1887

Abstract

The complete genome sequence of sp. WAY2 (WAY2) consists of a circular chromosome, three linear replicons and a small circular plasmid. The linear replicons contain typical actinobacterial invertron-type telomeres with the central CGTXCGC motif. Comparative phylogenetic analysis of the 16S rRNA gene along with phylogenomic analysis based on the genome-to-genome distance phylogeny (GBDP) algorithm and digital DNA–DNA hybridization (dDDH) with other type strains resulted in a clear differentiation of WAY2, which is likely a new species. The genome of WAY2 contains five distinct clusters of , and genes, putatively involved in the degradation of several aromatic compounds. These clusters are distributed throughout the linear plasmids. The high sequence homology of the ring-hydroxylating subunits of these systems with other known enzymes has allowed us to model the range of aromatic substrates they could degrade. Further functional characterization revealed that WAY2 was able to grow with biphenyl, naphthalene and xylene as sole carbon and energy sources, and could oxidize multiple aromatic compounds, including ethylbenzene, phenanthrene, dibenzofuran and toluene. In addition, WAY2 was able to co-metabolize 23 polychlorinated biphenyl congeners, consistent with the five different ring-hydroxylating systems encoded by its genome. WAY2 could also use -alkanes of various chain-lengths as a sole carbon source, probably due to the presence of and gene copies, which are only found in its chromosome. These results show that WAY2 has a potential to be used for the biodegradation of multiple organic compounds.

Funding
This study was supported by the:
  • Ondrej Uhlik , Grantová Agentura České Republiky , (Award 17-00227S)
  • Marta Martin , Ministerio de Ciencia, Innovación y Universidades , (Award RTI2018-0933991-B-I00)
  • Rafael Rivilla , H2020 LEIT Biotechnology , (Award 826312)
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2020-06-04
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References

  1. Sharma S, Pant A. Crude oil degradation by a marine actinomycete Rhodococcus sp. Indian J Mar Sci 2001; 30:146–150
    [Google Scholar]
  2. Ruberto LAM, Vazquez S, Lobalbo A, Mac Cormack WP. Psychrotolerant hydrocarbon-degrading Rhodococcus strains isolated from polluted Antarctic soils. Antarct Sci 2005; 17:47–56 [CrossRef]
    [Google Scholar]
  3. Röttig A, Hauschild P, Madkour MH, Al-Ansari AM, Almakishah NH et al. Analysis and optimization of triacylglycerol synthesis in novel oleaginous Rhodococcus and Streptomyces strains isolated from desert soil. J Biotechnol 2016; 225:48–56 [CrossRef]
    [Google Scholar]
  4. Prescott JF. Rhodococcus equi: an animal and human pathogen. Clin Microbiol Rev 1991; 4:20–34 [CrossRef]
    [Google Scholar]
  5. Cornelis K, Ritsema T, Nijsse J, Holsters M, Goethals K et al. The plant pathogen Rhodococcus fascians colonizes the exterior and interior of the aerial parts of plants. Mol Plant Microbe Interact 2001; 14:599–608 [CrossRef]
    [Google Scholar]
  6. Yassin AF. Rhodococcus triatomae sp. nov., isolated from a blood-sucking bug. Int J Syst Evol Microbiol 2005; 55:1575–1579 [CrossRef]
    [Google Scholar]
  7. Kästner M, Breuer-Jammali M, Mahro B. Enumeration and characterization of the soil microflora from hydrocarbon-contaminated soil sites able to mineralize polycyclic aromatic hydrocarbons (PAH). Appl Microbiol Biotechnol 1994; 41:267–273 [CrossRef]
    [Google Scholar]
