Genomics of Rhodococcus

  • Martina CappellettiEmail author
  • Jessica Zampolli
  • Patrizia Di Gennaro
  • Davide Zannoni
Part of the Microbiology Monographs book series (MICROMONO, volume 16)


Members of the genus Rhodococcus have metabolic versatility and unique adaptation capacities to fluctuating environmental conditions, enabling the colonization of a wide variety of environments; they also play an important role in nutrient cycling and have potential applications in bioremediation, biotransformations and biocatalysis. Rhodococcus spp. are mainly distributed in soil, water and marine sediments, although some of them are also pathogens for humans, animals and plants. Consistent with the wide catabolic diversity, Rhodococcus spp. possess large and complex genomes (up to 10.1 Mbp), which contain a multiplicity of catabolic genes, high genetic redundancy of biosynthetic pathways and large catabolic plasmids, the latter encoding peculiar metabolic and physiological traits. Recently, the progress in sequencing technology led to a dramatic increase in the number of sequenced Rhodococcus genomes, which have been investigated through diverse bioinformatic approaches. In particular, whole-genome comparative and genome-based functional studies were associated to omic technologies for the study of the global Rhodococcus cell response with the aim of providing insight into the genetic basis of specific catabolic capacities and phenotypic traits. Lastly, genome-based advances in Rhodococcus engineering led to the first design of molecular toolkits for tunable and targeted genome editing. Besides this, genome-based metabolic models were developed to make metabolic predictions of the Rhodococcus cell response to specific growth conditions. Both the synthetic and system approaches offered new opportunities for genome-scale rational design of Rhodococcus cell for environmental and industrial applications.


Rhodococcus genome Comparative genomics Functional genomics Gene redundancy Catabolic plasmid 


  1. Ali A (2013) Microbial comparative genomics: an overview of tools and insights into the genus Corynebacterium. J Bacteriol Parasitol 04:1–16. CrossRefGoogle Scholar
  2. Alvarez HM, Mayer F, Fabritius D et al (1996) Formation of intracytoplasmic lipid inclusions by Rhodococcus opacus strain PD630. Arch Microbiol 165:377–386PubMedPubMedCentralCrossRefGoogle Scholar
  3. Amara S, Seghezzi N, Otani H et al (2016) Characterization of key triacylglycerol biosynthesis processes in rhodococci. Sci Rep 6:24985. CrossRefPubMedPubMedCentralGoogle Scholar
  4. Aminov RI (2011) Horizontal gene exchange in environmental microbiota. Front Microbiol 2:158. CrossRefPubMedPubMedCentralGoogle Scholar
  5. Anastasi E, MacArthur I, Scortti M (2016) Pangenome and phylogenomic analysis of the pathogenic actinobacterium Rhodococcus equi. Genome Biol Evol 8(10):3140–3148PubMedPubMedCentralCrossRefGoogle Scholar
  6. Bentley SD, Chater KF, Cerdeño-Tárraga AM et al (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417(6885):141–147PubMedCrossRefGoogle Scholar
  7. Cappelletti M (2010) Monooxygenases involved in the n-alkanes metabolism by Rhodococcus sp. BCP1. PhD Thesis Dissertation, University of BolognaGoogle Scholar
  8. spiepr A3B2 twb=.25w?>Cappelletti M, Fedi S, Frascari D et al (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 77:1619–1627PubMedCrossRefGoogle Scholar
  9. Cappelletti M, Frascari ZD et al (2012) Microbial degradation of chloroform. Appl Microbiol Biotechnol 96:1395–1409PubMedCrossRefGoogle Scholar
  10. spiepr A3B2 tlsb=-.02w?>Cappelletti M, Di Gennaro P, D’Ursi P et al (2013) Genome sequence of Rhodococcus sp. strain BCP1, a biodegrader of alkanes and chlorinated compounds. Genome Announc 1(5):e00657–e00613. CrossRefPubMedPubMedCentralGoogle Scholar
  11. Cappelletti M, Presentato A, Milazzo G et al (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 6:393. CrossRefPubMedPubMedCentralGoogle Scholar
  12. Cappelletti M, Fedi S, Zampolli J et al (2016) Phenotype microarray analysis may unravel genetic determinants of the stress response by Rhodococcus aetherivorans BCP1 and Rhodococcus opacus R7. Res Microbiol 167:1–9CrossRefGoogle Scholar
