Skip to main content

Advertisement

Springer Nature Link
Log in

Core genome and plasmidome of the quorum-quenching bacterium Rhodococcus erythropolis

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Rhodococcus erythropolis is a worldwide-distributed actinobacterium that exhibits a remarkable metabolic versatility illustrated by its ability to degrade complex compounds, such as quorum-sensing signals N-acylhomoserine lactones (NAHLs), phenols, sterols and fuel derivatives. Because of its catabolic properties, R. erythropolis strains are proposed as anti-biofouling agents against NAHL-dependent biofilms, biocontrol agents against NAHL-emitting plant pathogens, and bioremediation agents in contaminated waters and soils. Here, we used the PacBio technology to resolve the complete genome sequence of the biocontrol strain R. erythropolis R138. Its genome consisted in a circular chromosome (6,236,862 bp), a linear plasmid pLRE138 (477,915 bp) and a circular plasmid pCRE138 (91,729 bp). In addition, draft genomes of five R. erythropolis strains were determined by Illumina technology and compared with the other five R. erythropolis genomes that are available in public databases: 5,825 common CDSs were present in all of the eleven analyzed genomes and represented up to 87 % of those identified in R. erythropolis R138. This study highlighted the high proportion of core-genome genes in R. erythropolis, but a high variability of the plasmid content. Key-metabolic pathways which are involved in the degradation of complex molecules, such as NAHLs and phenol, catechol and sterol derivatives are coded by the R. erythropolis core-genome.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Aggarwal S, Karimi IA, Lee DY (2011) Flux-based analysis of sulfur metabolism in desulfurizing strains of Rhodococcus erythropolis. FEMS Microbiol Lett 315(2):115–121

    Article  CAS  PubMed  Google Scholar 

  • Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O (2008) The RAST server: rapid annotations using subsystems technology. BMC Genom 9:75

    Article  Google Scholar 

  • Barbey C, Crepin A, Cirou A, Budin-Verneuil A, Orange N, Feuilloley M, Faure D, Dessaux Y, Burini J-F, Latour X (2012) Catabolic pathway of gamma-caprolactone in the biocontrol agent Rhodococcus erythropolis. J Proteome Res 11(1):206–216

    Article  CAS  PubMed  Google Scholar 

  • Bertani G (1951) Studies on lysogenesis. 1. The mode of phage liberation by lysogenic Escherichia coli. J Bacteriol 62(3):293–300

  • Bouet JY, Funnell BE (1999) P1 ParA interacts with the P1 partition complex at parS and an ATP-ADP switch controls ParA activities. EMBO J 18:1415–1424

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cha C, Gao P, Chen YC, Shaw PD, Farrand SK (1998) Production of acyl-homoserine lactone quorum-sensing signals by gram-negative plant-associated bacteria. Mol Plant Microbe Interact 11(11):1119–1129

    Article  CAS  PubMed  Google Scholar 

  • Chilton MD, Currier TC, Farrand SK, Bendich AJ, Gordon MP, Nester EW (1974) Agrobacterium tumefaciens DNA and PS8 bacteriophage DNA not detected in crown gall tumors. Proc Natl Acad Sci USA 71(9):3672–3676

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cirou A, Diallo S, Kurt C, Latour X, Faure D (2007) Growth promotion of quorum-quenching bacteria in the rhizosphere of Solanum tuberosum. Environ Microbiol 9(6):1511–1522

    Article  CAS  PubMed  Google Scholar 

  • Cirou A, Raffoux A, Diallo S, Latour X, Dessaux Y, Faure D (2011) Gamma-caprolactone stimulates growth of quorum-quenching Rhodococcus populations in a large-scale hydroponic system for culturing Solanum tuberosum. Res Microbiol 162(9):945–950

    Article  CAS  PubMed  Google Scholar 

  • Cirou A, Mondy S, An S, Charrier A, Sarrazin A, Thoison O, DuBow M, Faure D (2012) Efficient biostimulation of native and introduced quorum-quenching Rhodococcus erythropolis populations is revealed by a combination of analytical chemistry, microbiology, and pyrosequencing. Appl Environ Microbiol 78(2):481–492