  8. Ghosh A, Paul D, Prakash D, Mayilraj S, Jain RK. Rhodococcus imtechensis sp. nov., a nitrophenol-degrading actinomycete. Int J Syst Evol Microbiol 2006; 56:1965–1969 [CrossRef]
    [Google Scholar]
  9. Jiménez N, Viñas M, Bayona JM, Albaiges J, Solanas AM. The Prestige oil spill: bacterial community dynamics during a field biostimulation assay. Appl Microbiol Biotechnol 2007; 77:935–945 [CrossRef]
    [Google Scholar]
  10. Song X, Xu Y, Li G, Zhang Y, Huang T et al. Isolation, characterization of Rhodococcus sp. P14 capable of degrading high-molecular-weight polycyclic aromatic hydrocarbons and aliphatic hydrocarbons. Mar Pollut Bull 2011; 62:2122–2128 [CrossRef]
    [Google Scholar]
  11. Shimizu S, Kobayashi H, Masai E, Fukuda M. Characterization of the 450-kb linear plasmid in a polychlorinated biphenyl degrader, Rhodococcus sp. strain RHA1. Appl Environ Microbiol 2001; 67:2021–2028 [CrossRef]
    [Google Scholar]
  12. McLeod MP, Warren RL, Hsiao WWL, Araki N, Myhre M et al. The complete genome of Rhodococcus sp. RHA1 provides insights into a catabolic powerhouse. Proc Natl Acad Sci USA 2006; 103:15582–15587 [CrossRef]
    [Google Scholar]
  13. Carvalho CCCR, Fonseca MMR. Degradation of hydrocarbons and alcohols at different temperatures and salinities by Rhodococcus erythropolis DCL14. FEMS Microbiol Ecol 2005; 51:389–399 [CrossRef]
    [Google Scholar]
  14. Iwasaki T, Takeda H, Miyauchi K, Yamada T, Masai E et al. Characterization of two biphenyl dioxygenases for biphenyl/PCB degradation in a PCB degrader, Rhodococcus sp. strain RHA1. Biosci Biotechnol Biochem 2007; 71:993–1002 [CrossRef]
    [Google Scholar]
  15. Behki R, Topp E, Dick W, Germon P. Metabolism of the herbicide atrazine by Rhodococcus strains. Appl Environ Microbiol 1993; 59:1955–1959 [CrossRef]
    [Google Scholar]
  16. Alvarez AF, Alvarez HM, Kalscheuer R, Wältermann M, Steinbüchel A. Cloning and characterization of a gene involved in triacylglycerol biosynthesis and identification of additional homologous genes in the oleaginous bacterium Rhodococcus opacus PD630. Microbiology 2008; 154:2327–2335 [CrossRef]
    [Google Scholar]
  17. Hernández MA, Mohn WW, Martínez E, Rost E, Alvarez AF et al. Biosynthesis of storage compounds by Rhodococcus jostii RHA1 and global identification of genes involved in their metabolism. BMC Genomics 2008; 9:600 [CrossRef]
    [Google Scholar]
  18. Goordial J, Raymond-Bouchard I, Zolotarov Y, de Bethencourt L, Ronholm J et al. 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 2016; 92:fiv154
    [Google Scholar]
  19. Larkin MJ, Kulakov LA, Allen CC. Genomes and plasmids in Rhodococcus . In: Biology of Rhodococcus Berlin and Heidleberg: Springer; 2010 pp 73–90
    [Google Scholar]
  20. Larkin MJ, Kulakov LA, Allen CCR. Biodegradation and Rhodococcus – masters of catabolic versatility. Curr Opin Biotechnol 2005; 16:282–290 [CrossRef]
    [Google Scholar]
  21. diCenzo GC, Finan TM. The divided bacterial genome: structure, function, and evolution. Microbiol Mol Biol Rev 2017; 81:e00019-17 [CrossRef]
    [Google Scholar]
  22. Chen CW, Huang C-H, Lee H-H, Tsai H-H, Kirby R. Once the circle has been broken: dynamics and evolution of Streptomyces chromosomes. Trends Genet 2002; 18:522–529 [CrossRef]
    [Google Scholar]
  23. Iwasaki T, Miyauchi K, Masai E, Fukuda M. 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 2006; 72:5396–5402 [CrossRef]
    [Google Scholar]
