäffer A (2006a) The degradation of α-quaternary nonylphenol isomers by Sphingomonas sp. strain TTNP3 involves a type II ipso-substitution mechanism. Appl Microbiol Biotechnol 70:114–122

  21. Corvini PF, Schäffer A, Schlosser D (2006b) Microbial degradation of nonylphenol and other alkylphenols—our evolving view. Appl Microbiol Biotechnol 72:223–243

  22. Contzen M, Moore ER, Blümel S, Stolz A, Kämpfer P (2000) Hydrogenophaga intermedia sp. nov., a 4-aminobenzenesulfonate degrading organism. Syst Appl Microbiol 23:487–493

  23. Coughlin MF, Kinkle BK, Bishop PL (1999) Degradation of azo dyes containing aminonaphthol by Sphingomonas sp. strain 1CX. J Ind Microbiol Biotechnol 23:341–346

  24. Crawford RL, Jung CM, Strap JL (2007) The recent evolution of pentachlorophenol (PCP)-4-monooxygenase (PcpB) and associated pathways for bacterial degradation of PCP. Biodegradation 18:525–539

  25. Cunliffe M, Kertesz MA (2006) Autecological properties of soil sphingomonads involved in the degradation of polycyclic aromatic hydrocarbons. Appl Microbiol Biotechnol 72:1083–1089

  26. Demanèche S, Meyer C, Micoud J, Louwagie M, Willison JC, Jouanneau Y (2004) Identification and functional analysis of two aromatic-ring-hydroxylating dioxygenases from a Sphingomonas strain that degrades various polycyclic aromatic hydrocarbons. Appl Environ Microbiol 70:6714–6725

  27. Dogra CV, Raina V, Pal R, Suar M, Lal S, Gartemann H-H, Holliger C, van der Meer JR, Lal R (2004) Organization of lin genes and IS6100 among different species of hexachlorocyclohexane-degrading Sphingomonas paucimobilis: evidence for horizontal gene transfer. J Bacteriol 186:2225–2235

  28. Don RH, Weightman AJ, Knackmuss H-J, Timmis KN (1985) Transposon mutagenesis and cloning analysis of the pathway for the degradation of 2,4-dichlorophenoxyacetic acid and 3-chlorobenzoate in Alcaligenes eutrophus JMP134(pJP4). J Bacteriol 161:85–96

  29. Dutta TK, Selifonov SA, Gunsalus IC (1998) Oxidation of methyl-substituted naphthalenes: pathways in a versatile Sphingomonas paucimobilis strain. Appl Environ Microbiol 64:1884–1889

  30. Ederer MM, Crawford RL, Herwig RP, Orser CS (1997) PCP degradation is mediated by closely related strains of the genus Sphingomonas. Mol Ecol 6:39–49

  31. Eguchi M, Nishikawa T, McDonald K, Cavicchioli R, Gottschal JC, Kjelleberg S (1996) Response to stress and nutrient availability by the marine ultramicrobacterium Sphingomonas sp. strain RB2256. Appl Environ Microbiol 62:1287–1294

  32. Eguchi M, Ostrowski M, Fegatella F, Bowman J, Nichols D, Nishino T, Cavicchioli R (2001) Sphingomonas alaskensis strain AFO1, an abundant oligotrophic ultramicrobacterium from the North Pacific. Appl Environ Microbiol 67:4945–4954

  33. Feng X, Ou L-T, Ogram A (1997a) Plasmid-mediated mineralization of carbofuran by Sphingomonas sp. CF-06. Appl Environ Microbiol 63:1332–1337

  34. Feng X, Ou L-T, Ogram A (1997b) Cloning and sequence analysis of a novel insertion element from plasmids harbored by the carbofuran-degrading bacterium, Sphingomonas sp. CF-06. Plasmid 37:169–179

  35. Fredrickson JK, Balkwill DL, Drake GR, Romine MF, Ringelberg DB, White DC (1995) Aromatic-degrading Sphingomonas isolates from the deep surface. Appl Environ Microbiol 61:1917–1922

  36. Fukuda K, Nagata S, Taniguchi H (2002) Isolation and characterization of dibenzofuran-degrading bacteria. FEMS Microbiol Lett 208:179–185

  37. Fujii K, Urano N, Ushio H, Satomi M, Kimura S (2001) Sphingomonas cloacae sp. nov., a nonylphenol-degrading bacterium isolated from wastewater of a sewage-treatment plant in Tokyo. Int J Syst Evol Microbiol 51:603–610

  38. Fujii K, Satomi M, Morita N, Motomura T, Tanaka T, Kikuchi S (2003a) Novosphingobium tardaugens sp. nov., an oestradiol-degrading bacterium isolated from activated sludge of a sewage treatment plant in Tokyo. Int J Syst Evol Microbiol 53:47–52

  39. Fujii K, Yamamoto R, Tanaka T, Hirakawa T, Kikuchi S (2003b) Potential of biotreatment: Sphingomonas cloacae S-3T degrades nonylphenol in industrial wastewater. J Ind Microbiol Biotechnol 30:531–535

  40. Fulthorpe RR, McGowan C, Maltseva OV, Holben WE, Tiedje JM (1995) 2,4-dichlorophenoxyacetic acid-degrading bacteria contain mosaic of catabolic genes. Appl Environ Microbiol 61:3274–3281

  41. Furukawa K, Simon JR, Chakrabarty AM (1983) Common induction and regulation of biphenyl, xylene/toluene, and salicylate catabolism in Pseudomonas paucimobilis. J Bacteriol 154:1356–1362

