Topoisomerase IV is required for partitioning of circular chromosomes but not linear chromosomes in streptomyces

Tzu-Wen Huang, Chinchen Hsu, Hanyu Yang, Carton W. Chen

Research output: Contribution to journalArticle

3 Citations (Scopus)

Abstract

Filamentous bacteria of the genus Streptomyces possess linear chromosomes and linear plasmids. Theoretically, linear replicons may not need a decatenase for post-replicational separation of daughter molecules. Yet, Streptomyces contain parC and parE that encode the subunits for the decatenase topoisomerase IV. The linear replicons of Streptomyces adopt a circular configuration in vivo through telomere-telomere interaction, which would require decatenation, if the circular configuration persists through replication. We investigated whether topoisomerase IV is required for separation of the linear replicons in Streptomyces. Deletion of parE from the Streptomyces coelicolor chromosome was achieved, when parE was provided on a plasmid. Subsequently, the plasmid was eliminated at high temperature, and ΔparE mutants were obtained. These results indicated that topoisomerase IV was not essential for Streptomyces. Presumably, the telomere-telomere association may be resolved during or after replication to separate the daughter chromosomes. Nevertheless, the mutants exhibited retarded growth, defective sporulation and temperature sensitivity. In the mutants, circular plasmids could not replicate, and spontaneous circularization of the chromosome was not observed, indicating that topoisomerase IV was required for decatenation of circular replicons. Moreover, site-specific integration of a plasmid is impaired in the mutants, suggesting the formation of DNA knots during integration, which must be resolved by topoisomerase IV. © 2013 The Author(s).
Original languageEnglish
Pages (from-to)10403-10413
Number of pages11
JournalNucleic Acids Research
Volume41
Issue number22
DOIs
Publication statusPublished - 2013
Externally publishedYes

Fingerprint

DNA Topoisomerase IV
Streptomyces
Replicon
Telomere
Plasmids
Chromosomes
Streptomyces coelicolor
Temperature
Bacteria
DNA
Growth

Keywords

  • DNA topoisomerase IV
  • protein ParC
  • protein ParE
  • article
  • bacterial chromosome
  • bacterial gene
  • chromosome replication
  • controlled study
  • DNA integration
  • gene deletion
  • gene mutation
  • in vivo study
  • nonhuman
  • parC gene
  • parE gene
  • phase partitioning
  • plasmid
  • priority journal
  • replicon
  • sporogenesis
  • Streptomyces
  • telomere
  • temperature sensitivity
  • Chromosome Segregation
  • Chromosomes, Bacterial
  • DNA Topoisomerase IV
  • Gene Deletion
  • Plasmids

Cite this

Topoisomerase IV is required for partitioning of circular chromosomes but not linear chromosomes in streptomyces. / Huang, Tzu-Wen; Hsu, Chinchen; Yang, Hanyu; Chen, Carton W.

In: Nucleic Acids Research, Vol. 41, No. 22, 2013, p. 10403-10413.

