The complete genome sequence of Rhodococcus 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 blast distance phylogeny (GBDP) algorithm and digital DNA-DNA hybridization (dDDH) with other Rhodococcus type strains resulted in a clear differentiation of WAY2, which is likely a new species. The genome of WAY2 contains five distinct clusters of bph, etb and nah 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 n-alkanes of various chain-lengths as a sole carbon source, probably due to the presence of alkB and ladA 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.

Departamento de Biología Facultad de Ciencias Universidad Autónoma de Madrid C Darwin 2 28049 Madrid Spain

Department of Biochemistry and Microbiology Faculty of Food and Biochemical Technology University of Chemistry and Technology Prague Technika 3 16628 Prague Czech Republic

Laboratory of Environmental Biotechnology Institute of Microbiology Czech Academy of Sciences v v i Vídeňská 1083 14200 Prague Czech Republic

Zobrazit více v PubMed

Sharma S, Pant A. Crude oil degradation by a marine actinomycete Rhodococcus sp. Indian J Mar Sci. 2001;30:146–150.

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. doi: 10.1017/S0954102005002415. DOI

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. doi: 10.1016/j.jbiotec.2016.03.040. PubMed DOI

Prescott JF. Rhodococcus equi: an animal and human pathogen. Clin Microbiol Rev. 1991;4:20–34. doi: 10.1128/CMR.4.1.20. PubMed DOI PMC

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. doi: 10.1094/MPMI.2001.14.5.599. PubMed DOI

Yassin AF. Rhodococcus triatomae sp. nov., isolated from a blood-sucking bug. Int J Syst Evol Microbiol. 2005;55:1575–1579. doi: 10.1099/ijs.0.63571-0. PubMed DOI

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. doi: 10.1007/BF00186971. DOI

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. doi: 10.1099/ijs.0.63939-0. PubMed DOI

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. doi: 10.1007/s00253-007-1229-9. PubMed DOI

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. doi: 10.1016/j.marpolbul.2011.07.013. PubMed DOI

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. doi: 10.1128/AEM.67.5.2021-2028.2001. PubMed DOI PMC

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. doi: 10.1073/pnas.0607048103. PubMed DOI PMC

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. doi: 10.1016/j.femsec.2004.09.010. PubMed DOI

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. doi: 10.1271/bbb.60663. PubMed DOI

Behki R, Topp E, Dick W, Germon P. Metabolism of the herbicide atrazine by Rhodococcus strains. Appl Environ Microbiol. 1993;59:1955–1959. doi: 10.1128/AEM.59.6.1955-1959.1993. PubMed DOI PMC

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. doi: 10.1099/mic.0.2008/016568-0. PubMed DOI

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. doi: 10.1186/1471-2164-9-600. PubMed DOI PMC

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. PubMed

Larkin MJ, Kulakov LA, Allen CC. In: Biology of Rhodococcus. Berlin and Heidleberg: Springer; 2010. Genomes and plasmids in Rhodococcus; pp. 73–90.

Larkin MJ, Kulakov LA, Allen CCR. Biodegradation and Rhodococcus – masters of catabolic versatility. Curr Opin Biotechnol. 2005;16:282–290. doi: 10.1016/j.copbio.2005.04.007. PubMed DOI

diCenzo GC, Finan TM. The divided bacterial genome: structure, function, and evolution. Microbiol Mol Biol Rev. 2017;81:e00019-17. doi: 10.1128/MMBR.00019-17. PubMed DOI PMC

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. doi: 10.1016/S0168-9525(02)02752-X. PubMed DOI

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. doi: 10.1128/AEM.00298-06. PubMed DOI PMC

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. doi: 10.1007/s00253-006-0481-8. PubMed DOI

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. doi: 10.1271/bbb.60551. PubMed DOI

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. doi: 10.1007/BF01574775. DOI

Furukawa K, Suenaga H, Goto M. Biphenyl dioxygenases: functional versatilities and directed evolution. J Bacteriol. 2004;186:5189–5196. doi: 10.1128/JB.186.16.5189-5196.2004. PubMed DOI PMC

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. doi: 10.1128/JB.01122-07. PubMed DOI PMC

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. doi: 10.1046/j.1365-2672.2002.01640.x. PubMed DOI

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. doi: 10.1007/BF02931064. DOI

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. doi: 10.1023/B:ABIM.0000025948.77233.dc. PubMed DOI

Krivoruchko A, Kuyukina M, Ivshina I. Advanced Rhodococcus biocatalysts for environmental biotechnologies. Catalysts. 2019;9:236. doi: 10.3390/catal9030236. DOI

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. doi: 10.1007/s11274-012-1110-6. PubMed DOI

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. doi: 10.1007/s00253-014-6002-2. PubMed DOI

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. doi: 10.2174/0929866523666151215105442. PubMed DOI

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. doi: 10.1128/genomeA.01406-16. PubMed DOI PMC

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. doi: 10.15171/apb.2018.023. PubMed DOI PMC

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. doi: 10.1016/j.biortech.2018.08.006. PubMed DOI