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • de Carvalho C, da Fonseca M (2005) The remarkable Rhodococcus erythropolis. Appl Microbiol Biotechnol 67:715–726

    Article  PubMed  Google Scholar 

  • de Carvalho C, Fatal V, Alves SS, da Fonseca MMR (2007) Adaptation of Rhodococcus erythropolis cells to high concentrations of toluene. Appl Microbiol Biotechnol 76(6):1423–1430

    Article  CAS  PubMed  Google Scholar 

  • de Carvalho C, Wick LY, Heipieper HJ (2009) Cell wall adaptations of planktonic and biofilm Rhodococcus erythropolis cells to growth on C5 to C16 n-alkane hydrocarbons. Appl Microbiol Biotechnol 82(2):311–320

    Article  CAS  PubMed  Google Scholar 

  • del Solar G, Giraldo R, Ruiz-Echevarría MJ, Espinosa M, Díaz-Orejas R (1998) Replication and control of circular bacterial plasmids. Microbiol Mol Biol Rev 62:434–464

    PubMed Central  PubMed  Google Scholar 

  • Deng W, Liou SR, Plunkett G, Mayhew GF, Rose DJ, Burland V et al (2003) Comparative genomics of Salmonella enterica serovar typhi strains Ty2 and CT18. J Bacteriol 185(7):2330–2337

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Faure D, Dessaux Y (2007) Novel biocontrol strategies directed at Pectobacterium carotovorum. Eur J Plant Pathol 119:353–365

    Article  CAS  Google Scholar 

  • Ferrarini M, Moretto M, Ward JA, Surbanovski N, Stevanovic V, Giongo L et al (2013) An evaluation of the PacBio RS platform for sequencing and de novo assembly of a chloroplast genome. BMC Genomics 14:11

  • Gogarten JP, Townsend JP (2005) Horizontal gene transfer, genome innovation and evolution. Nat Rev Microbiol 3:679–687

    Article  CAS  PubMed  Google Scholar 

  • Hannou N, Mondy S, Planamente S, Moumni M, Llop P, López M, Manceau C, Barny MA, Faure D (2013) Deep sequencing revealed genome-wide single-nucleotide polymorphism and plasmid content of Erwinia amylovora strains isolated in Middle Atlas. Morocco. Res Microbiol 164(8):815–820

    Article  CAS  Google Scholar 

  • Koren S, Harhay GP, Smith TP, Bono JL, Harhay DM, McVey SD et al (2013) Reducing assembly complexity of microbial genomes with single-molecule sequencing. Genome Biol 14(9):16

  • Kube M, Migdoll AM, Gehring I, Heitmann K, Mayer Y, Kuhl H, Knaust F, Geider K, Reinhardt R (2010) Genome comparison of the epiphytic bacteria Erwinia billingiae and E. tasmaniensis with the pear pathogen E. pyrifoliae. BMC Genom 11:393–408

    Article  Google Scholar 

  • Kwasiborski A, Mondy S, Beury-Cirou A, Faure D (2014) Genome sequence of the quorum-quenching Rhodococcus erythropolis strain R138. Genome Announc 2(2):e00224-14

    Article  PubMed Central  PubMed  Google Scholar 

  • Kwasiborski A, Mondy S, Chong T-M, Barbey C, Chan K-G, Beury-Cirou A, Latour X, Faure D (2015) Transcriptome of the quorum-sensing signal-degrading Rhodococcus erythropolis responds differentially to virulent and avirulent Pectobacterium atrosepticum. Heredity. doi:10.1038/hdy.2014.121

    PubMed  Google Scholar 

  • Lang J, Vigouroux A, Planamente S, El Sahili A, Blin P, Aumont-Nicaise M, Dessaux Y, Moréra S, Faure D (2014) Agrobacterium uses a unique ligand-binding mode for trapping opines and acquiring a competitive advantage in the niche construction on plant host. PLoS Pathog 10(10):e1004444

    Article  PubMed Central  PubMed  Google Scholar 

  • McClean KH, Winson MK, Fish L, Taylor A, Chhabra SR, Camara M, Daykin M, Lamb JH, Swift S, Bycroft BW, Stewart GSAB, Williams P (1997) Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology 143(12):3703–3711