  13. Cappelletti M, Pinelli D, Fedi S (2017) Aerobic co-metabolism of 1,1,2,2-tetrachloroethane by Rhodococcus aetherivorans TPA grown on propane: kinetic study and bioreactor configuration analysis. J Chem Technol Biotechnol 93:155–165CrossRefGoogle Scholar
  14. Carroll AC, Wong A (2018) Plasmid persistence: costs, benefits, and the plasmid paradox. Can J Microbiol 64:293–304PubMedCrossRefPubMedCentralGoogle Scholar
  15. Castro AR, Rocha I, Alves MM et al (2016) Rhodococcus opacus B4: a promising bacterium for production of biofuels and biobased chemicals. AMB Express 6:35. CrossRefPubMedPubMedCentralGoogle Scholar
  16. Ceniceros A, Dijkhuizen L, Petrusma M et al (2017) Genome-based exploration of the specialized metabolic capacities of the genus Rhodococcus. BMC Genomics 18:593. CrossRefPubMedPubMedCentralGoogle Scholar
  17. Chen CW, Huang CH, Lee HH et al (2002) Once the circle has been broken: dynamics and evolution of Streptomyces chromosomes. Trends Genet 18:522–529PubMedCrossRefPubMedCentralGoogle Scholar
  18. Chen Y, Ding Y, Yang L et al (2014) Integrated omics study delineates the dynamics of lipid droplets in Rhodococcus opacus PD630. Nucleic Acids Res 42(2):1052–1064PubMedPubMedCentralCrossRefGoogle Scholar
  19. Choi KY, Kim D, Sul WJ et al (2005) Molecular and biochemical analysis of phthalate and terephthalate degradation by Rhodococcus sp. strain DK17. FEMS Microbiol Lett 252:207–213PubMedCrossRefPubMedCentralGoogle Scholar
  20. Choi KY, Kim D, Chae JC et al (2007) Requirement of duplicated operons for maximal metabolism of phthalate by Rhodococcus sp. strain DK17. Biochem Biophys Res Commun 357:766–771PubMedCrossRefPubMedCentralGoogle Scholar
  21. Ciavarelli R, Cappelletti M, Fedi S et al (2012) Chloroform aerobic cometabolism by butane-growing Rhodococcus aetherovorans BCP1 in continuous-flow biofilm reactors. Bioprocess Biosyst Eng 35:667–681PubMedCrossRefPubMedCentralGoogle Scholar
  22. Costa JSD, Herrero OM, Alvarez HM et al (2015) Label-free and redox proteomic analyses of the triacylglycerol-accumulating Rhodococcus jostii RHA1. Microbiology 161:593–610CrossRefGoogle Scholar
  23. Creason AL, Vandeputte OM, Savory EA et al (2014a) Analysis of genome sequences from plant pathogenic Rhodococcus reveals genetic novelties in virulence loci. PLoS One 9(7):e101996. CrossRefPubMedPubMedCentralGoogle Scholar
  24. Creason AL, Davis EW II, Putnam ML et al (2014b) Use of whole genome sequences to develop a molecular phylogenetic framework for Rhodococcus fascians and the Rhodococcus genus. Front Plant Sci 5:406. CrossRefPubMedPubMedCentralGoogle Scholar
  25. Crespi M, Vereecke D, Temmerman W et al (1994) The fas operon of Rhodococcus fascians encodes new genes required for efficient fasciation of host plants. J Bacteriol 176:2492–2501PubMedPubMedCentralCrossRefGoogle Scholar
  26. Crombie TA, Rhodius VA, Miller MC et al (2015) Regulation of plasmid-encoded isoprene metabolism in Rhodococcus, a representative of an important link in the global isoprene cycle. Environ Microbiol 17:3314–3329PubMedPubMedCentralCrossRefGoogle Scholar
  27. de Carvalho CCCR, da Fonseca MMR (2005) The remarkable Rhodococcus erythropolis. Appl Microbiol Biotechnol 67:715–726CrossRefGoogle Scholar
  28. de Carvalho CCCR, Costa SS, Fernandes P et al (2014) Membrane transport systems and the biodegradation potential and pathogenicity of genus Rhodococcus. Front Physiol 5:133. CrossRefPubMedPubMedCentralGoogle Scholar
  29. spiepr A3B2 tlsb=-.02w?>De Mot R, Nagy I, De Schrijver A et al (1997) Structural analysis of the 6 kb cryptic plasmid pFAJ2600 from Rhodococcus erythropolis NI86/21 and construction of Escherichia coliRhodococcus shuttle vectors. Microbiology 143:3137–3147PubMedCrossRefPubMedCentralGoogle Scholar
  30. DeLorenzo DM, Rottinghaus AG, Henson WR et al (2018) Molecular toolkit for gene expression control and genome modification in Rhodococcus opacus PD630. ACS Synth Biol 7(2):727–738PubMedCrossRefPubMedCentralGoogle Scholar
  31. Denis-Larose C, Labbe D, Bergeron H et al (1997) Conservation of plasmid-encoded dibenzothiophene desulfurization genes in several rhodococci. Appl Environ Microbiol 63:2915–2919PubMedPubMedCentralGoogle Scholar