  24. Kimura N, Kitagawa W, Mori T, Nakashima N, Tamura T et al. Genetic and biochemical characterization of the dioxygenase involved in lateral dioxygenation of dibenzofuran from Rhodococcus opacus strain SAO101. Appl Microbiol Biotechnol 2006; 73:474–484 [CrossRef]
    [Google Scholar]
  25. Taguchi K, Motoyama M, Iida T, Kudo T. 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 2007; 71:1136–1144 [CrossRef]
    [Google Scholar]
  26. Resnick SM, Lee K, Gibson DT. Diverse reactions catalyzed by naphthalene dioxygenase from Pseudomonas sp strain NCIB 9816. J Ind Microbiol Biotechnol 1996; 17:438–457 [CrossRef]
    [Google Scholar]
  27. Furukawa K, Suenaga H, Goto M. Biphenyl dioxygenases: functional versatilities and directed evolution. J Bacteriol 2004; 186:5189–5196 [CrossRef]
    [Google Scholar]
  28. Patrauchan MA, Florizone C, Eapen S, Gomez-Gil L, Sethuraman B et al. Roles of ring-hydroxylating dioxygenases in styrene and benzene catabolism in Rhodococcus jostii RHA1. J Bacteriol 2008; 190:37–47 [CrossRef]
    [Google Scholar]
  29. Cavalca L, Colombo M, Larcher S, Gigliotti C, Collina E et al. Survival and naphthalene-degrading activity of Rhodococcus sp. strain 1BN in soil microcosms. J Appl Microbiol 2002; 92:1058–1065 [CrossRef]
    [Google Scholar]
  30. Kim J-D, Lee C-G. Microbial degradation of polycyclic aromatic hydrocarbons in soil by bacterium-fungus co-cultures. Biotechnol Bioprocess Engineer 2007; 12:410–416 [CrossRef]
    [Google Scholar]
  31. Kitova AE, Kuvichkina TN, Arinbasarova AY, Reshetilov AN. Degradation of 2,4-dinitrophenol by free and immobilized cells of Rhodococcus erythropolis HL PM-1. Appl Biochem Microbiol 2004; 40:258–261 [CrossRef]
    [Google Scholar]
  32. Krivoruchko A, Kuyukina M, Ivshina I. Advanced Rhodococcus biocatalysts for environmental biotechnologies. Catalysts 2019; 9:236 [CrossRef]
    [Google Scholar]
  33. Ivshina IB, Vikhareva EV, Richkova MI, Mukhutdinova AN, Karpenko JN. Biodegradation of drotaverine hydrochloride by free and immobilized cells of Rhodococcus rhodochrous IEGM 608. World J Microbiol Biotechnol 2012; 28:2997–3006 [CrossRef]
    [Google Scholar]
  34. Hernández MA, Comba S, Arabolaza A, Gramajo H, Alvarez HM. Overexpression of a phosphatidic acid phosphatase type 2 leads to an increase in triacylglycerol production in oleaginous Rhodococcus strains. Appl Microbiol Biotechnol 2015; 99:2191–2207 [CrossRef]
    [Google Scholar]
  35. Thakur N, Kumar V, Sharma NK, Thakur S, Bhalla TC. Aliphatic amidase of Rhodococcus rhodochrous PA-34: purification, characterization and application in synthesis of acrylic acid. Protein Pept Lett 2016; 23:152–158 [CrossRef][PubMed]
    [Google Scholar]
  36. Adnani N, Braun DR, McDonald BR, Chevrette MG, Currie CR et al. Complete genome sequence of Rhodococcus sp. strain WMMA185, a marine sponge-associated bacterium. Genome Announc 2016; 4:e01406-16 [CrossRef]
    [Google Scholar]
  37. Alizadeh-Sani M, Hamishehkar H, Khezerlou A, Azizi-Lalabadi M, Azadi Y et al. Bioemulsifiers derived from microorganisms: applications in the drug and food industry. Adv Pharm Bull 2018; 8:191–199 [CrossRef]
    [Google Scholar]
  38. Cheng P, Shan R, Yuan H-R, Deng L-F, Chen Y. Enhanced Rhodococcus pyridinivorans HR-1 anode performance by adding trehalose lipid in microbial fuel cell. Bioresour Technol 2018; 267:774–777 [CrossRef]
    [Google Scholar]
  39. Garrido-Sanz D, Manzano J, Martín M, Redondo-Nieto M, Rivilla R. Metagenomic analysis of a biphenyl-degrading soil bacterial consortium reveals the metabolic roles of specific populations. Front Microbiol 2018; 9:232 [CrossRef]