Research output: Contribution to journalArticle

Huang, Tzu-Wen ; Hsu, Chinchen ; Yang, Hanyu ; Chen, Carton W. / Topoisomerase IV is required for partitioning of circular chromosomes but not linear chromosomes in streptomyces. In: Nucleic Acids Research. 2013 ; Vol. 41, No. 22. pp. 10403-10413.
@article{cc514a49288e4806a992244a7523941c,
title = "Topoisomerase IV is required for partitioning of circular chromosomes but not linear chromosomes in streptomyces",
abstract = "Filamentous bacteria of the genus Streptomyces possess linear chromosomes and linear plasmids. Theoretically, linear replicons may not need a decatenase for post-replicational separation of daughter molecules. Yet, Streptomyces contain parC and parE that encode the subunits for the decatenase topoisomerase IV. The linear replicons of Streptomyces adopt a circular configuration in vivo through telomere-telomere interaction, which would require decatenation, if the circular configuration persists through replication. We investigated whether topoisomerase IV is required for separation of the linear replicons in Streptomyces. Deletion of parE from the Streptomyces coelicolor chromosome was achieved, when parE was provided on a plasmid. Subsequently, the plasmid was eliminated at high temperature, and ΔparE mutants were obtained. These results indicated that topoisomerase IV was not essential for Streptomyces. Presumably, the telomere-telomere association may be resolved during or after replication to separate the daughter chromosomes. Nevertheless, the mutants exhibited retarded growth, defective sporulation and temperature sensitivity. In the mutants, circular plasmids could not replicate, and spontaneous circularization of the chromosome was not observed, indicating that topoisomerase IV was required for decatenation of circular replicons. Moreover, site-specific integration of a plasmid is impaired in the mutants, suggesting the formation of DNA knots during integration, which must be resolved by topoisomerase IV. {\circledC} 2013 The Author(s).",
keywords = "DNA topoisomerase IV, protein ParC, protein ParE, article, bacterial chromosome, bacterial gene, chromosome replication, controlled study, DNA integration, gene deletion, gene mutation, in vivo study, nonhuman, parC gene, parE gene, phase partitioning, plasmid, priority journal, replicon, sporogenesis, Streptomyces, telomere, temperature sensitivity, Chromosome Segregation, Chromosomes, Bacterial, DNA Topoisomerase IV, Gene Deletion, Plasmids",
author = "Tzu-Wen Huang and Chinchen Hsu and Hanyu Yang and Chen, {Carton W.}",
note = "被引用次數:2 Export Date: 1 April 2016 CODEN: NARHA 通訊地址: Chen, C.W.; Department of Life Sciences, Institute of Genome Sciences, National Yang-Ming University, Shih-Pai 112, Taiwan; 電子郵件: cwchen@ym.edu.tw 化學物質/CAS: DNA topoisomerase IV, 144941-31-1; DNA Topoisomerase IV, 5.99.1.- 參考文獻: Adams, D.E., Shekhtman, E.M., Zechiedrich, E.L., Schmid, M.B., Cozzarelli, N.R., The role of topoisomerase IV in partitioning bacterial replicons and the structure of catenated intermediates in DNA replication (1992) Cell, 71, pp. 277-288; Zechiedrich, E.L., Cozzarelli, N.R., Roles of topoisomerase IV and DNA gyrase in DNA unlinking during replication in Escherichia coli (1995) Genes Dev, 9, pp. 2859-2869; Hirota, Y., Ryter, A., Jacob, F., Thermosensitive mutants of E. Coli affected in the processes of DNA synthesis and cellular division (1968) Cold Spring Harb. Symp. Quant. Biol, 33, pp. 677-693; Kato, J., Nishimura, Y., Yamada, M., Suzuki, H., Hirota, Y., Gene organization in the region containing a new gene involved in chromosome partition in Escherichia coli (1988) J. Bacteriol, 170, pp. 3967-3977; Kreuzer, K.N., Cozzarelli, N.R., Escherichia coli mutants thermosensitive for deoxyribonucleic acid gyrase subunit A: Effects on deoxyribonucleic