  42. Furukawa K, Hayase N, Taira K, Tomizuka N (1989) Molecular relationship of chromosomal genes encoding biphenyl/polychlorinated biphenyl catabolism: some soil bacteria possess highly conserved bph operons. J Bacteriol 171:5467–5472

  43. Gabriel FL, Giger W, Guenther K, Kohler H-P (2005) Differential degradation of nonylphenol isomers by Sphingomonas xenophaga Bayram. Appl Environ Microbiol 71:1123–1129

  44. Gerischer U (2002) Specific and global regulation of genes associated with the degradation of aromatic compounds in bacteria. J Mol Microbiol Biotechnol 4:111–121

  45. Gibson DT, Roberts RL, Wells MC, Kobal VM (1973) Oxidation of biphenyl by a Beijerinckia species. Biochem Biophys Res Comm 50:211–219

  46. Gomila M, Gascó J, Busquets A, Gil J, Barnabeu R, Buades JM, Lalucat J (2005) Identification of culturable bacteria present in haemodialysis water and fluid. FEMS Microbiol Ecol 52:101–114

  47. Habe H, Omori T (2003) Genetics of polycyclic aromatic hydrocarbon metabolism in diverse aerobic bacteria. Biosci Biotechnol Biochem 67:225–243

  48. Habe H, Ashikawa Y, Saiki Y, Yoshida T, Nojiri H, Omori T (2002) Sphingomonas sp. strain KA1, carrying a carbazole dioxygenase gene homologue, degrades chlorinated dibenzo-p-dioxins in soil. FEMS Microbiol Lett 211:43–49

  49. Hara H, Masai E, Miyauchi K, Katayama Y, Fukuda M (2003) Characterization of the 4-carboxy-4-hydroxy-2-oxoadipate aldolase gene and operon structure of the protocatechuate 4,5-cleavage pathway genes in Sphingomonas paucimobilis SYK-6. J Bacteriol 185:41–50

  50. Harayama S (1997) Polycyclic aromatic hydrocarbon bioremediation design. Curr Opin Biotechnol 8:268–273

  51. Harms H, Wilkes H, Wittich R-M, Fortnagel P (1995) Metabolism of hydroxy dibenzofurans, methoxy benzofurans, acetoxy dibenzofurans, and nitro dibenzofurans by Sphingomonas sp. HH69. Appl Environ Microbiol 61:2499–2505

  52. Hashidoko Y, Kitagawa E, Iwahashi H, Purnomo E, Hasegawa T, Tahara S (2007) Design of sphingomonad-detecting probes for a DNA array, and its application to investigate the behaviour, distribution, and source of rhizospherous Sphingomonas and other sphingomonads inhabiting an acid sulfate soil paddock in Kalimantan, Indonesia. Biosci Biotechnol Biochem 71:345–351

  53. Hashimoto W, Momma K, Maruyama Y, Yamasaki M, Mikami B, Murata K (2005) Structure and function of bacterial super-biosystem responsible for import and depolymerization of macromolecules. Biosci Biotechnol Biochem 69:673–692

  54. Haug W, Schmidt A, Nörtemann B, Hempel DC, Stolz A, Knackmuss H-J (1991) Mineralization of the sulfonated azo dye Mordant Yellow 3 by a 6-aminonaphthalene-2-sulfonate degrading bacterial consortium. Appl Environ Microbiol 57:3144–3149

  55. He Z, Parales RE, Spain JC, Johnson GR (2007) Novel organization of catechol meta pathway genes in the nitrobenzene degrader Comamonas sp. JS765 and its evolutionary implication. J Ind Microbiol Biotechnol 34:99–104

  56. Hernáez MJ, Reineke W, Santero E (1999) Genetic analysis of biodegradation of tetralin by Sphingomonas strain. Appl Environ Microbiol 65:1806–1810

  57. Hong HB, Chang YS, Nam IH, Fortnagel P, Schmidt S (2002) Biotransformation of 2,7-dichloro-and 1,2,3,4-tetrachlorodibenzo-p-dioxin by Sphingomonas wittichii RW1. Appl Environ Microbiol 68:2584–2588

  58. Hong HB, Nam ICH, Murugesan K, Kim YM, Chang YS (2004) Biodegradation of dibenzo-p-dioxins by Pseudomonas veronii PH-03. Biodegradation 15:303–313

  59. Hu X, Mamoto R, Jujioka Y, Tani A, Kimbara K, Kawai F (2008) The pva operon is located on the megaplasmid of Sphingopyxis sp. strain 113P and is constitutively expressed, although expression is enhanced by PVA. Appl Microbiol Biotechnol 78:685–693

  60. Huong NL, Itoh K, Miyamato M, Suyama K, Yamamoto H (2007) Chlorophenol hydroxylase activity encoded by TfdB from 2,4-dichlorophenoxyacetic acid (2,4-D)-degrading Bradyrhizobium sp. strain RD5-C2. Biosci Biotechnol Biochem 71:1691–1696

  61. Iida T, Nakamura K, Izumi A, Mukouzaka Y, Kudo T (2006) Isolation and characterization of a gene cluster for dibenzofuran degradation in a new dibenzofuran-utilizing bacterium, Paenibacillus sp. strain YK5. Arch Microbiol 184:305–315

  62. Inoue K, Habe H, Yamane H, Omori T, Nojiri H (2005) Diversity of carbazole-degrading bacteria having the car gene cluster: isolation of a novel Gram-positive carbazole-degrading bacterium. FEMS Microbiol Lett 245:145–153