    [Google Scholar]
  40. Brazil GM, Kenefick L, Callanan M, Haro A, de Lorenzo V et al. Construction of a rhizosphere pseudomonad with potential to degrade polychlorinated biphenyls and detection of bph gene expression in the rhizosphere. Appl Environ Microbiol 1995; 61:1946–1952 [CrossRef][PubMed]
    [Google Scholar]
  41. Bedard DL, Unterman R, Bopp LH, Brennan MJ, Haberl ML et al. Rapid assay for screening and characterizing microorganisms for the ability to degrade polychlorinated biphenyls. Appl Environ Microbiol 1986; 51:761–768 [CrossRef]
    [Google Scholar]
  42. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [CrossRef]
    [Google Scholar]
  43. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [CrossRef]
    [Google Scholar]
  44. Koren S, Walenz BP, Berlin K, Miller JR, Bergman NH et al. Canu: scalable and accurate long-read assembly via adaptive k -mer weighting and repeat separation. Genome Res 2017; 27:722–736 [CrossRef]
    [Google Scholar]
  45. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J et al. BLAST+: architecture and applications. BMC Bioinformatics 2009; 10:421 [CrossRef]
    [Google Scholar]
  46. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K et al. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 2010; 20:1297–1303 [CrossRef]
    [Google Scholar]
  47. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9:357359 [CrossRef]
    [Google Scholar]
  48. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009; 25:2078–2079 [CrossRef]
    [Google Scholar]
  49. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ et al. The seed and the rapid annotation of microbial genomes using subsystems technology (RAST). Nucleic Acids Res 2014; 42:D206–D214 [CrossRef]
    [Google Scholar]
  50. Huerta-Cepas J, Forslund K, Coelho LP, Szklarczyk D, Jensen LJ et al. Fast genome-wide functional annotation through orthology assignment by eggNOG-Mapper. Mol Biol Evol 2017; 34:2115–2122 [CrossRef]
    [Google Scholar]
  51. Cros M-J, de Monte A, Mariette J, Bardou P, Grenier-Boley B et al. RNAspace.org: an integrated environment for the prediction, annotation, and analysis of ncRNA. RNA 2011; 17:1947–1956 [CrossRef]
    [Google Scholar]
  52. Carver T, Thomson N, Bleasby A, Berriman M, Parkhill J. DNAPlotter: circular and linear interactive genome visualization. Bioinformatics 2009; 25:119–120 [CrossRef]
    [Google Scholar]
  53. Edgar RC. Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [CrossRef]
    [Google Scholar]
  54. Kalkus J, Menne R, Reh M, Schlegel HG. The terminal structures of linear plasmids from Rhodococcus opacus . Microbiology 1998; 144:1271–1279 [CrossRef]
    [Google Scholar]
  55. Warren R, Hsiao WWL, Kudo H, Myhre M, Dosanjh M et al. Functional characterization of a catabolic plasmid from polychlorinated-biphenyl-degrading Rhodococcus sp. strain RHA1. J Bacteriol 2004; 186:7783–7795 [CrossRef]
    [Google Scholar]
  56. Bertelli C, Laird MR, Williams KP, Lau BY. Simon Fraser University Research Computing Group IslandViewer 4: expanded prediction of genomic islands for larger-scale datasets. Nucleic Acids Res 2017; 45:W30–W35
    [Google Scholar]
  57. Bertelli C, Brinkman FSL. Improved genomic island predictions with IslandPath-DIMOB. Bioinformatics 2018; 34:2161–2167 [CrossRef]
    [Google Scholar]
  58. Waack S, Keller O, Asper R, Brodag T, Damm C et al. Score-based prediction of genomic islands in prokaryotic genomes using hidden Markov models. BMC Bioinformatics 2006; 7:142 [CrossRef]
