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tdd8: a TerD domain-encoding gene involved in Streptomyces coelicolor differentiation

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Abstract

The Streptomyces coelicolor genome contains 17 TerD domain-encoding genes (tdd genes) of unknown function. The proteins encoded by these genes have been presumed to be involved in tellurite resistance on the basis of their homology with the protein TerD of Serratia marcescens. To elucidate the role of a Tdd protein (Tdd8), both a deletion mutant for the corresponding gene tdd8 (SCO2368) and a recombinant strain over-expressing tdd8 were produced in S. coelicolor M145. The deletion mutant (Δtdd8), like the wild strain, was not resistant to potassium tellurite. The deletion was not lethal but had a marked effect on differentiation. The deletion strain showed more rapid growth in liquid medium and produced long chains of short spores with a dense and non-spherical spore wall on agar plates. The strain over-expressing tdd8 had a growth delay in liquid medium and produced very few spores of irregular shapes and sizes on solid medium. The results of this study demonstrated that Tdd proteins might have a function other than tellurite resistance and this function seems to be of crucial importance for the proper development of the actinomycete S. coelicolor.

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References

  • Benson DA, Boguski MS, Lipman DJ, Ostell J, Ouellette BFF (1998) GenBank. Nucleic Acids Res 26:1–7

    Article  PubMed  CAS  Google Scholar 

  • Bentley SD, Chater KF, Cerdeno-Tarraga AM et al (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141–147

    Article  PubMed  Google Scholar 

  • Chasteen TG, Fuentes DE, Tantalean JC, Vasquez CC (2009) Tellurite: history, oxidative stress, and molecular mechanisms of resistance. FEMS Microbiol Rev 33:820–832

    Article  PubMed  CAS  Google Scholar 

  • Claessen D, de Jong W, Dijkhuizen L, Wosten HA (2006) Regulation of Streptomyces development: reach for the sky! Trends Microbiol 14:313–319

    Article  PubMed  CAS  Google Scholar 

  • Clinical and Laboratory Standards Institute (2006) Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobicall; approved standard, 7th edn. Clinical and Laboratory Standards Institute, Wayne

    Google Scholar 

  • Davidsen T, Beck E, Ganapathy A, Montgomery R, Zafar N, Yang Q, Madupu R, Goetz P, Galinsky K, White O, Sutton G (2010) The comprehensive microbial resource. Nucleic Acids Res 38:D340–D345

    Article  PubMed  CAS  Google Scholar 

  • De Boer E, Heuvelink AE (2000) Methods for the detection and isolation of Shiga toxin-producing Escherichia coli. J Appl Microbiol 88:133S–143S

    Google Scholar 

  • De Mot R, Schoofs G, Nagy I (2007) Proteome analysis of Streptomyces coelicolor mutants affected in the proteasome system reveals changes in stress-responsive proteins. Arch Microbiol 188:257–271

    Article  PubMed  Google Scholar 

  • Dedrick RM, Wildschutte H, McCormick JR (2009) Genetic interactions of smc, ftsK, and parB genes in Streptomyces coelicolor and their developmental genome segregation phenotypes. J Bacteriol 191:320–332

    Article  PubMed  CAS  Google Scholar 

  • Denis F, Brzezinski R (1992) A versatile shuttle cosmid vector for use in Escherichia coli and actinomycetes. Gene 111:115–118

    Article  PubMed  CAS  Google Scholar 

  • Fahey RC, Brody S, Mikolajczyk SD (1975) Changes in the glutathione thiol-disulfide status of Neurospora crassa conidia during germination and aging. J Bacteriol 121:144–151

    PubMed  CAS  Google Scholar 

  • Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, Hotz H-R, Ceric G, Forslund K, Eddy SR, Sonnhammer ELL, Bateman A (2008) The comprehensive microbial resource. Nucleic Acids Res 36:D281–D288

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez-Ceron G, Licona P, Servin-Gonzalez L (2001) Modified xylE and xylTE reporter genes for use in Streptomyces: analysis of the effect of xylT. FEMS Microbiol Lett 196:229–234

    Article  PubMed  CAS  Google Scholar 

  • Gordon ND, Ottaviano GL, Connell SE, Tobkin GV, Son CH, Shterental S, Gehring AM (2008) Secreted-protein response to σU activity in Streptomyces coelicolor. J Bacteriol 190:894–904