  63. Jakoncic J, Jouanneau Y, Meyer C, Stojanoff V (2007) The crystal structure of the ring-hydroxylating dioxygenase from Sphingomonas CHY-1. FEBS J 274:2479–2481

  64. Johnsen AR, Karlson U (2004) Evaluation of bacterial strategies to promote the bioavailability of polycyclic aromatic hydrocarbons. Appl Microbiol Biotechnol 63:452–459

  65. Jouanneau Y, Meyer C (2006) Purification and characterization of an arene cis-dihydrodiol dehydrogenase endowed with broad substrate specificity toward polycyclic aromatic hydrocarbon dihydrodiols. Appl Environ Microbiol 72:4726–4734

  66. Jouanneau Y, Micoud J, Meyer C (2007) Purification and characterization of an a three-component salicylate 1-hydroxylase from Sphingomonas sp. strain CHY-1. Appl Environ Microbiol 73:7515–7521

  67. Kamoda S, Saburi Y (1993) Structural and enzymatical comparison of lignostilbene-α,β-lignostilbene-dioxygenase isoenzymes, I, II, and III from Pseudomonas paucimobilis TMY1009. Biosci Biotech Biochem 57:931–934

  68. Kamoda S, Terada T, Saburi Y (2003) A common structure shared by lignostilbene dioxygenase isoenzymes from Sphingomonas paucimobilis TMY1009. Biosci Biotech Biochem 67:1394–1396

  69. Kaneko A, Miyadai H, Danbara H, Kawahara K (2000) Construction of mutants of Sphingomonas paucimobilis defective in terminal mannose in the glycosphingolipid. Biosci Biotechnol Biochem 64:1298–1301

  70. Karlson U, Rojo F, van Elsas JD, Moore E (1995) Genetic and serological evidence for the recognition of four pentachlorophenol-degrading bacterial strains as a species of the genus Sphingomonas. Syst Appl Microbiol 18:539–548

  71. Kawahara K, Kuraishi H, Zähringer U (1999) Chemical structure and function of glycosphingolipids of Sphingomonas spp and their distribution among members of the α-4 subclass of Proteobacteria. J Ind Microbiol Biotechnol 23:408–413

  72. Kawai F (1999) Sphingomonads involved in the biodegradation of xenobiotic polymers. J Ind Microbiol Biotechnol 23:400–407

  73. Keck A, Klein J, Kudlich M, Stolz A, Knackmuss H-J, Mattes R (1997) Reduction of azo dyes by redox mediators originating in the naphthalene sulfonic acid degradation pathway of Sphingomonas sp. strain BN6. Appl Environ Microbiol 63:3684–3690

  74. Keck A, Rau J, Reemstma T, Mattes R, Stolz A, Klein J (2002) Identification of quinoide redox mediators that are formed during the degradation of naphthalene-2-sulfonate by Sphingomonas xenophaga BN6. Appl Environ Microbiol 68:4341–4349

  75. Keck A, Conradt D, Mahler A, Stolz A, Mattes R, Klein J (2006) Identification and functional analysis of the genes for the naphthalene sulfonate catabolism by Sphingomonas xenophaga BN6. Microbiology 152:1929–1940

  76. Kelley ST, Theisen U, Angenent LT, Amand AS, Pace NR (2004) Molecular analysis of shower curtain biofilm microbes. Appl Environ Microbiol 70:4187–4192

  77. Khan AA, Wang R-F, Cao W-W, Franklin W, Franklin CE (1996) Reclassification of a polycyclic aromatic hydrocarbon-metabolizing bacterium, Beijerinckia sp. strain B1, as Sphingomonas yanoikuyae by fatty acid analysis, protein pattern analysis, DNA–DNA hybridization, and 16S ribosomal DNA sequencing. Int J Syst Bacteriol 46:466–469

  78. Kilbane JJ II, Daram A, Abbasian J, Kayser KJ (2002) Isolation and characterization of Sphingomonas sp. GTIN11 capable of carbazole metabolism in petroleum. Biochem Biophys Res Comm 297:242–248

  79. Kilic A, Senses Z, Kurekci E, Aydogan H, Sener K, Kismet E, Basustaoglu AC (2007) Nosocomial outbreak of Sphingomonas paucimobilis bacteremia in a hemato/oncology unit. Jpn J Infect Dis 60:394–396

  80. Kim E, Zylstra GJ (1995) Molecular and biochemical characterization of two meta-cleavage dioxygenases involved in biphenyl and m-xylene degradation by Beijerinckia sp. strain B1. J Bacteriol 177:3095–3103

  81. Kim E, Zylstra GJ (1999) Functional analysis of genes involved in biphenyl, naphthalene, phenanthrene, and m-xylene degradation by Sphingomonas yanoikuyae B1. J Ind Microbiol Biotechnol 23:294–302

  82. Kim E, Aversano PJ, Romine MF, Schneider RP, Zylstra GJ (1996) Homology between genes for aromatic hydrocarbon degradation in surface and deep-subsurface Sphingomonas strains. Appl Environ Microbiol 62:1467–1470

  83. Kim H, Nishiyama M, Kunito T, Senoo K, Kawahara K, Murakami K, Oyaizu H (1998) High population of Sphingomonas species on plant surface. J Appl Microbiol 85:731–736