    [Google Scholar]
  59. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K et al. Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal omega. Mol Syst Biol 2011; 7:539 [CrossRef]
    [Google Scholar]
  60. Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 2000; 17:540–552 [CrossRef]
    [Google Scholar]
  61. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [CrossRef]
    [Google Scholar]
  62. Tavaré S. Some probabilistic and statistical problems in the analysis of DNA sequences. Lectures Mathemat Life Sci 1986; 17:57–86
    [Google Scholar]
  63. Pattengale ND, Alipour M, Bininda-Emonds ORP, Moret BME, Stamatakis A. How many bootstrap replicates are necessary?. J Comput Biol 2010; 17:337–354 [CrossRef]
    [Google Scholar]
  64. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [CrossRef]
    [Google Scholar]
  65. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [CrossRef]
    [Google Scholar]
  66. Meier-Kolthoff JP, Göker M. TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 2019; 10:2182 [CrossRef]
    [Google Scholar]
  67. Liu Y, Lai Q, Göker M, Meier-Kolthoff JP, Wang M et al. Genomic insights into the taxonomic status of the Bacillus cereus group. Sci Rep 2015; 5:14082 [CrossRef]
    [Google Scholar]
  68. SQ L, Gascuel O. An improved general amino acid replacement matrix. Mol Biol Evol 2008; 25:1307–1320
    [Google Scholar]
  69. Seto M, Kimbara K, Shimura M, Hatta T, Fukuda M et al. A novel transformation of polychlorinated biphenyls by Rhodococcus sp. strain RHA1. Appl Environ Microbiol 1995; 61:3353–3358 [CrossRef]
    [Google Scholar]
  70. Seeger M, Timmis KN, Hofer B. Degradation of chlorobiphenyls catalyzed by the bph-encoded biphenyl-2,3-dioxygenase and biphenyl-2,3-dihydrodiol-2,3-dehydrogenase of Pseudomonas sp. LB400. FEMS Microbiol Lett 1995; 133:259–264 [CrossRef]
    [Google Scholar]
  71. Seeger M, Timmis KN, Hofer B. Conversion of chlorobiphenyls into phenylhexadienoates and benzoates by the enzymes of the upper pathway for polychlorobiphenyl degradation encoded by the BPH locus of Pseudomonas sp. strain LB400. Appl Environ Microbiol 1995; 61:2654–2658 [CrossRef]
    [Google Scholar]
  72. Ridl J, Suman J, Fraraccio S, Hradilova M, Strejcek M et al. Complete genome sequence of Pseudomonas alcaliphila JAB1 (=DSM 26533), a versatile degrader of organic pollutants. Stand Genomic Sci 2018; 13:3 [CrossRef]
    [Google Scholar]
  73. Čvančarová M, Křesinová Z, Filipová A, Covino S, Cajthaml T. Biodegradation of PCBs by ligninolytic fungi and characterization of the degradation products. Chemosphere 2012; 88:1317–1323 [CrossRef]
    [Google Scholar]
  74. Bao K, Cohen SN. Recruitment of terminal protein to the ends of Streptomyces linear plasmids and chromosomes by a novel telomere-binding protein essential for linear DNA replication. Genes Dev 2003; 17:774–785 [CrossRef]
    [Google Scholar]
  75. Zhang R, Yang Y, Fang P, Jiang C, Xu L et al. Diversity of telomere palindromic sequences and replication genes among Streptomyces linear plasmids. Appl Environ Microbiol 2006; 72:5728–5733 [CrossRef]
    [Google Scholar]
  76. Kolkenbrock S, Naumann B, Hippler M, Fetzner S. A novel replicative enzyme encoded by the linear Arthrobacter plasmid pAL1. J Bacteriol 2010; 192:4935–4943 [CrossRef]
    [Google Scholar]
  77. Yamaichi Y, Niki H. Active segregation by the Bacillus subtilis partitioning system in Escherichia coli . Proc Natl Acad Sci USA 2000; 97:14656–14661 [CrossRef]