    Article  PubMed  CAS  Google Scholar 

  • Gust B, Challis GL, Fowler K, Kieser T, Chater KF (2003) PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc Natl Acad Sci USA 100:1541–1546

    Article  PubMed  CAS  Google Scholar 

  • Kanehisa M, Goto S, Hattori M, Aoki-Kinoshita KF, Itoh M, Kawashima S, Katayama T, Araki M, Hirakawa M (2006) From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res 34:D354–D357

    Article  PubMed  CAS  Google Scholar 

  • Kay CA, Noce T, Tsang AS (1987) Translocation of an unusual cAMP receptor to the nucleus during development of Dictyostelium discoideum. Proc Natl Acad Sci USA 84:2322–2326

    Article  PubMed  CAS  Google Scholar 

  • Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA (2000) Practical streptomyces genetics. John Innes Foundation, Norwich

    Google Scholar 

  • Kim DW, Chater K, Lee KJ, Hesketh A (2005) Changes in the extracellular proteome caused by the absence of the bldA gene product, a developmentally significant tRNA, reveal a new target for the pleiotropic regulator AdpA in Streptomyces coelicolor. J Bacteriol 187:2957–2966

    Article  PubMed  CAS  Google Scholar 

  • Kormutakova R, Klucar L, Turna J (2000) DNA sequence analysis of the tellurite-resistance determinant from clinical strain of Escherichia coli and identification of essential genes. Biometals 13:135–139

    Article  PubMed  CAS  Google Scholar 

  • Langlois P, Bourassa S, Poirier GG, Beaulieu C (2003) Identification of Streptomyces coelicolor proteins that are differentially expressed in the presence of plant material. Appl Environ Microbiol 69:1884–1889

    Article  PubMed  CAS  Google Scholar 

  • Lu Y, Wang W, Shu D, Zhang W, Chen L, Qin Z, Yang S, Jiang W (2007) Characterization of a novel two-component regulatory system involved in the regulation of both actinorhodin and a type I polyketide in Streptomyces coelicolor. Appl Microbiol Biotechnol 77:625–635

    Article  PubMed  CAS  Google Scholar 

  • Manteca A, Mader U, Connolly BA, Sanchez J (2006) A proteomic analysis of Streptomyces coelicolor programmed cell death. Proteomics 6:6008–6022

    Article  PubMed  CAS  Google Scholar 

  • Manteca A, Claessen D, Lopez-Iglesias C, Sanchez J (2007) Aerial hyphae in surface cultures of Streptomyces lividans and Streptomyces coelicolor originate from viable segments surviving an early programmed cell death event. FEMS Microbiol Lett 274:118–125

    Article  PubMed  CAS  Google Scholar 

  • Newton GL, Fahey RC (2008) Regulation of mycothiol metabolism by σR and the thiol redox sensor anti-sigma factor RsrA. Mol Microbiol 68:805–809

    Article  PubMed  CAS  Google Scholar 

  • Newton GL, Arnold K, Price MS, Sherrill C, Delcardayre SB, Aharonowitz Y, Cohen G, Davies J, Fahey RC, Davis C (1996) Distribution of thiols in microorganisms: mycothiol is a major thiol in most actinomycetes. J Bacteriol 178:1990–1995

    PubMed  CAS  Google Scholar 

  • Novotna J, Vohradsky J, Berndt P, Gramajo H, Langen H, Li XM, Minas W, Orsaria L, Roeder D, Thompson CJ (2003) Proteomic studies of diauxic lag in the differentiating prokaryote Streptomyces coelicolor reveal a regulatory network of stress-induced proteins and central metabolic enzymes. Mol Microbiol 48:1289–1303

    Article  PubMed  CAS  Google Scholar 

  • Paget MS, Kang JG, Roe JH, Buttner MJ (1998) σR, an RNA polymerase sigma factor that modulates expression of the thioredoxin system in response to oxidative stress in Streptomyces coelicolor A3(2). EMBO J 17:5776–5782

    Article  PubMed  CAS  Google Scholar 

  • Park JH, Roe JH (2008) Mycothiol regulates and is regulated by a thiol-specific antisigma factor RsrA and σR in Streptomyces coelicolor. Mol Microbiol 68:861–870

    Article  PubMed  CAS  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:2002–2007