  84. Kim S-J, Chun J, Bae KS, Kim Y-C (2000) Polyphasic assignment of an aromatic-degrading Pseudomonas sp., strain DJ77, in the genus Sphingomonas as Sphingomonas chungbukensis sp. nov. Int J Syst Evol Microbiol 50:1641–1647

  85. Kim IS, Ryu JY, Hur HG, Gu MB, Kim SD, Shim JM (2004) Sphingomonas sp. strain SB5 degrades carbofuran to a new metabolite by hydrolysis of the furanyl ring. J Agric Food Chem 52:2309–2314

  86. Kirimura K, Nakagawa H, Tsuji K, Matsuda K, Kurane R, Usami S (1999) Selective and continuous degradation of carbazole in petroleum oil by resting cells of Sphingomonas sp. CDH-7. Biosci Biotechnol Biochem 63:1563–1568

  87. Koskinen R, Ali-Vehmas T, Kämpfer P, Laurikkala M, Tsitko I, Kostyal E, Atroshi F, Salkinoja-Salkonen M (2000) Characterization of Sphingomonas isolates from Finnish and Swedish drinking water distribution systems. J Appl Microbiol 89:687–696

  88. Kouzuma A, Pinyakong O, Nojiri H, Omori T, Yamane H, Habe H (2006) Functional and transcriptional analysis of the initial oxygenase genes for acenaphthene degradation from Sphingomonas sp. strain A4. Microbiology 152:2455–2467

  89. Kudlich M, Keck A, Klein J, Stolz A (1997) Localization of the enzyme system involved in the anaerobic reduction of azo dyes by Sphingomonas sp. BN6 and effect of artificial redox mediators on the rate of azo dye reduction. Appl Environ Microbiol 63:3691–3694

  90. Kuhm AE, Stolz A, Ngai K-L, Knackmuss H-J (1991a) Purification and characterization of a 1,2-dihydroxynaphthalene dioxygenase from a bacterium that degrades naphthalene sulfonic acids. J Bacteriol 173:3795–3802

  91. Kuhm AE, Stolz A, Knackmuss H-J (1991b) Metabolism of naphthalene by the biphenyl degrading bacterium Pseudomonas paucimobilis Q1. Biodegradation 2:115–120

  92. Kuhm AE, Knackmuss H-J, Stolz A (1993a) Purification and properties of 2′-hydroxybenzalpyruvate aldolase from a bacterium that degrades naphthalene sulfonates. J Biol Chem 268:9484–9489

  93. Kuhm AE, Knackmuss H-J, Stolz A (1993b) 2-Hydroxychromene-2-carboxylate isomerase from bacteria that degrade naphthalene sulfonates. Biodegradation 4:155–162

  94. Kumari R, Subudhi S, Suar M, Dhingra G, Raina V, Dogra C, Lal S, van der Meer JR, Holliger C, Lal R (2002) Cloning and characterization of lin genes responsible for the degradation of hexachlorocyclohexane isomers by Sphingomonas paucimobilis strain B90. Appl Environ Microbiol 68:6021–6028

  95. Lang E, Kroppenstedt RM, Swiderski J, Schumann P, Ludwig W, Schmid A, Weiss N (2003) Emended description of Janibacter terrae, including ten dibenzofuran-degrading strains and Janibacter brevis as its later heterotypic synonym. Int J Syst Evol Microbiol 53:1999–2005

  96. Li X, He J, Li S (2007) Isolation of a chlorpyrifos-degrading bacterium, Sphingomonas sp. strain Dsp-2, and cloning of the mpd gene. Res Microbiol 158:143–149

  97. Lim J-S, Jung M-K, Kim M-S, Ahn J-H, Ka J-O (2004) Genetic and phenotypic diversity of (R/S)-mecoprop [2-(2-methyl-4-chlorophenoxy)propionic acid]-degrading bacteria isolated from soils. J Microbiol 42:87–93

  98. Liu Y, Zhang J, Zhang Z (2004) Isolation and characterization of polycyclic aromatic hydrocarbons-degrading Sphingomonas sp. strain ZL5. Biodegradation 15:205–212

  99. Magony M, Kákonyi I, Gara A, Rapali P, Perei K, Kovács KL, Rákhely G (2007) Overlaps between the various biodegradation pathways in Sphingomonas subarctica SA1. Acta Biol Hungarica (Suppl) 58:37–49

  100. Manickam N, Mau M, Schlömann M (2006) Characterization of the novel HCH-degrading strain, Microbacterium sp. ITRC1. Appl Microbiol Biotechnol 69:580–588

  101. Manickam N, Misra R, Mayilraj S (2007) A novel pathway for the biodegradation of gamma-hexachlorocyclohexane by a Xanthomonas sp. strain ICH12. J Appl Microbiol 102:1468–1478

  102. Männistö MK, Tiirola MA, Salkinoja-Salonen MS, Kulomas MS, Puhakka JA (1999) Diversity of chlorophenol-degrading bacteria isolated from contaminated boreal groundwater. Arch Microbiol 171:189–197

  103. Martinez-Pérez O, Moreno-Ruiz E, Floriano B, Santero E (2004) Regulation of tetralin biodegradation and identification of genes essential for expression of thn operons. J Bacteriol 186:6101–6109

  104. Maruyama K, Shibayama T, Ichikawa A, Sakou Y, Yamada S, Sugisaki H (2004) Cloning and characterization of the genes encoding enzymes for the protocatechuate meta-degradation pathway of Pseudomonas ochracea NGJ1. Biosci Biotechnol Biochem 68:1434–1441