    Article  CAS  PubMed  Google Scholar 

  • Moreno-Horn M, Martinez-Rojas E, Gorisch H, Tressl R, Garbe LA (2007) Oxidation of 1,4-alkanediols into gamma-lactones via gamma-lactols using Rhodococcus erythropolis as biocatalyst. J Mol Catal B-Enzym 49(1–4):24–27

    Article  CAS  Google Scholar 

  • Oh HS, Kim SR, Cheong WS, Lee CH, Lee JK (2013) Biofouling inhibition in MBR by Rhodococcus sp. BH4 isolated from real MBR plant. Appl Microbiol Biotechnol 97(23):10223–10231

    Article  CAS  PubMed  Google Scholar 

  • Ohshiro T, Kojima T, Torii K, Kawasoe H, Izumi Y (1999) Purification and characterization of dibenzothiophene (DBT) sulfone monooxygenase, an enzyme involved in DBT desulfurization, from Rhodococcus erythropolis D-1. J Biosc Bioeng 88:610–616

    Article  CAS  Google Scholar 

  • Patrauchan MA, Florizone C, Dosanjh M, Molm WW, Davies J, Eltis LD (2005) Catabolism of benzoate and phthalate in Rhodococcus sp strain RHA1: redundancies and convergence. J Bacteriol 187(12):4050–4063

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Peng L, Yang C, Zeng G, Wang L, Dai C, Long Z, Liu H, Zhong Y (2014) Characterization and application of bioflocculant prepared by Rhodococcus erythropolis using sludge and livestock wastewater as cheap culture media. Appl Microbiol Biotechnol 98(15):6847–6858

    Article  CAS  PubMed  Google Scholar 

  • Petrusma M, van der Geize R, Dijkhuizen L (2014) 3-Ketosteroid 9 alpha-hydroxylase enzymes: rieske non-heme monooxygenases essential for bacterial steroid degradation. Anton Leeuw Int J G 106(1):157–172

    Article  CAS  Google Scholar 

  • Rodionov O, Lobocka M, Yarmolinsky M (1999) Silencing of genes flanking the P1 plasmid centromere. Science 283:546–549

    Article  CAS  PubMed  Google Scholar 

  • Rossi M, Brigidi P, y Rodriguez AGV, Matteuzzi D (1996) Characterization of the plasmid pMB1 from Bifidobacterium longum and its use for shuttle vector construction. Res Microbiol 147:133–143

    Article  CAS  PubMed  Google Scholar 

  • Sekine M, Tanikawa S, Omata S, Saito M, Fujisawa T, Tsukatani N et al (2006) Sequence analysis of three plasmids harboured in Rhodococcus erythropolis strain PR4. Environ Microbiol 8(2):334–346

    Article  CAS  PubMed  Google Scholar 

  • Shevtsov A, Tarlykov P, Zholdybayeva E, Momynkulov D, Sarsenova A, Moldagulova N, Momynaliev K (2013) Draft Genome sequence of Rhodococcus erythropolis DN1, a crude oil biodegrader. Genome Announc 1(5):e00846-13

    PubMed Central  PubMed  Google Scholar 

  • Stolt P, Stoker NG (1997) Mutational analysis of the regulatory region of the Mycobacterium plasmid pAL5000. Nucleic Acids Res 25:3840–3846

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tao F, Zhao P, Li Q, Su F, Yu B, Ma C, Tang H, Tai C, Wu G, Xu P (2011) Genome sequence of Rhodococcus erythropolis XP, a biodesulfurizing bacterium with industrial potential. J Bacteriol 193(22):6422–6423

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tian XJ, Liu XY, Liu H, Wang SJ, Zhou NY (2013) Biodegradation of 3-nitrotoluene by Rhodococcus sp strain ZWL3NT. Appl Microbiol Biotechnol 97(20):9217–9223

    Article  CAS  PubMed  Google Scholar 

  • Uroz S, D’Angelo-Picard C, Carlier A, Elasri M, Sicot C, Petit A, Oger P, Faure D, Dessaux Y (2003) Novel bacteria degrading N-acylhomoserine lactones and their use as quenchers of quorum-sensing-regulated functions of plant-pathogenic bacteria. Microbiology 149(8):1981–1989

