Advertisement

Genome analysis and -omics approaches provide new insights into the biodegradation potential of Rhodococcus

  • Jessica Zampolli
  • Zahraa Zeaiter
  • Alessandra Di Canito
  • Patrizia Di GennaroEmail author
Mini-Review
  • 165 Downloads

Abstract

The past few years observed a breakthrough of genome sequences of bacteria of Rhodococcus genus with significant biodegradation abilities. Invaluable knowledge from genome data and their functional analysis can be applied to develop and design strategies for attenuating damages caused by hydrocarbon contamination. With the advent of high-throughput -omic technologies, it is currently possible to utilize the functional properties of diverse catabolic genes, analyze an entire system at the level of molecule (DNA, RNA, protein, and metabolite), simultaneously predict and construct catabolic degradation pathways. In this review, the genes involved in the biodegradation of hydrocarbons and several emerging plasticizer compounds in Rhodococcus strains are described in detail (aliphatic, aromatics, PAH, phthalate, polyethylene, and polyisoprene). The metabolic biodegradation networks predicted from omics-derived data along with the catabolic enzymes exploited in diverse biotechnological and bioremediation applications are characterized.

Keywords

Rhodococcus -omics Biodegradation Recalcitrant compounds Gene cluster 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in this study were in compliance with ethical standards. This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Abbasian F, Palanisami T, Megharaj M, Naidu R, Lockington R, Ramadass K (2016) Microbial diversity and hydrocarbon degrading gene capacity of a crude oil field soil as determined by metagenomics analysis. Biotechnol Prog 32:638–648CrossRefGoogle Scholar
  2. Alvarez HM (2010) Central metabolism of the species of the genus Rhodococcus. In: Alvarez HM (ed) Biology of Rhodococcus. Springer-Verlag, Berlin Heidelber, pp 91–108CrossRefGoogle Scholar
  3. Amouric A, Quéméneur M, Grossi V, Liebgott PP, Auria R, Casalot L (2010) Identification of different alkane hydroxylase systems in Rhodococcus ruber strain SP2B, an hexane-degrading actinomycete. J Appl Microbiol 108:1903–1916CrossRefGoogle Scholar
  4. Barka EA, Vatsa P, Sanchez L, Gaveau-Vaillant N, Jacquard C, Klenk H-P, Clément C, Ouhdouch Y, van Wezel GP (2016) Taxonomy, physiology, and natural products of Actinobacteria. Microbiol Mol Biol Rev 80:1–43CrossRefGoogle Scholar
  5. Bernhardt R, Urlacher VB (2014) Cytochromes P450 as promising catalysts for biotechnological application: chances and limitations. Appl Microbiol Biotechnol 98:6185–6203CrossRefGoogle Scholar
  6. Cappelletti M, Fedi S, Frascari D, Ohtake H, Turner RJ, Zannoni D (2011) Analyses of both the alkB gene transcriptional start site and alkB promoter-inducing properties of Rhodococcus sp. strain BCP1 grown on n-alkanes. Appl Environ Microbiol 77:1619–1627CrossRefGoogle Scholar
  7. Cappelletti M, Di Gennaro P, D’Ursi P, Orro A, Mezzelani A, Landini M, Fedi S, Frascari D, Presentato A, Zannoni D, Milanesi L (2013) Genome sequence of Rhodococcus sp. strain BCP1, a biodegrader of alkanes and chlorinated compounds. Genome Announc 1:e00657–e00613CrossRefGoogle Scholar