  32. Desomer J, Crespi M, Van Montagu M (1991) Illegitimate integration of non-replicative vectors in the genome of Rhodococcus fascians upon electrotransformation as an insertional mutagenesis system. Mol Microbiol 5:2115–2124PubMedCrossRefGoogle Scholar
  33. Di Canito A, Zampolli J, Orro A et al (2018) Genome-based analysis for the identification of genes involved in o-xylene degradation in Rhodococcus opacus R7. BMC Genomics 19:587PubMedPubMedCentralCrossRefGoogle Scholar
  34. Di Gennaro P, Rescalli E, Galli E et al (2001) Characterization of Rhodococcus opacus R7, a strain able to degrade naphthalene and o-xylene isolated from polycyclic aromatic hydrocarbon-contaminated soil. Res Microbiol 152:641–651PubMedCrossRefPubMedCentralGoogle Scholar
  35. Di Gennaro P, Terreni P, Masi G et al (2010) Identification and characterization of genes involved in naphthalene degradation in Rhodococcus opacus R7. Appl Microbiol Biotechnol 87(1):297–308PubMedCrossRefGoogle Scholar
  36. Di Gennaro P, Zampolli J, Presti I et al (2014) Genome sequence of Rhodococcus opacus strain R7, a biodegrader of mono- and polycyclic aromatic hydrocarbons. Genome Announc 2(4):e00827–e00814. CrossRefPubMedPubMedCentralGoogle Scholar
  37. Dib JR, Wagenknecht M, Farías ME et al (2015) Strategies and approaches in plasmidome studies—uncovering plasmid diversity disregarding of linear elements? Front Microbiol 6:463. CrossRefPubMedPubMedCentralGoogle Scholar
  38. Dodge AG, Wackett LP, Sadowsky MJ (2011) Plasmid localization and organization of melamine degradation genes in Rhodococcus sp strain Mel. Appl Environ Microbiol 78(5):1397–1403. CrossRefPubMedGoogle Scholar
  39. Dueholm MS, Albertsen M, D’Imperio S (2014) Complete genome of Rhodococcus pyridinivorans SB3094, a methyl-ethyl-ketone-degrading bacterium used for bioaugmentation. Genome Announc 2(3):e00525-14. CrossRefPubMedPubMedCentralGoogle Scholar
  40. Duran R (1998) New shuttle vectors for Rhodococcus sp. R312 (formerly Brevibacterium sp. R312), a nitrile hydratase producing strain. J Basic Microbiol 38:101–106PubMedCrossRefGoogle Scholar
  41. Ellinger J, Schmidt-Dannert C (2017) Construction of a BioBrick™ compatible vector system for Rhodococcus. Plasmid 90:1–4. CrossRefPubMedGoogle Scholar
  42. Fang H, Xu T, Cao D et al (2016) Characterization and genome functional analysis of a novel metamitron-degrading strain Rhodococcus sp. MET via both triazinone and phenyl rings cleavage. Sci Rep 6:32339. CrossRefPubMedPubMedCentralGoogle Scholar
  43. Francis I, De Keyser A, De Backer P et al (2012) pFiD188, the linear virulence plasmid of Rhodococcus fascians D188. MPMI 25:637–647PubMedCrossRefGoogle Scholar
  44. Francis IM, Stes E, Zhang Y et al (2016) Mining the genome of Rhodococcus fascians, a plant growth-promoting bacterium gone astray. New Biotechnol 33:706–717CrossRefGoogle Scholar
  45. Frascari D, Pinelli D, Nocentini M et al (2006) Chloroform degradation by butane-grown cells of Rhodococcus aetherovorans BCP1. Appl Microbiol Biotechnol 73(2):421–428PubMedCrossRefGoogle Scholar
  46. Fukuda M, Shimizu S, Okita N et al (1998) Structural alteration of linear plasmids encoding the genes for polychlorinated biphenyl degradation in Rhodococcus strain RHA1. Antonie Leeuwenhoek 74:169–173PubMedCrossRefGoogle Scholar
  47. Gao B, Gupta RS (2012) Phylogenetic framework and molecular signatures for the main clades of the phylum Actinobacteria. Microbiol Mol Biol Rev 76(1):66–112. CrossRefPubMedPubMedCentralGoogle Scholar
  48. Gonçalves ER, Hara H, Miyazawa D et al (2006) Transcriptomic assessment of isozymes in the biphenyl pathway of Rhodococcus sp. strain RHA1. Appl Environ Microbiol 72:6183–6193PubMedPubMedCentralCrossRefGoogle Scholar
  49. Goodfellow M, Alderson G, Chun J (1998) Rhodococcal systematics: problems and developments. Antonie Van Leeuwenhoek 74:3–20PubMedCrossRefGoogle Scholar
  50. Goordial J, Raymond-Bouchard I, Zolotarov Y et al (2016) Cold adaptive traits revealed by comparative genomic analysis of the eurypsychrophile Rhodococcus sp. JG3 isolated from high elevation McMurdo Dry Valley permafrost, Antarctica. FEMS Microbiol Ecol 92.