acid replication, transcription, and bacteriophage growth (1979) J. Bacteriol, 140, pp. 424-435; Kato, J., Suzuki, H., Ikeda, H., Purification and characterization of DNA topoisomerase IV in Escherichia coli (1992) J. Biol. Chem, 267, pp. 25676-25684; Champoux, J.J., DNA topoisomerases: Structure function, and mechanism (2001) Annu. Rev. Biochem, 70, pp. 369-413; Schmutz, E., Hennig, S., Li, S.M., Heide, L., Identification of a topoisomerase IV in actinobacteria: Purification and characterization of ParYR and GyrBR from the coumermycin A1 producer Streptomyces rishiriensis DSM 40489 (2004) Microbiology, 150, pp. 641-647; Manjunatha, U.H., Dalal, M., Chatterji, M., Radha, D.R., Visweswariah, S.S., Nagaraja, V., Functional characterisation of mycobacterial DNA gyrase: An efficient decatenase (2002) Nucleic Acids Res, 30, pp. 2144-2153; Chen, C.W., Huang, C.H., Lee, H.H., Tsai, H.H., Kirby, R., Once the circle has been broken: Dynamics and evolution of Streptomyces chromosomes (2002) Trends Genet, 18, pp. 522-529; Lin, Y.S., Kieser, H.M., Hopwood, D.A., Chen, C.W., The chromosomal DNA of Streptomyces lividans 66 is linear (1993) Mol. Microbiol, 10, pp. 923-933; Tsai, H.H., Huang, C.H., Tessmer, I., Erie, D.A., Chen, C.W., Linear Streptomyces plasmids form superhelical circles through interactions between their terminal proteins (2011) Nucleic Acids Res., 39, pp. 2165-2174; Dinardo, S., Voelkel, K., Sternglanz, R., DNA topoisomerase II mutant of Saccharomyces cerevisiae: Topoisomerase II is required for segregation of daughter molecules at the termination of DNA replication (1984) Proc. Natl Acad. Sci. USA, 81, pp. 2616-2620; Uemura, T., Ohkura, H., Adachi, Y., Morino, K., Shiozaki, K., Yanagida, M., DNA topoisomerase II is required for condensation and separation of mitotic chromosomes in S. Pombe (1987) Cell, 50, pp. 917-925; Hopwood, D.A., Kieser, T., Wright, H.M., Bibb, M.J., Plasmids recombination, and chromosomal mapping in Streptomyces lividans 66 (1983) J. Gen. Microbiol, 129, pp. 2257-2269; Weaver, D., Karoonuthaisiri, N., Tsai, H.H., Huang, C.H., Ho, M.L., Gai, S., Patel, K.G., Hopwood, D.A., Genome plasticity in Streptomyces: Identification of 1 Mb TIRs in the S. Coelicolor A3(2) chromosome (2004) Mol. Microbiol., 51, pp. 1530-1550; Gust, B., Challis, G.L., Fowler, K., Kieser, T., Chater, K.F., PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin (2003) Proc. Natl Acad. Sci. USA, 100, pp. 1541-1546; Paget, M.S., Chamberlin, L., Atrih, A., Foster, S.J., Buttner, M.J., Evidence that the extracytoplasmic function sigma factor sigmaE is required for normal cell wall structure in Streptomyces coelicolor A3(2) (1999) J. Bacteriol., 181, pp. 204-211; Redenbach, M., Kieser, H.M., Denapaite, D., Eichner, A., Cullum, J., Kinashi, H., Hopwood, D.A., A set of ordered cosmids and a detailed genetic and physical map for the 8 Mb Streptomyces coelicolor A3(2) chromosome (1996) Mol. Microbiol., 21, pp. 77-96; Hu, Z., Bao, K., Zhou, X., Zhou, Q., Hopwood, D.A., Kieser, T., Deng, Z., Repeated polyketide synthase modules involved in the biosynthesis of a heptaene macrolide by Streptomyces sp (1994) FR-008. Mol. Microbiol, 14, pp. 163-172; Huang, C.H., Chen, C.Y., Tsai, H.H., Chen, C., Lin, Y.S., Chen, C.W., Linear plasmid SLP2 of Streptomyces lividans is a composite replicon (2003) Mol. Microbiol, 47, pp. 1563-1576; Leu, W.M., Wu, S.Y., Lin, J.J., Lo, S.J., Lee, Y.H., Analysis of the promoter region of the melanin locus from Streptomyces antibioticus (1989) Gene, 84, pp. 267-277; Qin, Z., Cohen, S.N., Replication at the telomeres of the Streptomyces linear plasmid pSLA2 (1998) Mol. Microbiol, 28, pp. 893-904; Huang, C.H., Tsai, H.H., Tsay, Y.G., Chien, Y.N., Wang, S.L., Cheng, M.Y., Ke, C.H., Chen, C.W., The telomere system of the Streptomyces linear plasmid SCP1 represents a novel class (2007) Mol. Microbiol, 63, pp. 1710-1718; Bierman, M., Logan, R., O'Brien, K., Seno, E.T., Rao, R.N., Schoner, B.E., Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp (1992) Gene, 116, pp. 43-49; Kieser, T., Bibb, M., Buttner, M.J., Chater, K.F., Hopwood, D.A., (2000) Practical Streptomyces Genetics, , The John Innes Foundation, Norwich; Sambrook, J., MacCallum, P., Russel, D., (2001) Molecular Cloning. 