  8. Cappelletti M, Presentato A, Milazzo G, Turner RJ, Fedi S, Frascari D, Zannoni D (2015) Growth of Rhodococcus sp. strain BCP1 on gaseous n-alkanes: new metabolic insights and transcriptional analysis of two soluble di-iron monooxygenase genes. Front Microbiol  https://doi.org/10.3389/fmicb.2015.00393
  9. Cardini G, Jurtshuk P (1970) The enzymatic hydroxylation of n-octane by Corynebacterium sp. strain 7E1C. J Biol Chem 245:2789–2796PubMedGoogle Scholar
  10. Cerniglia CE (1984) Microbial metabolism of polycyclic aromatic hydrocarbons. Adv Appl Microbiol 30:31–71CrossRefGoogle Scholar
  11. Choi KY, Kim D, Sul WJ, Chae J-C, Zylstra GJ, Kim YM, Kim E (2005) Molecular and biochemical analysis of phthalate and terephthalate degradation by Rhodococcus sp. strain DK17. FEMS Microbiol Lett 252:207–213CrossRefGoogle Scholar
  12. Ciavarelli R, Cappelletti M, Fedi S, Pinelli D, Frascari D (2012) Chloroform aerobic cometabolism by butane-growing Rhodococcus aetherivorans BCP1 in continuous-flow biofilm reactors. Bioprocess Biosyst Eng 35:667–681CrossRefGoogle Scholar
  13. Crombie AT, El Khawand M, Rhodius VA, Fengler KA, Miller MC, Whited GM, Mcgenity TJ, Murrell JC (2015) Regulation of plasmid-encoded isoprene metabolism in Rhodococcus, a representative of an important link in the global isoprene cycle. Environ Microbiol 17:3314–3329CrossRefGoogle Scholar
  14. De Carvalho CCCR, Da Cruz AARL, Pons MN, Pinheiro HMRV, Cabral JMS, Da Fonseca MMR, Ferreira BS, Fernandes P (2004) Mycobacterium sp., Rhodococcus erythropolis, and Pseudomonas putida behavior in the presence of organic solvents. Microsc Res Tech 64:215–222CrossRefGoogle Scholar
  15. Di Canito A, Zampolli J, Orro A, D’Ursi P, Milanesi L, Sello G, Steinbüchel A, Di Gennaro P (2018) Genome-based analysis for the identification of genes involved in o-xylene degradation in Rhodococcus opacus R7. BMC Genomics 19:587CrossRefGoogle Scholar
  16. Di Gennaro P, Terreni P, Masi G, Botti S, De Ferra F, Bestetti G (2010) Identification and characterization of genes involved in naphthalene degradation in Rhodococcus opacus R7. Appl Microbiol Biotechnol 87:297–308CrossRefGoogle Scholar
  17. Di Gennaro P, Zampolli J, Presti I, Cappelletti M, D’Ursi P, Orro A, Mezzelani A, Milanesi L (2014) Genome sequence of Rhodococcus opacus strain R7, a biodegrader of mono- and polycyclic aromatic hydrocarbons. Genome Announc 2:e00827CrossRefGoogle Scholar
  18. Fang Y, Du Y, Hu L, Xu J, Long Y, Shen D (2016) Effects of sulfur-metabolizing bacterial community diversity on H2S emission behavior in landfills with different operation modes. Biodegradation 27:237–246CrossRefGoogle Scholar
  19. Fialova A, Cejkova A, Masak J, Jirku V (2003) Comparison of yeast (Candida maltosa) and bacterial (Rhodococcus erythropolis) phenol hydroxylase activity and its properties in the phenolic compounds biodegradation. Commun Agric Appl Biol Sci 68:155–158PubMedGoogle Scholar
  20. Field JA, Sierra-Alvarez R (2004) Biodegradability of chlorinated solvents and related chlorinated aliphatic compounds. Rev Environ Sci Biotechnol 3:185–254CrossRefGoogle Scholar