    [Google Scholar]
  78. Valero-Rello A, Hapeshi A, Anastasi E, Alvarez S, Scortti M et al. An invertron-like linear plasmid mediates intracellular survival and virulence in bovine isolates of Rhodococcus equi . Infect Immun 2015; 83:2725–2737 [CrossRef]
    [Google Scholar]
  79. Sekine M, Tanikawa S, Omata S, Saito M, Fujisawa T et al. Sequence analysis of three plasmids harboured in Rhodococcus erythropolis strain PR4. Environ Microbiol 2006; 8:334–346 [CrossRef]
    [Google Scholar]
  80. Klatte S, Kroppenstedt RM, Rainey FA. Rhodococcus opacus sp.nov., an unusual nutritionally versatile Rhodococcus-species. Syst Appl Microbiol 1994; 17:355–360 [CrossRef]
    [Google Scholar]
  81. Kampfer P, Dott W, Martin K, Glaeser SP. Rhodococcus defluvii sp. nov., isolated from wastewater of a bioreactor and formal proposal to reclassify [Corynebacterium hoagii] and Rhodococcus equi as Rhodococcus hoagii comb. nov. Int J Syst Evol Microbiol 2014; 64:755–761 [CrossRef]
    [Google Scholar]
  82. diCenzo GC, Mengoni A, Perrin E. Chromids aid genome expansion and functional diversification in the family Burkholderiaceae . Mol Biol Evol 2019; 36:562–574 [CrossRef]
    [Google Scholar]
  83. Foght JM, Westlake DWS. Degradation of polycyclic aromatic hydrocarbons and aromatic heterocycles by a Pseudomonas species. Can J Microbiol 1988; 34:1135–1141 [CrossRef]
    [Google Scholar]
  84. Selifonov S, Slepen'kin A, Adanin V, Nefedova M, Starovoĭtov I. Oxidation of dibenzofuran by Pseudomonas strains harboring plasmids of naphthalene degradation. Mikrobiologiia 1991; 60:67–71
    [Google Scholar]
  85. Furukawa K, Suenaga H, Goto M. Biphenyl dioxygenases: functional versatilities and directed evolution. J Bacteriol 2004; 186:5189–5196 [CrossRef]
    [Google Scholar]
  86. Luz AP, Pellizari VH, Whyte LG, Greer CW. A survey of indigenous microbial hydrocarbon degradation genes in soils from Antarctica and Brazil. Can J Microbiol 2004; 50:323–333 [CrossRef]
    [Google Scholar]
  87. Köberl M, Müller H, Ramadan EM, Berg G. Desert farming benefits from microbial potential in arid soils and promotes diversity and plant health. PLoS One 2011; 6:e24452 [CrossRef]
    [Google Scholar]
  88. Undabarrena A, Salvà-Serra F, Jaén-Luchoro D, Castro-Nallar E, Mendez KN et al. Complete genome sequence of the marine Rhodococcus sp. H-CA8f isolated from Comau fjord in Northern Patagonia, Chile. Mar Genomics 2018; 40:13–17 [CrossRef]
    [Google Scholar]
  89. Alvarez HM. Central metabolism of species of the genus Rhodococcus . In: Biology of Rhodococcus Berlin and Heidelberg: Springer; 2010 pp 91–108
    [Google Scholar]
  90. Alvarez HM, Luftmann H, Silva RA, Cesari AC, Viale A et al. Identification of phenyldecanoic acid as a constituent of triacylglycerols and wax ester produced by Rhodococcus opacus PD630. Microbiology 2002; 148:1407–1412 [CrossRef]
    [Google Scholar]
  91. Navarro-Llorens JM, Patrauchan MA, Stewart GR, Davies JE, Eltis LD et al. Phenylacetate catabolism in Rhodococcus sp. strain RHA1: a central pathway for degradation of aromatic compounds. J Bacteriol 2005; 187:4497–4504 [CrossRef]
    [Google Scholar]
  92. Kim D, Chae J-C, Zylstra GJ, Kim Y-S, Kim S-K et al. Identification of a novel dioxygenase involved in metabolism of o-xylene, toluene, and ethylbenzene by Rhodococcus sp. strain DK17. Appl Environ Microbiol 2004; 70:7086–7092 [CrossRef]
    [Google Scholar]
  93. Yang X, Sun Y, Qian S. Biodegradation of seven polychlorinated biphenyls by a newly isolated aerobic bacterium (Rhodococcus sp. R04). J Ind Microbiol Biotechnol 2004; 31:415–420 [CrossRef]