3rd Edn, , Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York; Lee, L.F., Chen, Y.J., Kirby, R., Chen, C., Chen, C.W., A multidrug efflux system is involved in colony growth in Streptomyces lividans (2007) Microbiology, 153, pp. 924-934; Kanehisa, M., Goto, S., Sato, Y., Furumichi, M., Tanabe, M., KEGG for integration and interpretation of large-scale molecular data sets (2012) Nucleic Acids Res., 40, pp. D109-D114; Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., Kumar, S., MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods (2011) Mol. Biol. Evol., 28, pp. 2731-2739; Huang, T.W., Chen, C.W., A recA null mutation may be generated in Streptomyces coelicolor (2006) J. Bacteriol, 188, pp. 6771-6779; Huang, T.W., Chen, C.W., DNA polymerase i is not required for replication of linear chromosomes in Streptomyces (2008) J. Bacteriol, 190, pp. 755-758; Hsu, C.C., Chen, C.W., Linear plasmid SLP2 is maintained by partitioning, intrahyphal spread, and conjugal transfer in Streptomyces (2010) J. Bacteriol., 192, pp. 307-315; Redenbach, M., Flett, F., Piendl, W., Glocker, I., Rauland, U., Wafzig, O., Leblond, P., Cullum, J., The Streptomyces lividans 66 chromosome contains a 1 Mb deletogenic region flanked by two amplifiable regions (1993) Mol. Gen. Genet, 241, pp. 255-262; Kato, J.I., Nishimura, Y., Imamura, R., Niki, H., Hiraga, S., Suzuki, H., New topoisomerase essential for chromosome segregation in E. Coli (1990) Cell, 63, pp. 393-404; Chen, C.W., (2007) Microbial Linear Plasmids, pp. 33-61. , Meinhardt, F. and Klassen, R. (eds) Springer Verlag, Berlin, Heidelberg; Holm, C., Goto, T., Wang, J.C., Botstein, D., DNA topoisomerase II is required at the time of mitosis in yeast (1985) Cell, 41, pp. 553-563; Holm, C., Stearns, T., Botstein, D., DNA topoisomerase II must act at mitosis to prevent nondisjunction and chromosome breakage (1989) Mol. Cel. Biol, 9, pp. 159-168; Funabiki, H., Hagan, I., Uzawa, S., Yanagida, M., Cell cycle-dependent specific positioning and clustering of centromeres and telomeres in fission yeast (1993) J. Cell Biol, 121, pp. 961-976; Spell, R.M., Holm, C., Nature and distribution of chromosomal intertwinings in Saccharomyces cerevisiae (1994) Mol. Cell. Biol, 14, pp. 1465-1476; Graeme-Cook, K.A., May, G., Bremer, E., Higgins, C.F., Osmotic regulation of porin expression: A role for DNA supercoiling (1989) Mol. Microbiol, 3, pp. 1287-1294; Higgins, C.F., Dorman, C.J., Stirling, D.A., Waddell, L., Booth, I.R., May, G., Bremer, E., A physiological role for DNA supercoiling in the osmotic regulation of gene expression in S. Typhimurium and E. Coli (1988) Cell, 52, pp. 569-584; Bhriain, N.N., Dorman, C.J., Isolation and characterization of a topA mutant of Shigella flexneri (1993) Mol. Microbiol, 7, pp. 351-358; Zechiedrich, E.L., Khodursky, A.B., Cozzarelli, N.R., Topoisomerase IV, not gyrase, decatenates products of sitespecific recombination in Escherichia coli (1997) Genes Dev, 11, pp. 2580-2592; Lopez, V., Martnez-Robles, M.L., Hernandez, P., Krimer, D.B., Schvartzman, J.B., Topo IV is the topoisomerase that knots and unknots sister duplexes during DNA replication (2012) Nucleic Acids Res., 40, pp. 3563-3573",
year = "2013",
doi = "10.1093/nar/gkt757",
language = "English",
volume = "41",
pages = "10403--10413",
journal = "Nucleic Acids Research",
issn = "0305-1048",
publisher = "Oxford University Press",
number = "22",