    Article  Google Scholar 

  • Piette A, Derouaux A, Gerkens P, Noens EE, Mazzucchelli G, Vion S, Koerten HK, Titgemeyer F, De Pauw E, Leprince P, van Wezel GP, Galleni M, Rigali S (2005) From dormant to germinating spores of Streptomyces coelicolor A3(2): new perspectives from the crp null mutant. J Proteome Res 4:1699–1708

    Article  PubMed  CAS  Google Scholar 

  • Redenbach M, Kieser HM, Denapaite D, Eichner A, Cullum J, Kinashi H, Hopwood DA (1996) A set of ordered cosmids and a detailed genetic and physical map for the 8 Mb Streptomyces coelicolor A3(2) chromosome. Mol Microbiol 21:77–96

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Maniatis T, Fritsch EF (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor

    Google Scholar 

  • Setlow B, Setlow P (1977) Levels of acetyl coenzyme A, reduced and oxidized coenzyme A, and coenzyme A in disulfide linkage to protein in dormant and germinated spores and growing and sporulating cells of Bacillus megaterium. J Bacteriol 132:444–452

    PubMed  CAS  Google Scholar 

  • Taylor DE (1999) Bacterial tellurite resistance. Trends Microbiol 7:111–115

    Article  PubMed  CAS  Google Scholar 

  • Taylor DE, Rooker M, Keelan M, Ng LK, Martin I, Perna NT, Burland NT, Blattner FR (2002) Genomic variability of O islands encoding tellurite resistance in enterohemorrhagic Escherichia coli O157:H7 isolates. J Bacteriol 184:4690–4698

    Article  PubMed  CAS  Google Scholar 

  • Touzain F, Schbath S, Debled-Rennesson I, Aigle B, Kucherov G, Leblond P (2008) SIGffRid: a tool to search for sigma factor binding sites in bacterial genomes using comparative approach and biologically driven statistics. BMC Bioinformatics 9:73

    Article  PubMed  Google Scholar 

  • Tsang AS, Tasaka M (1986) Identification of multiple cyclic AMP-binding proteins in developing Dictyostelium discoideum cells. J Biol Chem 261:10753–10759

    PubMed  CAS  Google Scholar 

  • Vohradsky J, Thompson CJ (2006) Systems level analysis of protein synthesis patterns associated with bacterial growth and metabolic transitions. Proteomics 6:785–793

    Article  PubMed  CAS  Google Scholar 

  • Walter EG, Taylor DE (1992) Plasmid-mediated resistance to tellurite: expressed and cryptic. Plasmid 27:52–64

    Article  PubMed  CAS  Google Scholar 

  • Whelan KF, Colleran E, Taylor DE (1995) Phage inhibition, colicin resistance, and tellurite resistance are encoded by a single cluster of genes on the IncHI2 plasmid R478. J Bacteriol 177:5016–5027

    PubMed  CAS  Google Scholar 

  • Wu G, Culley DE, Zhang W (2005) Predicted highly expressed genes in the genomes of Streptomyces coelicolor and Streptomyces avermitilis and the implications for their metabolism. Microbiology 151:2175–2187

    Article  PubMed  CAS  Google Scholar 

  • Yang YH, Song E, Kim EJ, Lee K, Kim WS, Park SS, Hahn JS, Kim BG (2009) NdgR, an IclR-like regulator involved in amino-acid-dependent growth, quorum sensing, and antibiotic production in Streptomyces coelicolor. Appl Microbiol Biotechnol 82:501–511

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant from the Natural Sciences and Engineering Research Council of Canada (NSERC) to CB. ÉS gratefully acknowledges the receipt of scholarships from NSERC and the Fonds Québécois de la Recherche sur la Nature et les Technologies (FQRNT). The authors thank Yinhua Lu for the gift of plasmid pSET152 m, Karine Robert, Isabelle Madore, Irène Kelsey and Anne-Marie Simao-Beaunoir for technical assistance and Ryszard Brzezinski for critical reading of the manuscript.

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The authors declare that they have no conflict of interest.

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Correspondence to Carole Beaulieu.

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Sanssouci, É., Lerat, S., Grondin, G. et al. tdd8: a TerD domain-encoding gene involved in Streptomyces coelicolor differentiation. Antonie van Leeuwenhoek 100, 385–398 (2011). https://doi.org/10.1007/s10482-011-9593-y

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