  51. Goris J, Konstantinidis KT, Klappenbach JA (2007) DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 57:81–91PubMedCrossRefGoogle Scholar
  52. Gravouil K, Ferru-Clément R, Colas S et al (2017) Transcriptomics and lipidomics of the environmental strain Rhodococcus ruber point out consumption pathways and potential metabolic bottlenecks for polyethylene degradation. Environ Sci Technol 51:5172–5181. CrossRefPubMedGoogle Scholar
  53. Grӧning JAD, Eulberg D, Tischler D et al (2014) Gene redundancy of two-component (chloro)phenol hydroxylases in Rhodococcus opacus 1CP. FEMS Microbiol Lett 361:68–75CrossRefGoogle Scholar
  54. Grzeszik C, Lubbers M, Reh M et al (1997) Genes encoding the NAD-reducing hydrogenase of Rhodococcus opacus MR11. Microbiology 143:1271–1286PubMedPubMedCentralCrossRefGoogle Scholar
  55. Guo C, Wu ZL (2017) Construction and functional analysis of a whole-cell biocatalyst based on CYP108N7. Enzym Microb Technol 106:28–34CrossRefGoogle Scholar
  56. Gürtler V, Mayall BC, Seviour R (2004) Can whole genome analysis refine the taxonomy of the genus Rhodococcus? FEMS Microbiol Rev 28:377–403PubMedPubMedCentralCrossRefGoogle Scholar
  57. Hara H, Eltis LD, Davies JE et al (2007) Transcriptomic analysis reveals a bifurcated terephthalate degradation pathway in Rhodococcus sp. strain RHA1. J Bacteriol 189:1641–1647PubMedCrossRefGoogle Scholar
  58. Hernández MA, Mohn WW, Martínez E et al (2008) Biosynthesis of storage compounds by Rhodococcus jostii RHA1 and global identification of genes involved in their metabolism. BMC Genomics 9:600. CrossRefPubMedPubMedCentralGoogle Scholar
  59. Hirasawa K, Ishii Y, Kobayashi M et al (2001) Improvement of desulfurization activity in Rhodococcus erythropolis KA2-5-1 by genetic engineering. Biosci Biotechnol Biochem 65:239–246PubMedCrossRefPubMedCentralGoogle Scholar
  60. Holder JW, Ulrich JC, DeBono AC et al (2011) Comparative and functional genomics of Rhodococcus opacus PD630 for biofuels development. PLoS Genet 7(9):e1002219. CrossRefPubMedPubMedCentralGoogle Scholar
  61. Honda K, Yamashita S, Nakagawa H et al (2008) Stabilization of water-in-oil emulsion by Rhodococcus opacus B-4 and its application to biotransformation. Appl Microbiol Biotechnol 78:767–773PubMedCrossRefGoogle Scholar
  62. Honda K, Imura M, Okano K et al (2012) Identification of replication region of a 111-kb circular plasmid from Rhodococcus opacus B-4 by λ red recombination-based deletion analysis. Biosci Biotechnol Biochem 76:1758–1764PubMedCrossRefGoogle Scholar
  63. Hori K, Kobayashi A, Ikeda H et al (2009) Rhodococcus aetherivorans IAR1, a new bacterial strain synthesizing poly(3-hydroxybutyrate-co-3-hydroxyvalerate) from toluene. J Biosci Bioeng 107:145–150PubMedCrossRefGoogle Scholar
  64. Hülter N, Ilhan J, Wein T et al (2017) An evolutionary perspective on plasmid lifestyle modes. Curr Opin Microbiol 38:74–80PubMedCrossRefGoogle Scholar
  65. 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 78:341–352PubMedCrossRefGoogle Scholar
  66. Iwasaki T, Miyauchi K, Masai E et al (2006) Multiple-subunit genes of the aromatic-ring-hydroxylating dioxygenase play an active role in biphenyl and polychlorinated biphenyl degradation in Rhodococcus sp. strain RHA1. Appl Environ Microbiol 72:5396–5402PubMedPubMedCentralCrossRefGoogle Scholar
  67. Iwasaki T, Takeda H, Miyauchi K et al (2007) Characterization of two biphenyl dioxygenases for biphenyl/PCB degradation in a PCB degrader, Rhodococcus sp. strain RHA1. Biosci Biotechnol Biochem 71:993–1002PubMedCrossRefGoogle Scholar
  68. Kalkus J, Dorrie C, Fischer D et al (1993) The giant linear plasmid pHG207 from Rhodococcus sp. encoding hydrogen autotrophy: characterization of the plasmid and its termini. J Gen Microbiol 139:2055–2065PubMedCrossRefGoogle Scholar
  69. Kalscheuer R, Arenskötter M, Steinbüchel A (1999) Establishment of a gene transfer system for Rhodococcus opacus PD630 based on electroporation and its application for recombinant biosynthesis of poly(3-hydroxyalkanoic acids). Appl Microbiol Biotechnol 52:508–515PubMedCrossRefGoogle Scholar
  70. Khairy H, Meinert C, Wübbeler JH et al (2016) Genome and proteome analysis of Rhodococcus erythropolis MI2: elucidation of the 4,4′-dithiodibutyric acid catabolism. PLoS One 11(12):e0167539. CrossRefPubMedPubMedCentralGoogle Scholar
  71. Kikuchi Y, Hirai K, Gunge N et al (1985) Hairpin plasmid-a novel linear DNA of perfect hairpin structure. EMBO J 4:1881–1886PubMedPubMedCentralCrossRefGoogle Scholar
  72. Kim D, Kim YS, Kim SK et al (2002) Monocyclic aromatic hydrocarbon degradation by Rhodococcus sp. strain DK17. Appl Environ Microbiol 6:3270–3278CrossRefGoogle Scholar