  105. Maruyama T, Park H-D, Ozawa K, Tanaka Y, Sumino T, Hamana K, Hiraishi A, Kato K (2006) Sphingosinicella microcystinivorans gen. nov., sp. nov., a microcystin-degrading bacterium. Int J Syst Evol Microbiol 56:85–89

  106. Masai E, Katayama Y, Fukuda M (2007) Genetic and biochemical investigations on bacterial catabolic pathways for lignin-derived aromatic compounds. Biosci Biotechnol Biochem 71:1–15

  107. Miethling R, Karlson U (1996) Accelerated mineralization of pentachlorophenol in soil upon inoculation with Mycobacterium chlorophenolicum PCP1 and Sphingomonas chlorophenolica RA2. Appl Environ Microbiol 62:4361–4366

  108. Miyauchi K, Lee H-S, Fukuda M, Takagi M, Nagata Y (2002) Cloning and characterization of linR involved in regulation of the downstream pathway for γ-hexachlorocyclohexane degradation in Sphingomonas paucimobilis UT26. Appl Environ Microbiol 68:1803–1807

  109. Mueller JG, Devereux R, Santavy DL, Lantz SE, Willis SG, Pritchard PH (1997) Phylogenetic and physiological comparison of PAH-degrading bacteria from geographically diverse soils. Antonie van Leeuwenhoek 71:329–343

  110. Müller TA, Byrde SM, Werlen C, van der Meer JR, Kohler H-PE (2004) Genetic analysis of phenoxyalkanoic acid degradation in Sphingomonas herbicidovorans MH. Appl Environ Microbiol 70:6066–6075

  111. Nagata Y, Miyauchi M, Takagi M (1999) Complete analysis of genes and enzymes for γ-hexachlorocyclohexane degradation in Sphingomonas paucimobilis UT26. J Ind Microbiol 23:380–390

  112. Nagata Y, Kamakura M, Endo R, Miyazaki R, Ohtsubo Y, Tsuda M (2006) Distribution of γ-hexachlorocyclohexane-degrading genes on three replicons in Sphingobium japonicum UT26. FEMS Microbiol Lett 256:112–118

  113. Nagata Y, Endo R, Ito M, Ohtsubo Y, Tsuda M (2007) Aerobic degradation of lindane (γ-hexachlorocyclohexane) in bacteria and its biochemical and molecular basis. Appl Microbiol Biotechnol 76:741–752

  114. Nam I-H, Kim Y-M, Schmidt S, Chang Y-S (2006) Biotransformation of 1,2,3-tri- and 1,2,3,4,7,8-hexachlorodibenzo-p-dioxin by Sphingomonas wittichii strain RW1. Appl Environ Microbiol 72:112–116

  115. Nohynek LJ, Suhonen EL, Nurmiaho-Lassila E-L, Hantula J, Salkinoja-Salonen M (1995) Description of four pentachlorophenol-degrading bacterial strains as Sphingomonas chlorophenolica sp. nov. Syst Appl Microbiol 18:527–538

  116. Nohynek LJ, Nurmiaho-Lassila E-L, Suhonen EL, Busse H-J, Mohammadi M, Hantula J, Rainey F, Salkinoja-Salonen M (1996) Description of chlorophenol-degrading Pseudomonas sp. strains KF1, KF3, and NKF1 as a new species of the genus Sphingomonas, Sphingomonas subarctica sp. nov. Int J Syst Bacteriol 46:1042–1055

  117. Nojiri H, Omori T (2002) Molecular basis of aerobic degradation of dioxins: involvement of angular dioxygenation. Biosci Biotechnol Biochem 66:2001–2016

  118. Nörtemann B, Baumgarten J, Rast HG, Knackmuss H-J (1986) Bacterial communities degrading amino- and hydroxynaphthalene sulfonates. Appl Environ Microbiol 52:1195–1202

  119. Novikova N, De Boever P, Poddubko S, Deshevaya E, Polikarpov N, Rakova N, Coninx I, Mergeay M (2006) Survey of environmental biocontamination on board of the International Space Station. Res Microbiol 157:5–12

  120. Ogram AV, Duan Y-P, Trabue SL, Feng X, Castro H, Ou L-T (2000) Carbofuran degradation mediated by three related plasmid systems. FEMS Microbiol Ecol 32:197–203

  121. Orser CS, Lange CC (1994) Molecular analysis of pentachlorophenol degradation. Biodegradation 5:277–288

  122. Oshiman K, Tsutsumi Y, Nishida T, Matsumara Y (2007) Isolation and characterization of a novel bacterium, Sphingomonas bisphenolicum AO1, that degrades bisphenol A. Biodegradation 18:247–253

  123. Ostrowski M, Caviccioli R, Blaauw M, Gottschal JC (2001) Specific growth rate plays a critical role in hydrogen peroxide resistance of the marine oligotrophic ultramicrobacterium Sphingomonas alaskensis strain RB2256. Appl Environ Microbiol 67:1292–1299

  124. Pal R, Bala S, Dadhwal M, Kumar M, Dhingra G, Prakash O, Prabagaran SR, Shivaji S, Cullum J, Holliger C, Lal R (2005) Hexachlorocyclohexane-degrading bacterial strains Sphingomonas paucimobilis B90A, UT26 and Sp+, having similar lin genes, represent three distinct species, Sphingobium indicum sp. nov., Sphingobium japonicum sp. nov. and Sphingobium francense sp. nov., and reclassification of [Sphingomonas] chungbukensis as Sphingobium chungbukensis comb. nov. Int J Syst Evol Microbiol 55:1965–1972