    [Google Scholar]
  94. Yen KM, Karl MR, Blatt LM, Simon MJ, Winter RB et al. Cloning and characterization of a Pseudomonas mendocina KR1 gene cluster encoding toluene-4-monooxygenase. J Bacteriol 1991; 173:5315–5327 [CrossRef][PubMed]
    [Google Scholar]
  95. de Carvalho CCCR, da Cruz AARL, Pons M-N, Pinheiro HMRV, Cabral JMS et al. Mycobacterium sp., Rhodococcus erythropolis, and Pseudomonas putida behavior in the presence of organic solvents. Microsc Res Tech 2004; 64:215–222 [CrossRef][PubMed]
    [Google Scholar]
  96. Peters F, Heintz D, Johannes J, van Dorsselaer A, Boll M. Genes, enzymes, and regulation of para-cresol metabolism in Geobacter metallireducens . J Bacteriol 2007; 189:4729–4738 [CrossRef]
    [Google Scholar]
  97. Ji Y, Mao G, Wang Y, Bartlam M. Structural insights into diversity and n-alkane biodegradation mechanisms of alkane hydroxylases. Front Microbiol 2013; 4:58 [CrossRef]
    [Google Scholar]
  98. van Beilen JB, Wubbolts MG, Witholt B. Genetics of alkane oxidation by Pseudomonas oleovorans . Biodegradation 1994; 5:161–174 [CrossRef]
    [Google Scholar]
  99. Bihari Z, Szvetnik A, Szabó Z, Blastyák A, Zombori Z et al. Functional analysis of long-chain n-alkane degradation by Dietzia spp. FEMS Microbiol Lett 2011; 316:100–107 [CrossRef]
    [Google Scholar]
  100. Whyte LG, Slagman SJ, Pietrantonio F, Bourbonnière L, Koval SF et al. Physiological adaptations involved in alkane assimilation at a low temperature by Rhodococcus sp. strain Q15. Appl Environ Microbiol 1999; 65:2961–2968 [CrossRef]
    [Google Scholar]
  101. Niescher S, Wray V, Lang S, Kaschabek SR, Schlömann M. Identification and structural characterisation of novel trehalose dinocardiomycolates from n-alkane-grown Rhodococcus opacus 1CP. Appl Microbiol Biotechnol 2006; 70:605–611 [CrossRef]
    [Google Scholar]
  102. Zampolli J, Collina E, Lasagni M, Di Gennaro P. Biodegradation of variable-chain-length n-alkanes in Rhodococcus opacus R7 and the involvement of an alkane hydroxylase system in the metabolism. AMB Express 2014; 4:73 [CrossRef]
    [Google Scholar]
  103. Chan SI, Chen KH-C, Yu SS-F, Chen C-L, Kuo SS-J. Toward delineating the structure and function of the particulate methane monooxygenase from methanotrophic bacteria. Biochemistry 2004; 43:4421–4430 [CrossRef][PubMed]
    [Google Scholar]
  104. de Carvalho CCCR, Parreño-Marchante B, Neumann G, da Fonseca MMR, Heipieper HJ. Adaptation of Rhodococcus erythropolis DCL14 to growth on n-alkanes, alcohols and terpenes. Appl Microbiol Biotechnol 2005; 67:383–388 [CrossRef][PubMed]
    [Google Scholar]
  105. Pirog TP, Korzh YV, Shevchuk TA, Tarasenko DA. Peculiarities of C2 metabolism and intensification of the synthesis of surface-active substances in Rhodococcus erythropolis EK-1 grown in ethanol. Microbiology 2008; 77:665–673 [CrossRef]
    [Google Scholar]
  106. Kurane R, Hatamochi K, Kakuno T, Kiyohara M, Hirano M et al. Production of a bioflocculant by Rhodococcus erythropolis S-1 grown on alcohols. Biosci Biotechnol Biochem 1994; 58:428–429 [CrossRef]
    [Google Scholar]
  107. Alvarez HM, Mayer F, Fabritius D, Steinbüchel A. Formation of intracytoplasmic lipid inclusions by Rhodococcus opacus strain PD630. Arch Microbiol 1996; 165:377–386 [CrossRef][PubMed]
    [Google Scholar]
  108. Alvarez HM, Kalscheuer R, Steinbüchel A. Accumulation and mobilization of storage lipids by Rhodococcus opacus PD630 and Rhodococcus ruber NCIMB 40126. Appl Microbiol Biotechnol 2000; 54:218–223 [CrossRef][PubMed]