  21. Fleischmann RD, Adams MD, White O, Clayton RA, Kirkness EF, Kerlavage AR, Bult CJ, Tomb JF, Dougherty BA, Merrick JM, McKenney K, Sutton G, FitzHugh W, Fields C, Gocayne JD, Scott J, Shirley R, Liu LI, Glodek A, Kelley JM, Weidman JF, Phillips CA, Spriggs T, Hedblom E, Cotton MD, Utterback TR, Hanna MC, Nguyen DT, Saudek DM, Brandon RC, Fine LD, Fritchman JL, Fuhrmann JL, Geoghagen NSM, Gnehm CL, McDonald LA, Small KV, Fraser CM, Smith HO, Venter JC (1995) Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269:496–512CrossRefGoogle Scholar
  22. Goncalves ER, Hara H, Miyazawa D, Davies JE, Eltis LD, Mohn WW (2006) Transcriptomic assessment of isozymes in the biphenyl pathway of Rhodococcus sp. strain RHA1. Appl Environ Microbiol 72:6183–6193CrossRefGoogle Scholar
  23. Gravouil K, Ferru-Clément R, Colas S, Helye R, Kadri L, Bourdeau L, Moumen B, Mercier A, Ferreira T (2017) Transcriptomics and lipidomics of the environmental strain Rhodococcus ruber point out consumption pathways and potential metabolic bottlenecks for polyethylene degradation. Environ Sci Technol 51:5172–5181CrossRefGoogle Scholar
  24. Guzik U, Greń I, Hupert-Kocurek K, Wojcieszyńska D (2011) Catechol 1,2-dioxygenase from the new aromatic compounds-degrading Pseudomonas putida strain N6. Int Biodeterior Biodegrad 65:504–512CrossRefGoogle Scholar
  25. Hara H, Eltis LD, Davies JE, Mohn WW (2007) Transcriptomic analysis reveals a bifurcated terephthalate degradation pathway in Rhodococcus sp. strain RHA1. J Bacteriol 189:1641–1647CrossRefGoogle Scholar
  26. Hara H, Stewart GR, Mohn WW (2010) Involvement of a novel ABC transporter and monoalkyl phthalate ester hydrolase in phthalate ester catabolism by Rhodococcus jostii RHA1. Appl Environ Microbiol 76:1516–1523CrossRefGoogle Scholar
  27. Holder JW, Ulrich JC, DeBono AC, Godfrey PA, Desjardins CA, Zucker J, Zeng Q, Leach ALB, Ghiviriga I, Dancel C, Abeel T, Gevers D, Kodira CD, Desany B, Affourtit JP, Birren BW, Sinskey AJ (2011) Comparative and functional genomics of Rhodococcus opacus PD630 for biofuels development. PLoS Genet 7:e1002219CrossRefGoogle Scholar
  28. Imbernon L, Oikonomou EK, Norvez S, Leibler L (2015) Chemically crosslinked yet reprocess able epoxidized natural rubber via thermo-activated disulfide rearrangements. Polym Chem 6:4271–4278CrossRefGoogle Scholar
  29. Irvine VA, Kulakov LA, Larkin MJ (2000) The diversity of extradiol dioxygenase “edo” genes in cresol degrading rhodococci from a creosote-contaminated site that express a wide range of degradative abilities. Antonie van Leeuwenhoek, Int J Gen Mol Microbiol 78:341–352CrossRefGoogle Scholar
  30. Jang L, Keng H (2006) Development and characterization of as a monolayer for protein chips. Sens Mater 18:367–380Google Scholar
  31. Jones A, Goodfellow M (2010) Genus II. Rhodococcus (Zopf 1891) emend Goodfellow et al. 1998. In: Bergey’s Manual of Systematic Bacteriology, vol 4, 2nd edn. Springer, Berlin, pp 1–65Google Scholar
  32. Juwarkar AA, Singh SK, Mudhoo A (2010) A comprehensive overview of elements in bioremediation. Rev Environ Sci Biotechnol 9:215–288CrossRefGoogle Scholar