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. doi: 10.3389/fmicb.2018.00232. PubMed DOI PMC

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. doi: 10.1128/AEM.61.5.1946-1952.1995. PubMed DOI PMC

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. doi: 10.1128/AEM.51.4.761-768.1986. PubMed DOI PMC

Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–2120. doi: 10.1093/bioinformatics/btu170. PubMed DOI PMC

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. doi: 10.1089/cmb.2012.0021. PubMed DOI PMC

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. doi: 10.1101/gr.215087.116. PubMed DOI PMC

Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, et al. BLAST+: architecture and applications. BMC Bioinformatics. 2009;10:421. doi: 10.1186/1471-2105-10-421. PubMed DOI PMC

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. doi: 10.1101/gr.107524.110. PubMed DOI PMC

Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357. doi: 10.1038/nmeth.1923. PubMed DOI PMC

Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25:2078–2079. doi: 10.1093/bioinformatics/btp352. PubMed DOI PMC

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. doi: 10.1093/nar/gkt1226. PubMed DOI PMC

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. doi: 10.1093/molbev/msx148. PubMed DOI PMC

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. doi: 10.1261/rna.2844911. PubMed DOI PMC

Carver T, Thomson N, Bleasby A, Berriman M, Parkhill J. DNAPlotter: circular and linear interactive genome visualization. Bioinformatics. 2009;25:119–120. doi: 10.1093/bioinformatics/btn578. PubMed DOI PMC

Edgar RC. Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–1797. doi: 10.1093/nar/gkh340. PubMed DOI PMC

Kalkus J, Menne R, Reh M, Schlegel HG. The terminal structures of linear plasmids from Rhodococcus opacus . Microbiology. 1998;144:1271–1279. doi: 10.1099/00221287-144-5-1271. PubMed DOI

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. doi: 10.1128/JB.186.22.7783-7795.2004. PubMed DOI PMC

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. PubMed PMC

Bertelli C, Brinkman FSL. Improved genomic island predictions with IslandPath-DIMOB. Bioinformatics. 2018;34:2161–2167. doi: 10.1093/bioinformatics/bty095. PubMed DOI PMC

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. doi: 10.1186/1471-2105-7-142. PubMed DOI PMC

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. doi: 10.1038/msb.2011.75. PubMed DOI PMC

Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000;17:540–552. doi: 10.1093/oxfordjournals.molbev.a026334. PubMed DOI

Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30:1312–1313. doi: 10.1093/bioinformatics/btu033. PubMed DOI PMC

Tavaré S. Some probabilistic and statistical problems in the analysis of DNA sequences. Lectures Mathemat Life Sci. 1986;17:57–86.

Pattengale ND, Alipour M, Bininda-Emonds ORP, Moret BME, Stamatakis A. How many bootstrap replicates are necessary? J Comput Biol. 2010;17:337–354. doi: 10.1089/cmb.2009.0179. PubMed DOI

Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016;33:1870–1874. doi: 10.1093/molbev/msw054. PubMed DOI PMC

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. doi: 10.1186/1471-2105-14-60. PubMed DOI PMC

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. doi: 10.1038/s41467-019-10210-3. PubMed DOI PMC

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. doi: 10.1038/srep14082. PubMed DOI PMC

SQ L, Gascuel O. An improved general amino acid replacement matrix. Mol Biol Evol. 2008;25:1307–1320. PubMed

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. doi: 10.1128/AEM.61.9.3353-3358.1995. PubMed DOI PMC

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. doi: 10.1111/j.1574-6968.1995.tb07894.x. PubMed DOI

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. doi: 10.1128/AEM.61.7.2654-2658.1995. PubMed DOI PMC

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. doi: 10.1186/s40793-017-0306-7. PubMed DOI PMC

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. doi: 10.1016/j.chemosphere.2012.03.107. PubMed DOI

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. doi: 10.1101/gad.1060303. PubMed DOI PMC

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. doi: 10.1128/AEM.00707-06. PubMed DOI PMC

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. doi: 10.1128/JB.00614-10. PubMed DOI PMC

Yamaichi Y, Niki H. Active segregation by the Bacillus subtilis partitioning system in Escherichia coli . Proc Natl Acad Sci USA. 2000;97:14656–14661. doi: 10.1073/pnas.97.26.14656. PubMed DOI PMC

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. doi: 10.1128/IAI.00376-15. PubMed DOI PMC

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. doi: 10.1111/j.1462-2920.2005.00899.x. PubMed DOI

Klatte S, Kroppenstedt RM, Rainey FA. Rhodococcus opacus sp.nov., an unusual nutritionally versatile Rhodococcus-species. Syst Appl Microbiol. 1994;17:355–360. doi: 10.1016/S0723-2020(11)80051-2. DOI

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. doi: 10.1099/ijs.0.053322-0. PubMed DOI

diCenzo GC, Mengoni A, Perrin E. Chromids aid genome expansion and functional diversification in the family Burkholderiaceae . Mol Biol Evol. 2019;36:562–574. doi: 10.1093/molbev/msy248. PubMed DOI