}

TY - JOUR

T1 - Topoisomerase IV is required for partitioning of circular chromosomes but not linear chromosomes in streptomyces

AU - Huang, Tzu-Wen

AU - Hsu, Chinchen

AU - Yang, Hanyu

AU - Chen, Carton W.

N1 - 被引用次數:2 Export Date: 1 April 2016 CODEN: NARHA 通訊地址: Chen, C.W.; Department of Life Sciences, Institute of Genome Sciences, National Yang-Ming University, Shih-Pai 112, Taiwan; 電子郵件: cwchen@ym.edu.tw 化學物質/CAS: DNA topoisomerase IV, 144941-31-1; DNA Topoisomerase IV, 5.99.1.- 參考文獻: Adams, D.E., Shekhtman, E.M., Zechiedrich, E.L., Schmid, M.B., Cozzarelli, N.R., The role of topoisomerase IV in partitioning bacterial replicons and the structure of catenated intermediates in DNA replication (1992) Cell, 71, pp. 277-288; Zechiedrich, E.L., Cozzarelli, N.R., Roles of topoisomerase IV and DNA gyrase in DNA unlinking during replication in Escherichia coli (1995) Genes Dev, 9, pp. 2859-2869; Hirota, Y., Ryter, A., Jacob, F., Thermosensitive mutants of E. Coli affected in the processes of DNA synthesis and cellular division (1968) Cold Spring Harb. Symp. Quant. Biol, 33, pp. 677-693; Kato, J., Nishimura, Y., Yamada, M., Suzuki, H., Hirota, Y., Gene organization in the region containing a new gene involved in chromosome partition in Escherichia coli (1988) J. Bacteriol, 170, pp. 3967-3977; Kreuzer, K.N., Cozzarelli, N.R., Escherichia coli mutants thermosensitive for deoxyribonucleic acid gyrase subunit A: Effects on deoxyribonucleic acid replication, transcription, and bacteriophage growth (1979) J. Bacteriol, 140, pp. 424-435; Kato, J., Suzuki, H., Ikeda, H., Purification and characterization of DNA topoisomerase IV in Escherichia coli (1992) J. Biol. Chem, 267, pp. 25676-25684; Champoux, J.J., DNA topoisomerases: Structure function, and mechanism (2001) Annu. Rev. Biochem, 70, pp. 369-413; Schmutz, E., Hennig, S., Li, S.M., Heide, L., Identification of a topoisomerase IV in actinobacteria: Purification and characterization of ParYR and GyrBR from the coumermycin A1 producer Streptomyces rishiriensis DSM 40489 (2004) Microbiology, 150, pp. 641-647; Manjunatha, U.H., Dalal, M., Chatterji, M., Radha, D.R., Visweswariah, S.S., Nagaraja, V., Functional characterisation of mycobacterial DNA gyrase: An efficient decatenase (2002) Nucleic Acids Res, 30, pp. 2144-2153; Chen, C.W., Huang, C.H., Lee, H.H., Tsai, H.H., Kirby, R., Once the circle has been broken: Dynamics and evolution of Streptomyces chromosomes (2002) Trends Genet, 18, pp. 522-529; Lin, Y.S., Kieser, H.M., Hopwood, D.A., Chen, C.W., The chromosomal DNA of Streptomyces lividans 66 is linear (1993) Mol. Microbiol, 10, pp. 923-933; Tsai, H.H., Huang, C.H., Tessmer, I., Erie, D.A., Chen, C.W., Linear Streptomyces plasmids form superhelical circles through interactions between their terminal proteins (2011) Nucleic Acids Res., 