  33. Khairy H, Meinert C, Wübbeler JH, Poehlein A, Daniel R, Voigt B, Riedel K, Steinbüchel A (2016) Genome and proteome analysis of Rhodococcus erythropolis MI2: elucidation of the 4,4′-dithiodibutyric acid catabolism. PLoS One 11:e0167539CrossRefGoogle Scholar
  34. Kim D, Kim Y-S, Kim S-K, Kim SW, Zylstra GJ, Kim YM, Kim E (2002) Monocyclic aromatic hydrocarbon degradation by Rhodococcus sp. strain DK17. Appl Environ Microbiol 68:3270–3278CrossRefGoogle Scholar
  35. Kim SH, Han HY, Lee YJ, Kim CW, Yang JW (2010) Effect of electrokinetic remediation on indigenous microbial activity and community within diesel contaminated soil. Sci Total Environ 408:3162–3168CrossRefGoogle Scholar
  36. Kim D, Choi KY, Yoo M, Zylstra GJ, Kim E (2018) Biotechnological potential of Rhodococcus biodegradative pathways. J Microbiol Biotechnol 28:1037–1051PubMedGoogle Scholar
  37. Kolomytseva MP, Baskunov BP, Golovleva LA (2007) Intradiol pathway of para-cresol conversion by Rhodococcus opacus 1CP. Biotechnol J 2:886–893CrossRefGoogle Scholar
  38. Koutny M, Sancelme M, Dabin C, Pichon N, Delort AM, Lemaire J (2006) Acquired biodegradability of polyethylenes containing pro-oxidant additives. Polym Degrad Stab 91:1495–1503CrossRefGoogle Scholar
  39. Kulakov LA, Allen CCR, Lipscomb DA, Larkin MJ (2000) Cloning and characterization of a novel cis-naphthalene dihydrodiol dehydrogenase gene (narB) from Rhodococcus sp. NCIMB12038. FEMS Microbiol Lett 182:327–331CrossRefGoogle Scholar
  40. Kulakov LA, Chen S, Allen CCR, Larkin MJ (2005) Web-type evolution of Rhodococcus gene clusters associated with utilization of naphthalene. Appl Environ Microbiol 71:1754–1764CrossRefGoogle Scholar
  41. Kulig JK, Spandolf C, Hyde R, Ruzzini AC, Eltis LD, Grönberg G, Hayes MA, Grogan G (2015) A P450 fusion library of heme domains from Rhodococcus jostii RHA1 and its evaluation for the biotransformation of drug molecules. Bioorganic Med Chem 23:5603–5609CrossRefGoogle Scholar
  42. Laczi K, Kis Á, Horváth B, Maróti G, Hegedüs B, Perei K, Rákhely G (2015) Metabolic responses of Rhodococcus erythropolis PR4 grown on diesel oil and various hydrocarbons. Appl Microbiol Biotechnol 99:9745–9759CrossRefGoogle Scholar
  43. Land M, Hauser L, Jun SR, Nookaew I, Leuze MR, Ahn TH, Karpinets T, Lund O, Kora G, Wassenaar T, Poudel S, Ussery DW (2015) Insights from 20 years of bacterial genome sequencing. Funct Integr Genomics 15:141–161CrossRefGoogle Scholar
  44. Larkin MJ, Kulakov LA, Allen CC (2006) Biodegradation by members of the genus Rhodococcus: biochemistry, physiology, and genetic adaptation. Adv Appl Microbiol 59:1–29CrossRefGoogle Scholar
  45. Larkin MJ, Kulakov LA, Allen CC (2010) Genomes and plasmids in Rhodococcus. In: Alvarez HM (ed) Biology of Rhodococcus. Springer, Berlin, pp 73–90CrossRefGoogle Scholar
  46. LeBlanc JC, Gonçalves ER, Mohn WW (2008) Global response to desiccation stress in the soil actinomycete Rhodococcus jostii RHA1. Appl Environ Microbiol 74:2627–2636CrossRefGoogle Scholar
  47. Ludwig W, Euzéby J, Schumann P, Buss HJ, Trujillo ME, Kämpfer P, Whiteman WB (2012) Road map of the phylum Actinobacteria. In: Goodfellow M, Kämpfer P, Busse HJ, Trujillo ME, Suzuki KI, Ludwig W, Whitman WB (eds) Bergey’s manual of systematic bacteriology. Springer-Verlag, New York, pp 1–28Google Scholar