  73. Kim D, Choi KY, Yoo M (2018) Biotechnological potential of Rhodococcus biodegradative pathways. J Microbiol Biotechnol 28(7):1037–1051PubMedPubMedCentralGoogle Scholar
  74. Konig C, Eulberg D, Groning J et al (2004) A linear megaplasmid, p1CP, carrying the genes for chlorocatechol catabolism of Rhodococcus opacus 1CP. Microbiology 150:3075–3087PubMedCrossRefGoogle Scholar
  75. Konishi M, Nishi S, Fukuoka T et al (2014) Deep-sea Rhodococcus sp. BS-15, lacking the phytopathogenic fas genes, produces a novel glucotriose lipid biosurfactant. Mar Biotechnol 16:484–493PubMedCrossRefGoogle Scholar
  76. Konstantinidis KT, Tiedje JM (2005) Towards a genome-based taxonomy for prokaryotes. J Bacteriol 187:6258–6264. CrossRefPubMedPubMedCentralGoogle Scholar
  77. Kosono S, Maeda M, Fuji F et al (1997) Three of the seven bphC genes of Rhodococcus erythropolis TA421, isolated from a termite ecosystem, are located on an indigenous plasmid associated with biphenyl degradation. Appl Environ Microbiol 63:3282–3285PubMedPubMedCentralGoogle Scholar
  78. Kostichka K, Tao L, Bramucci M et al (2003) A small cryptic plasmid from Rhodococcus erythropolis: characterization and utility for gene expression. Appl Microbiol Biotechnol 62:61–68PubMedCrossRefGoogle Scholar
  79. Kulakov LA, Larkin MJ (2002) Genomic organization of Rhodococcus. In: Danchin A (ed) Genomics of GC-rich gram-positive bacteria. Caister Academic Press, Norfolk, pp 15–46Google Scholar
  80. Kulakov LA, Larkin MJ, Kulakova AN (1997) Cryptic plasmid pKA22 isolated from the naphthalene degrading derivative of Rhodococcus rhodochrous NCIMB13064. Plasmid 38:61–69PubMedCrossRefPubMedCentralGoogle Scholar
  81. Kulakov LA, Chen S, Allen CC et al (2005) Web-type evolution of Rhodococcus gene clusters associated with utilization of naphthalene. Appl Environ Microbiol 71:1754–1764PubMedPubMedCentralCrossRefGoogle Scholar
  82. Kulakova AN, Stafford TM, Larkin MJ et al (1995) Plasmid pRTL1 controlling 1-chloroalkane degradation by Rhodococcus rhodochrous NCIMB13064. Plasmid 33:208–217PubMedCrossRefPubMedCentralGoogle Scholar
  83. Kwasiborski A, Mondy S, Teik-Min C et al (2015) Core genome and plasmidome of the quorum-quenching bacterium Rhodococcus erythropolis. Genetica 143:253–261PubMedCrossRefPubMedCentralGoogle Scholar
  84. Laczi K, Kis A, Horváth B et al (2015) Metabolic responses of Rhodococcus erythropolis PR4 grown on diesel oil and various hydrocarbons. Appl Microbiol Biotechnol 99:9745–9759PubMedCrossRefPubMedCentralGoogle Scholar
  85. Larkin MJ, DeMot R, Kulakov LA et al (1998) Applied aspects of Rhodococcus genetics. Antonie Van Leeuwenhoek 74:133–153PubMedCrossRefPubMedCentralGoogle Scholar
  86. Larkin MJ, Kulakov LA, Allen CCR (2010) Genomes and plasmids in Rhodococcus. In: Alvarez HM (ed) Biology of Rhodococcus. Springer, Berlin, pp 73–90CrossRefGoogle Scholar
  87. LeBlanc JC, Gonçalves ER, Mohn WW (2008) Global response to desiccation stress in the soil actinomycete Rhodococcus jostii RHA1. Appl Environ Microbiol 74:2627–2636PubMedPubMedCentralCrossRefGoogle Scholar
  88. Letek M, González P, MacArthur I et al (2010) The genome of a pathogenic Rhodococcus: cooptive virulence underpinned by key gene acquisitions. PLoS Genet 6(9):e1001145. CrossRefPubMedPubMedCentralGoogle Scholar
  89. Martìnkovà L, Uhnàkovà B, Pàtek M et al (2009) Biodegradation potential of the genus Rhodococcus. Environ Int 35:162–177PubMedCrossRefGoogle Scholar
  90. Matsui T, Saeki H, Shinzato N et al (2006) Characterization of RhodococcusE. coli shuttle vector pNC9501 constructed from the cryptic plasmid of a propene-degrading bacterium. Curr Microbiol 52:445–448PubMedCrossRefPubMedCentralGoogle Scholar
  91. McLeod MP, Warren RL, Hsiao WW et al (2006) The complete genome of Rhodococcus sp. RHA1 provides insights into a catabolic powerhouse. Proc Natl Acad Sci U S A 103(42):15582–15587PubMedPubMedCentralCrossRefGoogle Scholar
  92. Meinhardt F, Schaffrath R, Larsen M (1997) Microbial linear plasmids. Appl Microbiol Biotechnol 47:329–336PubMedCrossRefPubMedCentralGoogle Scholar
  93. Moran NA (2002) Microbial minimalism: genome reduction in bacterial pathogens. Cell 108:583–586PubMedCrossRefPubMedCentralGoogle Scholar
  94. Na K, Kuroda A, Takiguchia N (2005) Isolation and characterization of benzene-tolerant Rhodococcus opacus strains. J Biosci Bioeng 99:378–382PubMedCrossRefPubMedCentralGoogle Scholar
  95. Nakashima N, Tamura T (2004a) A novel system for expressing recombinant proteins over a wide temperature range from 4 to 35°C. Biotechnol Bioeng 86:136–148PubMedCrossRefPubMedCentralGoogle Scholar