  125. Pal R, Bhasin VK, Lal R (2006) Proposal to reclassify [Sphingomonas] xenophaga Stolz et al. 2000 and [Sphingomonas] taejonensis Lee et al. 2001 as Sphingobium xenophagum comb. nov. and Sphingopyxis taejonensis comb. nov., respectively. Int J Syst Evol Microbiol 55:667–670

  126. Perei K, Rákhely G, Kiss I, Polyák B, Kovács KL (2001) Biodegradation of sulfanilic acid by Pseudomonas paucimobilis. Appl Microbiol Biotechnol 55:101–107

  127. Pfaller SL, Sutton SD, Kinkle BK (1999) Sphingomonas sp. strain Lep1: an aerobic degrader of 4-methylquinoline. Can J Microbiol 45:623–626

  128. Pieper DH (2005) Aerobic degradation of polychlorinated biphenyls. Appl Microbiol Biotechnol 67:170–191

  129. Pinyakong O, Habe H, Supaka N, Pinpanichkarn P, Juntongjin K, Yoshida T, Furihata K, Nojiri H, Yamane H, Omori T (2000) Identification of novel metabolites in the degradation of phenanthrene by Sphingomonas sp. Strain P2. FEMS Microbiol Lett 191:115–121

  130. Pinyakong O, Habe H, Omori T (2003a) The unique aromatic catabolic genes in sphingomonads degrading polycyclic aromatic hydrocarbons (PAHs). J Gen Appl Microbiol 49:1–9

  131. Pinyakong O, Habe H, Yoshida T, Nojiri H, Omori T (2003b) Identification of three novel salicylate 1-hydroxylases involved in the phenanthrene degradation of Sphingobium sp. strain P2. Biochem Biophys Res Comm 301:350–357

  132. Pinyakong O, Habe H, Kouzuma A, Nojiri H, Yamane H, Omori T (2004) Isolation and characterization of genes encoding polycyclic aromatic hydrocarbon dioxygenase from acenaphthene and acenaphthylene degrading Sphingomonas sp. strain A4. FEMS Microbiol Lett 238:297–305

  133. Porter AW, Hay AG (2007) Identification of opdA, a gene involved in biodegradation of the endocrine disrupter octylphenol. Appl Environ Microbiol 73:7373–7379

  134. Qu Y, Zhou J, Wang J, Song Z, Xing L, Fu X (2006) Bioaugmentation of bromoamine acid degradation with Sphingomonas xenophaga QYY and DNA fingerprint analysis of augmented systems. Biodegradation 17:83–91

  135. Reddy GSN, Garcia-Pichel F (2007) Sphingomonas mucosissima sp. nov. and Sphingomonas desiccabilis sp. nov., from biological soil crusts in the Colorado Plateau, USA. Int J Syst Evol Microbiol 57:1028–1054

  136. Romine MF, Stillwell LC, Wong K-K, Thurston SJ, Sisk EC, Sensen C, Gaasterland T, Fredrickson JK, Saffer JD (1999a) Complete sequence of a 184-kilobase catabolic plasmid from Sphingomonas aromaticivorans F199. J Bacteriol 181:1585–1602

  137. Romine MF, Fredrickson JK, Li S-MW (1999b) Induction of aromatic catabolic activity in Sphingomonas aromaticivorans F199. J Ind Microbiol Biotechnol 23:303–313

  138. Sabaté J, Grifoll M, Viñas M, Solanas AM (1999) Isolation and characterization of a 2-methylphenanthrene utilizing bacterium: identification of ring cleavage metabolites. Appl Microbiol Biotechnol 52:704–712

  139. Sabaté J, Viñas M, Bayona JM, Solanas AM (2003) Isolation and taxonomic and catabolic characterization of a 3,6-dimethylphenanthrene-utilizing strain of Sphingomonas sp. Can J Microbiol 49:120–129

  140. Sakai K, Yamanaka H, Moriyoshi K, Ohmoto T, Ohe T (2007) Biodegradation of bisphenol A and related compounds by Sphingomonas sp. strain BP-7 isolated from seawater. Biosci Biotechnol Biochem 71:51–57

  141. Sánchez MA, González B (2007) Genetic characterization of 2,4.6-trichlorophenol degradation in Cupriavidus necator JMP134. Appl Environ Microbiol 73:2769–2776

  142. Sasaki M, Maki J, Oshiman K, Matsumara Y, Tsuchido T (2005) Biodegradation of bisphenol A by cells and cell lysate from Sphingomonas sp. strain AO1. Biodegradation 16:449–459

  143. Schleheck D, Cook AM (2003) Saccharin as sole source of carbon and energy for Sphingomonas xenophaga SKN. Arch Microbiol 179:191–196

  144. Schleinitz KM, Kleinsteuber S, Vallaeys T, Babel W (2004) Localization and characterization of two novel genes encoding stereospecific dioxygenases catalyzing 2(2,4-dichlorophenoxy)propionate cleavage in Delftia acidovorans MC1. Appl Environ Microbiol 70:5357–5365

  145. Schmidt S, Fortnagel P, Wittich R-M (1993) Biodegradation and transformation of 4,4′- and 2,4-dihalodiphenyl ethers by Sphingomonas sp. strain SS33. Appl Environ Microbiol 59:3931–3933