  48. Martínková L, Uhnáková B, Pátek M, Nešvera J, Křen V (2009) Biodegradation potential of the genus Rhodococcus. Environ Int 35:162–177CrossRefGoogle Scholar
  49. Maruyama T, Ishikura M, Taki H, Shindo K, Kasai H, Haga M, Inomata Y, Misawa N (2005) Isolation and characterization of o-xylene oxygenase genes from Rhodococcus opacus TKN14. Appl Environ Microbiol 71:7705–7715CrossRefGoogle Scholar
  50. McLeod MP, Warren RL, Hsiao WWL, Araki N, Myhre M, Fernandes C, Miyazawa D, Wong W, Lillquist AL, Wang D, Dosanjh M, Hara H, Petrescu A, Morin RD, Yang G, Stott JM, Schein JE, Shin H, Smailus D, Siddiqui AS, Marra MA, Jones SJM, Holt R, Brinkman FSL, Miyauchi K, Fukuda M, Davies JE, Mohn WW, Eltis LD (2006) The complete genome of Rhodococcus sp. RHA1 provides insights into a catabolic powerhouse. Proc Natl Acad Sci USA 103:15582–15587CrossRefGoogle Scholar
  51. Michałowicz J, Duda W (2007) Phenols-sources and toxicity. Polish J Environ Stud 6:347–362Google Scholar
  52. Nanthini J, Chia KH, Thottathil GP, Taylor TD, Kondo S, Najimudin N, Baybayane P, Singh S, Sudesh K (2015) Complete genome sequence of Streptomyces sp. strain CFMR 7, a natural rubber degrading actinomycete isolated from Penang, Malaysia. J Biotechnol 214:47–48CrossRefGoogle Scholar
  53. Orro A, Cappelletti M, D’Ursi P, Milanesi L, Di Canito A, Zampolli J, Collina E, Decorosi F, Viti C, Fedi S, Presentato A, Zannoni D, Di Gennaro P (2015) Genome and phenotype microarray analyses of Rhodococcus sp. BCP1 and Rhodococcus opacus R7: genetic determinants and metabolic abilities with environmental relevance. PLoS One 10:e0139467CrossRefGoogle Scholar
  54. Pathak A, Chauhan A, Blom J, Indest KJ, Jung CM, Stothard P, Bera G, Green SJ, Ogram A (2016) Comparative genomics and metabolic analysis reveals peculiar characteristics of Rhodococcus opacus strain M213 particularly for naphthalene degradation. PLoS One 11:e0161032CrossRefGoogle Scholar
  55. Patrauchan MA, Florizone C, Dosanjh M, Mohn WW, Davies J, Eltis LD (2005) Catabolism of benzoate and phthalate in Rhodococcus sp. strain RHA1: redundancies and convergence. J Bacteriol 187:4050–4063CrossRefGoogle Scholar
  56. Patrauchan MA, Miyazawa D, LeBlanc JC, Aiga C, Florizone C, Dosanjh M, Davies J, Eltis LD, Mohn WW (2012) Proteomic analysis of survival of Rhodococcus jostii RHA1 during carbon starvation. Appl Environ Microbiol 78:6714–6725CrossRefGoogle Scholar
  57. Pérez-Pantoja D, Donoso R, Junca H, González D, Pieper H (2009) Phylogenomics of aerobic bacterial degradation of aromatics. Handbook of hydrocarbon and lipid microbiology, In, pp 1355–1397Google Scholar
  58. Puglisi E, Cahill MJ, Lessard PA, Capri E, Sinskey AJ, Archer JAC, Boccazzi P (2010) Transcriptional response of Rhodococcus aetherivorans I24 to polychlorinated biphenyl-contaminated sediments. Microb Ecology 60:505–515CrossRefGoogle Scholar
  59. Rose K, Tenberge KB, Steinbüchel A (2005) Identification and characterization of genes from Streptomyces sp. strain K30 responsible for clear zone formation on natural rubber latex and poly(cis-1,4-isoprene) rubber degradation. Biomacromolecules 6:180–188CrossRefGoogle Scholar