  96. Nakashima N, Tamura T (2004b) Isolation and characterization of a rolling-circle-type plasmid from Rhodococcus erythropolis and application of the plasmid to multiple-recombinant-protein expression. Appl Environ Microbiol 70:5557–5568PubMedPubMedCentralCrossRefGoogle Scholar
  97. National Center for Biotechnology Information (NCBI) (2018) U.S. National Library of Medicine, Rockville Pike. Accessed July 2018
  98. Orro A, Cappelletti M, D’Ursi P et al (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(10):e0139467. CrossRefPubMedPubMedCentralGoogle Scholar
  99. Pathak A, Chauhan A, Blom J et al (2016) Comparative genomics and metabolic analysis reveals peculiar characteristics of Rhodococcus opacus strain M213 particularly for naphthalene degradation. PLoS One 17:1–32Google Scholar
  100. Patrauchan MA, Florizone C, Dosanjh M et al (2005) Catabolism of benzoate and phthalate in Rhodococcus sp. strain RHA1: redundancies and convergence. J Bacteriol 187:4050–4063PubMedPubMedCentralCrossRefGoogle Scholar
  101. Patrauchan MA, Florizone C, Eapen S et al (2008) Roles of ring-hydroxylating dioxygenases in styrene and benzene catabolism in Rhodococcus jostii RHA1. J Bacteriol 190(1):37–47PubMedPubMedCentralCrossRefGoogle Scholar
  102. Patrauchan MA, Miyazawa D, LeBlanc JC et al (2012) Proteomic analysis of survival of Rhodococcus jostii RHA1 during carbon starvation. Appl Environ Microbiol 78(18):6714–6725PubMedPubMedCentralCrossRefGoogle Scholar
  103. Pérez-Pérez JM, Candela H, Micol JL (2009) Understanding synergy in genetic interactions. Trends Genet 8:368–376CrossRefGoogle Scholar
  104. Petrusma M, Hessels G, Dijkhuizen L et al (2011) Multiplicity of 3-ketosteroid-9α-hydroxylase enzymes in Rhodococcus rhodochrous DSM43269 for specific degradation of different classes of steroids. J Bacteriol 193(15):3931–3940. CrossRefPubMedPubMedCentralGoogle Scholar
  105. Presentato A, Piacenza E, Anikovskiy M et al (2016) Rhodococcus aetherivorans BCP1 as cell factory for the production of intracellular tellurium nanorods under aerobic conditions. Microb Cell Factories 15:204. CrossRefGoogle Scholar
  106. Presentato A, Cappelletti M, Sansone A et al (2018a) Aerobic growth of Rhodococcus aetherivorans BCP1 using selected naphthenic acids as the sole carbon and energy sources. Front Microbiol 9:672. CrossRefPubMedPubMedCentralGoogle Scholar
  107. Presentato A, Piacenza E, Anikovskiy M et al (2018b) Biosynthesis of selenium-nanoparticles and -nanorods as a product of selenite bioconversion by the aerobic bacterium Rhodococcus aetherivorans BCP1. New Biotechnol 41:1–8CrossRefGoogle Scholar
  108. Presentato A, Piacenza E, Darbandi A et al (2018c) Assembly, growth and conductive properties of tellurium nanorods produced by Rhodococcus aetherivorans BCP1. Sci Rep 8:3923. CrossRefPubMedPubMedCentralGoogle Scholar
  109. Priefert H, O’Brien XM, Lessard PA et al (2004) Indene bioconversion by a toluene inducible dioxygenase of Rhodococcus sp. I24. Appl Microbiol Biotechnol 65:168–176PubMedCrossRefPubMedCentralGoogle Scholar
  110. Puglisi E, Cahill MJ, Lessard PA et al (2010) Transcriptional response of Rhodococcus aetherivorans I24 to polychlorinated biphenyl-contaminated sediments. Microb Ecol 60(3):505–515. CrossRefPubMedGoogle Scholar
  111. Qu J, Miao L-L, Liu Y et al (2015) Complete genome sequence of Rhodococcus sp. Strain IcdP1 shows diverse catabolic potential. Genome Announc 3(4):e00711-15. CrossRefPubMedPubMedCentralGoogle Scholar
  112. Radeck J, Kraft K, Bartels J (2013) The Bacillus BioBrick Box: generation and evaluation of essential genetic building blocks for standardized work with Bacillus subtilis. J Biol Eng 7:29PubMedPubMedCentralCrossRefGoogle Scholar
  113. Redenbach M, Altenbuchner J (2002) Why do some bacteria have linear chromosomes and plasmids. BIOspektrum 8:158–163Google Scholar
  114. Richter M, Rosselló-Móra R (2009) Shifting the genomic gold standard for the prokaryotic species definition. Proc Natl Acad Sci U S A 106:19126–19131PubMedPubMedCentralCrossRefGoogle Scholar
  115. Rodrigues JLM, Maltseva OV, Tsoi TV et al (2001) Development of a Rhodococcus recombinant strain for degradation of products from anaerobic dechlorination of PCBs. Environ Sci Technol 35:663–668PubMedCrossRefGoogle Scholar
  116. Sallam KI, Mitani Y, Tamura T (2006) Construction of random transposition mutagenesis system in Rhodococcus erythropolis using IS1415. J Biotechnol 121:13–22PubMedCrossRefGoogle Scholar
  117. Sameshima Y, Honda K, Kato J et al (2008) Expression of Rhodococcus opacus alkB genes in anhydrous organic solvents. J Biosci Bioeng 106:199–203CrossRefGoogle Scholar