  146. Schmidt S, Wittich R-M, Erdmann D, Wilkes H, Francke W, Fortnagel P (1992) Biodegradation of diphenyl ether and its monohalogenated derivatives by Sphingomonas sp. strain SS3. Appl Environ Microbiol 58:2744–2750

  147. Shepherd JM, Lloyd-Jones G (1998) Novel carbazole degradation genes of Sphingomonas CB3: sequence analysis, transcription, and molecular ecology. Biochem Biophys Res Comm 247:129–135

  148. Shi T, Fredrickson JK, Balkwill DL (2001) Biodegradation of polycyclic aromatic hydrocarbons by Sphingomonas strains isolated from terrestrial subsurface. J Ind Microbiol Biotechnol 26:283–289

  149. Shintani M, Urata M, Inoue K, Eto K, Habe H, Omori T, Yamane H, Nojiri H (2007) The Sphingomonas plasmid pCAR3 is involved in complete mineralization of carbazole. J Bacteriol 189:2007–2020

  150. Shuttleworth KL, Sung J, Kim E, Cerniglia CE (2000) Physiological and genetic comparison of two aromatic hydrocarbon-degrading Sphingomonas strains. Mol Cells 10:199–205

  151. Sørensen SR, Ronen Z, Aamand J (2001) Isolation from agricultural soil and characterization of a Sphingomonas sp. able to mineralize the phenylurea herbicide isoproturon. Appl Environ Microbiol 67:5403–5409

  152. Stolz A (1999) Degradation of substituted naphthalene sulfonic acids by Sphingomonas xenophaga BN6. J Ind Microbiol Biotechnol 23:391–399

  153. Stolz A, Schmidt-Maag C, Denner EBM, Busse H-J, Egli T, Kämpfer P (2000) Description of Sphingomonas xenophaga sp. nov for strains BN6T and N,N which degrade xenobiotic aromatic compounds. Int J Syst Bacteriol 50:35–41

  154. Story SP, Kline EL, Hughes TA, Riley MB, Hayasaka SS (2004) Degradation of aromatic hydrocarbons by Sphingomonas paucimobilis strain EPA505. Arch Environ Contam Toxicol 47:168–176

  155. Taira K, Hayase N, Arimura N, Yamashita S, Miyazaki T, Furukawa K (1988) Cloning and nucleotide sequence of the 2,3-dihydroxybiphenyl dioxygenase gene from the PCB-degrading strain of Pseudomonas paucimobilis Q1. Biochemistry 27:3990–3996

  156. Takeuchi M, Kawai F, Shimada Y, Yokota A (1993) Taxonomic study of polyethylene glycol-utilizing bacteria: emended description of the genus Sphingomonas and new descriptions of Sphingomonas macrogoltabidus sp. nov., Sphingomonas sanguis sp. nov. and Sphingomonas terrae sp. nov. Syst Appl Bacteriol 16:2227–2238

  157. Takeuchi M, Sakane T, Yanagi M, Yamasoto K, Hamana K, Yokota A (1995) Taxonomic study of bacteria isolated from plants: proposal of Sphingomonas rosa sp. nov., Sphingomonas pruni sp. nov., Sphingomonas asaccharolytica sp. nov., and Sphingomonas mali sp. nov. Int J Syst Bacteriol 45:334–341

  158. Takeuchi M, Hamana K, Hiraishi A (2001) Proposal of the genus Sphingomonas sensu strictu and three new genera, Sphingobium, Novosphingobium and Sphingopyxis, on the basis of phylogenetic and chemotaxonomic analyses. Int J Syst Evol Microbiol 51:1405–1417

  159. Tanghe T, Dhooge W, Verstraete W (1999) Isolation of a bacterial strain able to degrade branched nonylphenol. Appl Environ Microbiol 65:746–751

  160. Tani A, Charoenpanich J, Mori T, Takeichi M, Kimbara K, Kawai F (2007) Structure and conservation of a polyethylene glycol-degradative operon in sphingomonads. Microbiology 153:338–346

  161. Thiel M, Kaschabek S, Gröning J, Mau M, Schlömann M (2005) Two unusual chlorocatechol catabolic gene clusters in Sphingomonas sp. TFD44. Arch Microbiol 183:80–94

  162. Thomassin-Lacroix EJM, Yu Z, Eriksson M, Reimer KJ, Mohn WW (2001) DNA-based and culture-based characterization of a hydrocarbon-degrading consortium enriched from Arctic soil. Can J Microbiol 47:1107–1115

  163. Tiirola MA, Mannisto MK, Puhakka JA, Kulomaa MS (2002a) Isolation and characterization of Novosphingobium sp strain MT1, a dominant polychlorophenol-degrading strain in groundwater bioremediation system. Appl Environ Microbiol 68:173–180

  164. Tiirola MA, Wang H, Paulin L, Kulomaa MS (2002b) Evidence for natural horizontal transfer of the pcpB gene in the evolution of pentachlorophenol-degrading sphingomonads. Appl Environ Microbiol 68:4495–4501

  165. Tiirola MA, Busse H-J, Kämpfer P, Männisto MK (2005) Novosphingobium lentum sp. nov., a psychrotolerant bacterium from a polychlorophenol bioremediation process. Int J Syst Evol Microbiol 55:583–588

  166. Urata M, Uchimura H, Noguchi H, Sakaguchi T, Takemura T, Eto K, Habe H, Omori T, Yamane H, Nojiri H (2006) Plasmid pCAR3 contains multiple gene sets involved in the conversion of carbazole to anthranilate. Appl Environ Microbiol 72:3198–3205