  60. Rosłoniec KZ, Wilbrink MH, Capyk JK, Mohn WW, Ostendorf M, Van Der Geize R, Dijkhuizen L, Eltis LD (2009) Cytochrome P450 125 (CYP125) catalyses C26-hydroxylation to initiate sterol side-chain degradation in Rhodococcus jostii RHA1. Mol Microbiol 74:1031–1043CrossRefGoogle Scholar
  61. Rosłoniec KZ, van der Geize R, Dijkhuizen L (2013) CYP257A1 of Rhodococcus jostii strain RHA1 represents a novel cytochrome P450 enzyme family with demethylase activity and a putative physiological role in sterol metabolism. Dissertation, University of GroningenGoogle Scholar
  62. Sameshima Y, Honda K, Kato J, Omasa T, Ohtake H (2008) Expression of Rhodococcus opacus alkB genes in anhydrous organic solvents. J Biosci Bioeng 106:199–203CrossRefGoogle Scholar
  63. Santo M, Weitsman R, Sivan A (2013) The role of the copper-binding enzyme-laccase-in the biodegradation of polyethylene by the actinomycete Rhodococcus ruber. Int Biodeterior Biodegrad 84:204–210CrossRefGoogle Scholar
  64. Sekine M, Tanikawa S, Omata S, Saito M, Fujisawa T, Tsukatani N, Tajima T, Sekigawa T, Kosugi H, Matsuo Y, Nishiko R, Imamura K, Ito M, Narita H, Tago S, Fujita N, Harayama S (2006) Sequence analysis of three plasmids harboured in Rhodococcus erythropolis strain PR4. Environ Microbiol 8 (2):334–346Google Scholar
  65. Seto M, Kimbara K, Shimura M, Hatta T, Fukuda M, Yano K (1995) A novel transformation of polychlorinated biphenyls by Rhodococcus sp. strain RHA1. Appl Environ Microbiol 61:3353–3358PubMedPubMedCentralGoogle Scholar
  66. Sharkey TD (1996) Isoprene synthesis by plants and animals. Endeavour 20:74–78CrossRefGoogle Scholar
  67. Shields-Menard SA, AmirSadeghi M, Green M, Womack E, Sparks DL, Blake J, Edelmann M, Ding X, Sukhbaatar B, Hernandez R, Donaldson JR, French T (2017) The effects of model aromatic lignin compounds on growth and lipid accumulation of Rhodococcus rhodochrous. Int Biodeterior Biodegrad 121:79–90CrossRefGoogle Scholar
  68. Sivan A, Szanto M, Pavlov V (2006) Biofilm development of the polyethylene-degrading bacterium Rhodococcus ruber. Appl Microbiol Biotechnol 72:346–352CrossRefGoogle Scholar
  69. Smith MR (1990) The biodegradation of aromatic hydrocarbons by bacteria. Biodegradation 1:191–206CrossRefGoogle Scholar
  70. Swain K, Casabon I, Eltis LD, Mohn WW (2012) Two transporters essential for reassimilation of novel cholate metabolites by Rhodococcus jostii RHA1. J Bacteriol 194:6720–6727CrossRefGoogle Scholar
  71. Szőköl J, Rucká L, Šimčíková M, Halada P, Nešvera J, Pátek M (2014) Induction and carbon catabolite repression of phenol degradation genes in Rhodococcus erythropolis and Rhodococcus jostii. Appl Microbiol Biotechnol 98:8267–8279CrossRefGoogle Scholar
  72. Takeda H, Yamada A, Miyauchi K, Masai E, Fukuda M (2004) Characterization of transcriptional regulatory genes for biphenyl degradation in Rhodococcus sp. strain RHA1. J Bacteriol 186:2134–2146CrossRefGoogle Scholar
  73. Táncsics A, Benedek T, Farkas M, Máthé I, Márialigeti K, Szoboszlay S, Kukolya J, Kriszt B (2014) Sequence analysis of 16S rRNA, gyrB and catA genes and DNA-DNA hybridization reveal that Rhodococcus jialingiae is a later synonym of Rhodococcus qingshengii. Int J Syst Evol Microbiol 64:298–301CrossRefGoogle Scholar