  118. Sangal V, Jones AL, Goodfellow M et al (2014) Comparative genomic analyses reveal a lack of a substantial signature of host adaptation in Rhodococcus equi (“Prescottella equi”). Pathog Dis 71:352–356PubMedCrossRefGoogle Scholar
  119. Sekine M, Tanikawa S, Omata S et al (2006) Sequence analysis of three plasmids harboured in Rhodococcus erythropolis strain PR4. Environ Microbiol 8:334–346PubMedCrossRefGoogle Scholar
  120. Sekizaki T, Tanoue T, Osaki M (1998) Improved electroporation of Rhodococcus equi. J Vet Med Sci 60:277–279PubMedCrossRefPubMedCentralGoogle Scholar
  121. Shao Z, Dick WA, Behki RM (1995) An improved Escherichia coli – Rhodococcus shuttle vector and plasmid transformation in Rhodococcus spp. using electroporation. Lett Appl Microbiol 21:261–266PubMedCrossRefPubMedCentralGoogle Scholar
  122. Sheng HM, Gao HS, Xue LG et al (2011) Analysis of the composition and characteristics of culturable endophytic bacteria within subnival plants of the Tianshan Mountains, northwestern China. Curr Microbiol 62:923–932PubMedCrossRefPubMedCentralGoogle Scholar
  123. Shevtsov A, Tarlykov P, Zholdybayeva E et al (2013) Draft genome sequence of Rhodococcus erythropolis DN1, a crude oil biodegrader. Genome Announc 1:e00846–e00813. CrossRefPubMedPubMedCentralGoogle Scholar
  124. Shimizu S, Kobayashi H, Masai E et al (2001) Characterization of the 450-kb linear plasmid in a polychlorinated biphenyl degrader, Rhodococcus sp. strain RHA1. Appl Environ Microbiol 67:2021–2028PubMedPubMedCentralCrossRefGoogle Scholar
  125. Singer ME, Finnerty WR (1988) Construction of an Escherichia coliRhodococcus shuttle vector and plasmid transformation in Rhodococcus spp. J Bacteriol 170:638–645PubMedPubMedCentralCrossRefGoogle Scholar
  126. Swain K, Casabon I, Eltis LD et al (2012) Two transporters essential for the reassimilation of novel cholate metabolites by Rhodococcus jostii RHA1. J Bacteriol 194(24):6720–6727PubMedPubMedCentralCrossRefGoogle Scholar
  127. Szőköl J, Rucká L, Šimčíková M et al (2014) Induction and carbon catabolite repression of phenol degradation genes in Rhodococcus erythropolis and Rhodococcus jostii. Appl Microbiol Biotechnol 98:8267–8279PubMedCrossRefPubMedCentralGoogle Scholar
  128. Taguchi K, Motoyama M, Kudo T (2004) Multiplicity of 2, 3-dihydroxybiphenyl dioxygenase genes in the Gram-positive polychlorinated biphenyl degrading bacterium Rhodococcus rhodochrous K37. Biosci Biotechnol Biochem 68:787–795PubMedCrossRefPubMedCentralGoogle Scholar
  129. Taguchi K, Motoyama M, Iida T et al (2007) Polychlorinated biphenyl/biphenyl degrading gene clusters in Rhodococcus sp. K37, HA99, and TA431 are different from well-known bph gene clusters of rhodococci. Biosci Biotechnol Biochem 71:1136–1144PubMedCrossRefPubMedCentralGoogle Scholar
  130. Tajparast M, Frigon D (2015) Genome-scale metabolic model of Rhodococcus jostii RHA1 (iMT1174) to study the accumulation of storage compounds during nitrogen-limited condition. BMC Syst Biol 9:43. PubMedPubMedCentralCrossRefGoogle Scholar
  131. Tajparast M, Frigon D, Virolle MJ (2018) Predicting the accumulation of storage compounds by Rhodococcus jostii RHA1 in the feast-famine growth cycles using genome-scale flux balance analysis. PLoS One 13:e0191835. PubMedPubMedCentralCrossRefGoogle Scholar
  132. Takeda H, Shimodaira J, Yukawa K et al (2010) Dual two-component regulatory systems are involved in aromatic compound degradation in a polychlorinated-biphenyl degrader, Rhodococcus jostii RHA1. J Bacteriol 192:4741–4751PubMedPubMedCentralCrossRefGoogle Scholar
  133. Takei D, Washio K, Morikawa M (2008) Identification of alkane hydroxylase genes in Rhodococcus sp. strain TMP2 that degrades a branched alkane. Biotechnol Lett 30:1447–1452PubMedCrossRefPubMedCentralGoogle Scholar
  134. Taketani RG, Zucchi TD, Soares de Melo I et al (2013) Whole-genome shotgun sequencing of Rhodococcus erythropolis strain P27, a highly radiation-resistant actinomycete from Antarctica. Genome Announc 1(5):e00763–e00713. CrossRefGoogle Scholar
  135. Táncsics A, Benedek T, Szoboszlay S et al (2015) The detection and phylogenetic analysis of the alkane 1-monooxygenase gene of members of the genus Rhodococcus. Syst Appl Microbiol 38:1–7PubMedCrossRefPubMedCentralGoogle Scholar
  136. Tao F, Zhao P, Li Q et al (2011) Genome sequence of Rhodococcus erythropolis XP, a biodesulfurizing bacterium with industrial potential. J Bacteriol 193:6422–6423PubMedPubMedCentralCrossRefGoogle Scholar
  137. Tomás-Gallardo L, Canosa I, Santero E et al (2006) Proteomic and transcriptional characterization of aromatic degradation pathways in Rhodococcus sp. strain TFB. Proteomics 6:S119–S132. CrossRefPubMedGoogle Scholar