  167. Uyttebroek M, Ortega-Calvo J-J, Breugelmans P, Springael D (2006) Comparison of mineralization of solid-sorbed phenanthrene by polycyclic aromatic hydrocarbon (PAH)-degrading Mycobacterium spp. and Sphingomonas spp. Appl Microbiol Biotechnol 72:829–836

  168. Vallaeys T, Courde L, McGowan C, Wright AD, Fulthorpe RR (1999) Phylogenetic analyses indicate independent recruitment of diverse gene cassettes during assemblage of the 2,4-D catabolic pathway. FEMS Microbiol Ecol 28:373–382

  169. Vílchez R, Pozo C, Gómez MA, Rodelas B, González-López J (2007) Dominance of sphingomonads in a copper-exposed biofilm community for groundwater treatment. Microbiology 153:325–337

  170. Wattiau P, Bastiaens L, van Herwijnen R, Daal L, Parsons JR, Renard M-E, Springael D, Cornelis GR (2001) Fluorene degradation by Sphingomonas sp. LB126 proceeds through protocatechuic acid: a genetic analysis. Res Microbiol 152:861–872

  171. Wilkes H, Wittich R, Timmis KN, Fortnagel P, Francke W (1996) Degradation of chlorinated dibenzofurans and dibenzo-p-dioxins by Sphingomonas sp. strain RW1. Appl Environ Microbiol 62:367–371

  172. Willison JC (2004) Isolation and characterization of a novel sphingomonad capable of growth with chrysene as sole carbon and energy source. FEMS Microbiol Lett 241:143–150

  173. Wittich R-M (1998) Degradation of dioxin-like compounds by microorganisms. Appl Microbiol Biotechnol 49:489–499

  174. Wittich R-M, Wilkes H, Sinnwell V, Francke W, Fortnagel P (1992) Metabolism of dibenzo-p-dioxin by Sphingomonas sp. strain RW1. Appl Environ Microbiol 58:1005–1010

  175. Yabuuchi E, Yano I, Oyaizu H, Hashimoto Y, Ezaki T, Yamamoto H (1990) Proposals of Sphingomonas paucimobilis gen. nov. and comb. nov., Sphingomonas parapaucimobilis sp. nov., Sphingomonas yanoikuyae sp. nov., Sphingomonas adhaesiva sp. nov., Sphingomonas capsulata comb. nov., and two genospecies of the genus Sphingomonas. Microbiol Immunol 34:99–119

  176. Yabuuchi E, Yamamoto H, Terakubo S, Okamura N, Naka T, Fujiwara N, Kobayashi K, Kosako Y, Hiraishi A (2001) Proposal of Sphingomonas wittichii sp. nov. for strain RW1T, known as a dibenzo-p-dioxin metabolizer. Int J Syst Evol Microbiol 51:281–292

  177. Yabuuchi E, Kosako Y, Fujiwara N, Naka T, Matsunaga I, Ogura H, Kobayashi K (2002) Emendation of the genus Sphingomonas Yabuuchi et al. 1990 and junior objective synonymy of the species of three genera, Sphingobium, Novosphingobium and Sphingopyxis, in conjunction with Blastomonas ursincola. Int J Syst Evol Microbiol 52:1585–1496

  178. Yan Q-X, Hong Q, Han P, Dong X-J, Shen Y-J, Li S-P (2007) Isolation and characterization of a carbofuran-degrading strain Novosphingobium sp. FND-3. FEMS Microbiol Lett 271:207–213

  179. Ye D, Siddiqi MA, MacCubbin AE, Kumar S, Sikka HC (1996) Degradation of polynuclear aromatic hydrocarbons by Sphingomonas paucimobilis. Environ Sci Technol 30:136–142

  180. Yen K-M, Serdar CM (1988) Genetics of naphthalene catabolism in pseudomonads. CRC Crit Rev Microbiol 15:247–268

  181. Yrjälä K, Suomalainen S, Suhonen EL, Kilpi S, Paulin L, Romantschuk M (1998) Characterization and reclassification of an aromatic- and chloroaromatic-degrading Pseudomonas sp., strain HV3, as Sphingomonas sp. HV3. Int J Syst Bacteriol 48:1057–1062

  182. Yun NR, Shin YK, Hwang SY, Kuraishi H, Sugiyama J, Kawahara K (2000) Chemotaxonomic and phylogenetic analyses of Sphingomonas strains isolated from ears of plants in the family Gramineae and a proposal of Sphingomonas roseoflava sp. nov. J Gen Appl Microbiol 46:9–18

  183. Zipper C, Nickel K, Angst W, Kohler H-P (1996) Complete microbial degradation of both enantiomers of the chiral herbicide Mecoprop [(R,S)-2-(4-Chloro-2-methylphenoxy)propionic acid] in an enantioselective manner by Sphingomonas herbicidovorans sp. nov. Appl Environ Microbiol 62:4318–4322

  184. Zylstra GJ, Kim E (1997) Aromatic hydrocarbon degradation by Sphingomonas yanoikuyae B1. J Ind Microbiol Biotechnol 19:408–414

Download references

Author information

Correspondence to Andreas Stolz.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Stolz, A. Molecular characteristics of xenobiotic-degrading sphingomonads. Appl Microbiol Biotechnol 81, 793–811 (2009). https://doi.org/10.1007/s00253-008-1752-3

Download citation


  • Sphingomonas
  • Sphingomonads
  • Biodegradation
  • Xenobiotics
  • Degradative plasmids