    Article  CAS  PubMed  Google Scholar 

  • Uroz S, Chhabra SR, Cámara M, Williams P, Oger P, Dessaux Y (2005) N-Acylhomoserine lactone quorum-sensing molecules are modified and degraded by Rhodococcus erythropolis W2 by both amidolytic and novel oxidoreductase activities. Microbiology 151(10):3313–3322

    Article  CAS  PubMed  Google Scholar 

  • Uroz S, Oger PM, Chapelle E, Adeline MT, Faure D, Dessaux Y (2008) A Rhodococcus qsdA-encoded enzyme defines a novel class of large-spectrum quorum-quenching lactonases. Appl Environ Microbiol 74(5):1357–1366

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Uroz S, Dessaux Y, Oger P (2009) Quorum sensing and quorum-quenching: the yin and yang of bacterial communication. ChemBioChem 10(2):205–216

    Article  CAS  PubMed  Google Scholar 

  • van der Geize R, Dijkhuizen L (2004) Harnessing the catabolic diversity of rhodococci for environmental and biotechnological applications. Curr Opin Microbiol 7:255–261

    Article  PubMed  Google Scholar 

  • Vesely M, Knoppova M, Nesvera J, Patek M (2007) Analysis of catRABC operon for catechol degradation from phenol-degrading Rhodococcus erythropolis. Appl Microbiol Biotechnol 76(1):159–168

    Article  CAS  PubMed  Google Scholar 

  • Zidkova L, Szokof J, Rucka L, Patek M, Nesver J (2013) Biodegradation of phenol using recombinant plasmid-carrying Rhodococcus erythropolis strains. Int Biodeterioration Biodegradation 84:179–184

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work has benefited from the facilities and expertise of the high throughput sequencing platforms of IMAGIF (Gif-sur-Yvette). A.K. was supported by the region Ile-de-France (ASTREA), as well as by the CNRS and ANR (project SVSE7 2011 ECORUM). K.G.C. thanks the High Impact Research Grant (UM.C/625/1/HIR/MOHE/CHAN/14/1, No. H-50001-A000027) and the French Fellowship awarded to K.G. Chan by the French Embassy in Malaysia is also gratefully acknowledged.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Institut for Integrative Biology of the Cell, I2BC, Université Paris Saclay, Saclay Plant Sciences, UMR9198 CNRS CEA Université Paris-Sud, Avenue de la Terrasse, 91198, Gif-sur-Yvette Cedex, France

    Anthony Kwasiborski, Samuel Mondy & Denis Faure

  2. Division of Genetics and Molecular Biology, Institute of Biological Sciences, Faculty of Science, University of Malaya, 50603, Kuala Lumpur, Malaysia

    Teik-Min Chong & Kok-Gan Chan

  3. Comité Nord Plant de Pomme de Terre (CNPPT), Semences, Innovation, Protection Recherche et Environnement (SIPRE), rue des champs Potez, 62217, Achicourt, France

    Amélie Beury-Cirou

  4. Institut des Sciences du Végétal, UPR2355, Centre National de la Recherche Scientifique, 1, Avenue de la Terrasse, 91198, Gif-sur-Yvette, France

    Denis Faure

Authors
  1. Anthony Kwasiborski
    View author publications

    Search author on:PubMed Google Scholar

  2. Samuel Mondy
    View author publications

    Search author on:PubMed Google Scholar

  3. Teik-Min Chong
    View author publications

    Search author on:PubMed Google Scholar

  4. Kok-Gan Chan
    View author publications

    Search author on:PubMed Google Scholar

  5. Amélie Beury-Cirou
    View author publications

    Search author on:PubMed Google Scholar

  6. Denis Faure
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Denis Faure.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kwasiborski, A., Mondy, S., Chong, TM. et al. Core genome and plasmidome of the quorum-quenching bacterium Rhodococcus erythropolis . Genetica 143, 253–261 (2015). https://doi.org/10.1007/s10709-015-9827-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-015-9827-4

Keywords