  138. Treadway SL, Yanagimachi KS, Lankenau E (1999) Isolation and characterization of indene bioconversion genes from Rhodococcus strain I24. Appl Microbiol Biotechnol 51:786–793PubMedCrossRefGoogle Scholar
  139. Valero-Rello A, Hapeshi A, Anastasi E et al (2015) An invertron-like linear plasmid mediates intracellular survival and virulence in bovine isolates of Rhodococcus equi. Infect Immun 83:2725–2737. CrossRefPubMedPubMedCentralGoogle Scholar
  140. Van Beilen JB, Smits THM, Whyte LG et al (2002) Alkane hydroxylase homologues in gram-positive strains. Environ Microbiol 4:676–682PubMedCrossRefPubMedCentralGoogle Scholar
  141. Van der Geize, Dijkhuize L (2004) Harnessing the catabolic diversity of rhodococci for environmental and biotechnological applications. Curr Opin Microbiol 7:255–261PubMedPubMedCentralCrossRefGoogle Scholar
  142. Van der Geize R, Hessels GI, van Gerwen R (2001) Unmarked gene deletion mutagenesis of kstD, encoding 3-ketosteroid Δ1-dehydrogenase, in Rhodococcus erythropolis SQ1 using sacB as counters electable marker. FEMS Microbiol Lett 205:197–202PubMedCrossRefGoogle Scholar
  143. Van der Geize R, Yam K, Heuser T et al (2007) A gene cluster encoding cholesterol catabolism in a soil actinomycete provides insight into Mycobacterium tuberculosis survival in macrophages. Proc Natl Acad Sci U S A 104:1947–1952PubMedPubMedCentralCrossRefGoogle Scholar
  144. Van der Geize R, de Jong W, Hessels GI et al (2008) A novel method to generate unmarked gene deletions in the intracellular pathogen Rhodococcus equi using 5-fluorocytosine conditional lethality. Nucleic Acids Res 36:e151PubMedPubMedCentralCrossRefGoogle Scholar
  145. Venkataraman H, Evelien MP, Rosłoniec KZ et al (2015) Biosynthesis of a steroid metabolite by an engineered Rhodococcus erythropolis strain expressing a mutant cytochrome P450 BM3 enzyme. Appl Microbiol Biotechnol 99:4713–4721PubMedCrossRefGoogle Scholar
  146. Ventura M, Canchaya C, Tauch A et al (2007) Genomics of Actinobacteria: tracing the evolutionary history of an ancient phylum. Microbiol Mol Biol Rev 71:495–548PubMedPubMedCentralCrossRefGoogle Scholar
  147. Vick J, Johnson E, Choudhary S et al (2011) Optimized compatible set of BioBrick™ vectors for metabolic pathway engineering. Appl Microbiol Biotechnol 92:1275–1286PubMedCrossRefGoogle Scholar
  148. Villalba MS, Hernandéz MA, Silva RA et al (2013) Genome sequences of triacylglycerol metabolism in Rhodococcus as a platform for comparative genomics. J Mol Biochem 2:94–105Google Scholar
  149. Volff JN, Altenbuchner J (2000) A new beginning with new ends: linearization of circular chromosomes during bacterial evolution. FEMS Microbiol Lett 186:143–150. CrossRefPubMedGoogle Scholar
  150. Voss I, Steinbuchel A (2001) High cell density cultivation of Rhodococcus opacus for lipid production at a pilot-plant scale. Appl Microbiol Biotechnol 55:547–555CrossRefGoogle Scholar
  151. Warren R, Hsiao WW, Kudo H et al (2004) Functional characterization of a catabolic plasmid from polychlorinated-biphenyl degrading Rhodococcus sp. strain RHA1. J Bacteriol 186:7783–7795PubMedPubMedCentralCrossRefGoogle Scholar
  152. Watcharakul S, Röther W, Birke J (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 16:92. CrossRefPubMedPubMedCentralGoogle Scholar
  153. Whyte LG, Smits THM, Labbe’ D et al (2002) Gene cloning and characterization of multiple alkane hydroxylase systems in Rhodococcus strains Q15 and NRRL B-16531. Appl Environ Microbiol 68:5933–5942PubMedPubMedCentralCrossRefGoogle Scholar
  154. Xiong X, Wang X, Chen S (2012) Engineering of a xylose metabolic pathway in Rhodococcus strains. Appl Environ Microbiol 78(16):5483–5491. CrossRefPubMedPubMedCentralGoogle Scholar
  155. Xiong X, Lian J, Yu X et al (2016) Engineering levoglucosan metabolic pathway in Rhodococcus jostii RHA1 for lipid production. J Ind Microbiol Biotechnol 43:1551–1560PubMedCrossRefGoogle Scholar
  156. Xu JL, He J, Wang ZC et al (2007) Rhodococcus qingshengii sp. nov., a carbendazim-degrading bacterium. Int J Syst Evol Microbiol 57:2754–2757PubMedCrossRefGoogle Scholar
  157. Zampolli J, Collina E, Lasagni M et al (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 4:73PubMedPubMedCentralCrossRefGoogle Scholar
  158. Zhang J (2012) Genetic redundancies and their evolutionary maintenance. Evol Syst Biol 751:279–300CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Martina Cappelletti
    • 1
    Email author
  • Jessica Zampolli
    • 2
  • Patrizia Di Gennaro
    • 2
  • Davide Zannoni
    • 1
  1. 1.Department of Pharmacy and BiotechnologyUniversity of BolognaBolognaItaly
  2. 2.Department of Biotechnology and BiosciencesUniversity of Milano-BicoccaMilanItaly

Personalised recommendations