Foght JM, Westlake DWS. Degradation of polycyclic aromatic hydrocarbons and aromatic heterocycles by a Pseudomonas species. Can J Microbiol. 1988;34:1135–1141. doi: 10.1139/m88-200. PubMed DOI

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. PubMed

Furukawa K, Suenaga H, Goto M. Biphenyl dioxygenases: functional versatilities and directed evolution. J Bacteriol. 2004;186:5189–5196. doi: 10.1128/JB.186.16.5189-5196.2004. PubMed DOI PMC

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. doi: 10.1139/w04-008. PubMed DOI

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. doi: 10.1371/journal.pone.0024452. PubMed DOI PMC

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. doi: 10.1016/j.margen.2018.01.004. PubMed DOI

Alvarez HM. In: Biology of Rhodococcus. Berlin and Heidelberg: Springer; 2010. Central metabolism of species of the genus Rhodococcus; pp. 91–108.

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. doi: 10.1099/00221287-148-5-1407. PubMed DOI

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. doi: 10.1128/JB.187.13.4497-4504.2005. PubMed DOI PMC

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. doi: 10.1128/AEM.70.12.7086-7092.2004. PubMed DOI PMC

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. doi: 10.1007/s10295-004-0162-5. PubMed DOI

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. doi: 10.1128/JB.173.17.5315-5327.1991. PubMed DOI PMC

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. doi: 10.1002/jemt.20061. PubMed DOI

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. doi: 10.1128/JB.00260-07. PubMed DOI PMC

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. doi: 10.3389/fmicb.2013.00058. PubMed DOI PMC

van Beilen JB, Wubbolts MG, Witholt B. Genetics of alkane oxidation by Pseudomonas oleovorans . Biodegradation. 1994;5:161–174. doi: 10.1007/BF00696457. PubMed DOI

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. doi: 10.1111/j.1574-6968.2010.02198.x. PubMed DOI

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. doi: 10.1128/AEM.65.7.2961-2968.1999. PubMed DOI PMC

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. doi: 10.1007/s00253-005-0113-8. PubMed DOI

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. doi: 10.1186/s13568-014-0073-4. PubMed DOI PMC

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. doi: 10.1021/bi0497603. PubMed DOI

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. doi: 10.1007/s00253-004-1750-z. PubMed DOI

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. doi: 10.1134/S0026261708060039. PubMed DOI

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. doi: 10.1271/bbb.58.428. DOI

Alvarez HM, Mayer F, Fabritius D, Steinbüchel A. Formation of intracytoplasmic lipid inclusions by Rhodococcus opacus strain PD630. Arch Microbiol. 1996;165:377–386. doi: 10.1007/s002030050341. PubMed DOI

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. doi: 10.1007/s002530000395. PubMed DOI

Aragno M. In: The Prokaryotes. Berlin and Heidelberg: Springer; 1992. Thermophilic, aerobic, hydrogen-oxidizing (Knallgas) bacteria; pp. 3917–3933.

Grzeszik C, Lübbers M, Reh M, Schlegel HG. Genes encoding the NAD-reducing hydrogenase of Rhodococcus opacus MR11. Microbiology. 1997;143:1271–1286. doi: 10.1099/00221287-143-4-1271. PubMed DOI

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. doi: 10.1007/s002030050431. PubMed DOI

Mader HM, Pettitt ME, Wadham JL, Wolff EW, Parkes RJ. Subsurface ice as a microbial habitat. Geology. 2006;34:169–172. doi: 10.1130/G22096.1. DOI

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. doi: 10.1073/pnas.1000557107. PubMed DOI PMC

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. doi: 10.1371/journal.pgen.0010062. PubMed DOI PMC

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. doi: 10.4067/S0716-97602013000400008. PubMed DOI

Pagano M, Martins AF, Barth AL. Mobile genetic elements related to carbapenem resistance in Acinetobacter baumannii . Braz J Microbiol. 2016;47:785–792. doi: 10.1016/j.bjm.2016.06.005. PubMed DOI PMC

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. doi: 10.1111/1462-2920.12498. PubMed DOI

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. PubMed PMC

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. doi: 10.1371/journal.pone.0161032. PubMed DOI PMC

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. doi: 10.1007/s13205-016-0597-1. PubMed DOI PMC

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. doi: 10.1016/j.mineng.2007.03.014. DOI

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. doi: 10.4028/www.scientific.net/SSP.262.660. DOI

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. doi: 10.1016/j.atmosenv.2012.07.022. DOI

Differential effect of monoterpenes and flavonoids on the transcription of aromatic ring-hydroxylating dioxygenase genes in Rhodococcus opacus C1 and Rhodococcus sp. WAY2

Predominant Biphenyl Dioxygenase From Legacy Polychlorinated Biphenyl (PCB)-Contaminated Soil Is a Part of Unusual Gene Cluster and Transforms Flavone and Flavanone

Biphenyl 2,3-Dioxygenase in Pseudomonas alcaliphila JAB1 Is Both Induced by Phenolics and Monoterpenes and Involved in Their Transformation

Genomic analysis of dibenzofuran-degrading Pseudomonas veronii strain Pvy reveals its biodegradative versatility