  74. Tao F, Zhao P, Li Q, Su F, Yu B, Ma C, Tang H, Tai C, Wu G, Xu P (2011) Genome sequence of Rhodococcus erythropolis XP, a biodesulfurizing bacterium with industrial potential. J Bacteriol 193:6422–6423CrossRefGoogle Scholar
  75. Van Beilen JB, Funhoff EG, Van Loon A, Just A, Kaysser L, Bouza M, Holtackers R, Röthlisberger M, Li Z, Witholt B (2006) Cytochrome P450 alkane hydroxylases of the CYP153 family are common in alkane-degrading eubacteria lacking integral membrane alkane hydroxylases. Appl Environ Microbiol 72:59–65CrossRefGoogle Scholar
  76. Van Der Geize R, Dijkhuizen L (2004) Harnessing the catabolic diversity of rhodococci for environmental and biotechnological applications. Curr Opin Microbiol 7:255–261CrossRefGoogle Scholar
  77. Van Hylckama Vlieg JET, Leemhuis H, LutjeSpelberg JH, Janssen DB (2000) Characterization of the gene cluster involved in isoprene metabolism in Rhodococcus sp. strain AD45. J Bacteriol 182:1956–1963CrossRefGoogle Scholar
  78. Vilchez-Vargas R, Junca H, Pieper DH (2010) Metabolic networks, microbial ecology and “omics” technologies: towards understanding in situ biodegradation processes. Environ Microbiol 12:3089–3104CrossRefGoogle Scholar
  79. Watcharakul S, Röther W, Birke J, Umsakul K, Hodgson B, Jendrossek D (2016) Biochemical and spectroscopic characterization of purified latex clearing protein (Lcp) from newly isolated rubber degrading Rhodococcus rhodochrous strain RPK1 reveals novel properties of Lcp. BMC Microbiol 16:92CrossRefGoogle Scholar
  80. Whyte LG, Smits THM, Labbé D, Witholt B, Greer CW, Van Beilen JB (2002) Gene cloning and characterization of multiple alkane hydroxylase systems in Rhodococcus strains Q15 and NRRL B-16531. Appl Environ Microbiol 68:5933–5942CrossRefGoogle Scholar
  81. Xu-Xiang Z, Shu-Pei C, Cheng-Jun Z, Shi-Lei S (2006) Microbial PAH-degradation in soil: degradation pathways and contributing factors. Pedosphere 16:555–565CrossRefGoogle Scholar
  82. Yoneda A, Henson WR, Goldner NK, Park KJ, Forsberg KJ, Kim SJ, Pesesky MW, Foston M, Dantas G, Moon TS (2016) Comparative transcriptomics elucidates adaptive phenol tolerance and utilization in lipid-accumulating Rhodococcus opacus PD630. Nucleic Acids Res 44:2240–2254CrossRefGoogle Scholar
  83. Yoo M, Kim D, Choi KY, Chae JC, Zylstra GJ, Kim E (2012) Draft genome sequence and comparative analysis of the superb aromatic-hydrocarbon degrader Rhodococcus sp. strain DK17. J Bacteriol 194(16):4440Google Scholar
  84. Zampolli J, Collina E, Lasagni M, Di Gennaro P (2014) Biodegradation of variable-chain-length n-alkanes in Rhodococcus opacus R7 and the involvement of an alkane hydroxylase system in the metabolism. AMB Express 4:73CrossRefGoogle Scholar
  85. Zídková L, Szoköl J, Rucká L, Pátek M, Nešvera J (2013) Biodegradation of phenol using recombinant plasmid-carrying Rhodococcus erythropolis strains. Int Biodeterior Biodegrad 84:179–184CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Jessica Zampolli
    • 1
  • Zahraa Zeaiter
    • 1
  • Alessandra Di Canito
    • 1
  • Patrizia Di Gennaro
    • 1
    Email author
  1. 1.Department of Biotechnology and BiosciencesUniversity of Milano-BicoccaMilanItaly

Personalised recommendations