    [Google Scholar]
  109. Aragno M. Thermophilic, aerobic, hydrogen-oxidizing (Knallgas) bacteria. In: The Prokaryotes Berlin and Heidelberg: Springer; 1992 pp 3917–3933
    [Google Scholar]
  110. Grzeszik C, Lübbers M, Reh M, Schlegel HG. Genes encoding the NAD-reducing hydrogenase of Rhodococcus opacus MR11. Microbiology 1997; 143:1271–1286 [CrossRef][PubMed]
    [Google Scholar]
  111. Grzeszik C, Ross K, Schneider K, Reh M, Schlegel HG. Location, catalytic activity, and subunit composition of NAD-reducing hydrogenases of some Alcaligenes strains and Rhodococcus opacus MR22. Arch Microbiol 1997; 167:172–176 [CrossRef][PubMed]
    [Google Scholar]
  112. Mader HM, Pettitt ME, Wadham JL, Wolff EW, Parkes RJ. Subsurface ice as a microbial habitat. Geology 2006; 34:169–172 [CrossRef]
    [Google Scholar]
  113. Chin JP, Megaw J, Magill CL, Nowotarski K, Williams JP et al. Solutes determine the temperature windows for microbial survival and growth. Proc Natl Acad Sci USA 2010; 107:7835–7840 [CrossRef][PubMed]
    [Google Scholar]
  114. Hsiao WWL, Ung K, Aeschliman D, Bryan J, Finlay BB et al. Evidence of a large novel gene pool associated with prokaryotic genomic islands. PLoS Genet 2005; 1:e62 [CrossRef][PubMed]
    [Google Scholar]
  115. Navarro CA, von Bernath D, Jerez CA. Heavy metal resistance strategies of acidophilic bacteria and their acquisition: importance for biomining and bioremediation. Biol Res 2013; 46:363–371 [CrossRef][PubMed]
    [Google Scholar]
  116. Pagano M, Martins AF, Barth AL. Mobile genetic elements related to carbapenem resistance in Acinetobacter baumannii . Braz J Microbiol 2016; 47:785–792 [CrossRef][PubMed]
    [Google Scholar]
  117. Miyazaki R, Bertelli C, Benaglio P, Canton J, De Coi N et al. Comparative genome analysis of Pseudomonas knackmussii B13, the first bacterium known to degrade chloroaromatic compounds. Environ Microbiol 2015; 17:91–104 [CrossRef][PubMed]
    [Google Scholar]
  118. Levy-Booth DJ, Fetherolf MM, Stewart GR, Liu J, Eltis LD et al. Catabolism of alkylphenols in Rhodococcus via a meta-cleavage pathway associated with genomic islands. Front Microbiol 2019; 10:1862
    [Google Scholar]
  119. Pathak A, Chauhan A, Blom J, Indest KJ, Jung CM et al. Comparative genomics and metabolic analysis reveals peculiar characteristics of Rhodococcus opacus strain M213 particularly for naphthalene degradation. PLoS One 2016; 11:e0161032 [CrossRef][PubMed]
    [Google Scholar]
  120. Goswami L, Arul Manikandan N, Pakshirajan K, Pugazhenthi G. Simultaneous heavy metal removal and anthracene biodegradation by the oleaginous bacteria Rhodococcus opacus . 3 Biotech 2017; 7:37 [CrossRef][PubMed]
    [Google Scholar]
  121. Vásquez TGP, Botero AEC, de Mesquita LMS, Torem ML. Biosorptive removal of CD and Zn from liquid streams with a Rhodococcus opacus strain. Miner Eng 2007; 20:939–944 [CrossRef]
    [Google Scholar]
  122. Retamal-Morales G, Mehnert M, Schwabe R, Tischler D, Schlömann M et al. Genomic characterization of the arsenic-tolerant Actinobacterium, Rhodococcus erythropolis S43. Solid State Phenomena 2017; 262:660–663 [CrossRef]
    [Google Scholar]
  123. Pulles T, Denier van der Gon H, Appelman W, Verheul M. Emission factors for heavy metals from diesel and petrol used in European vehicles. Atmos Environ 2012; 61:641–651 [CrossRef]
    [Google Scholar]
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