39, pp. 2165-2174; Dinardo, S., Voelkel, K., Sternglanz, R., DNA topoisomerase II mutant of Saccharomyces cerevisiae: Topoisomerase II is required for segregation of daughter molecules at the termination of DNA replication (1984) Proc. Natl Acad. Sci. USA, 81, pp. 2616-2620; Uemura, T., Ohkura, H., Adachi, Y., Morino, K., Shiozaki, K., Yanagida, M., DNA topoisomerase II is required for condensation and separation of mitotic chromosomes in S. Pombe (1987) Cell, 50, pp. 917-925; Hopwood, D.A., Kieser, T., Wright, H.M., Bibb, M.J., Plasmids recombination, and chromosomal mapping in Streptomyces lividans 66 (1983) J. Gen. Microbiol, 129, pp. 2257-2269; Weaver, D., Karoonuthaisiri, N., Tsai, H.H., Huang, C.H., Ho, M.L., Gai, S., Patel, K.G., Hopwood, D.A., Genome plasticity in Streptomyces: Identification of 1 Mb TIRs in the S. Coelicolor A3(2) chromosome (2004) Mol. Microbiol., 51, pp. 1530-1550; Gust, B., Challis, G.L., Fowler, K., Kieser, T., Chater, K.F., PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin (2003) Proc. Natl Acad. Sci. USA, 100, pp. 1541-1546; Paget, M.S., Chamberlin, L., Atrih, A., Foster, S.J., Buttner, M.J., Evidence that the extracytoplasmic function sigma factor sigmaE is required for normal cell wall structure in Streptomyces coelicolor A3(2) (1999) J. Bacteriol., 181, pp. 204-211; Redenbach, M., Kieser, H.M., Denapaite, D., Eichner, A., Cullum, J., Kinashi, H., Hopwood, D.A., A set of ordered cosmids and a detailed genetic and physical map for the 8 Mb Streptomyces coelicolor A3(2) chromosome (1996) Mol. Microbiol., 21, pp. 77-96; Hu, Z., Bao, K., Zhou, X., Zhou, Q., Hopwood, D.A., Kieser, T., Deng, Z., Repeated polyketide synthase modules involved in the biosynthesis of a heptaene macrolide by Streptomyces sp (1994) FR-008. Mol. Microbiol, 14, pp. 163-172; Huang, C.H., Chen, C.Y., Tsai, H.H., Chen, C., Lin, Y.S., Chen, C.W., Linear plasmid SLP2 of Streptomyces lividans is a composite replicon (2003) Mol. Microbiol, 47, pp. 1563-1576; Leu, W.M., Wu, S.Y., Lin, J.J., Lo, S.J., Lee, Y.H., Analysis of the promoter region of the melanin locus from Streptomyces antibioticus (1989) Gene, 84, pp. 267-277; Qin, Z., Cohen, S.N., Replication at the telomeres of the Streptomyces linear plasmid pSLA2 (1998) Mol. Microbiol, 28, pp. 893-904; Huang, C.H., Tsai, H.H., Tsay, Y.G., Chien, Y.N., Wang, S.L., Cheng, M.Y., Ke, C.H., Chen, C.W., The telomere system of the Streptomyces linear plasmid SCP1 represents a novel class (2007) Mol. Microbiol, 63, pp. 1710-1718; Bierman, M., Logan, R., O'Brien, K., Seno, E.T., Rao, R.N., Schoner, B.E., Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp (1992) Gene, 116, pp. 43-49; Kieser, T., Bibb, M., Buttner, M.J., Chater, K.F., Hopwood, D.A., (2000) Practical Streptomyces Genetics, , The John Innes Foundation, Norwich; Sambrook, J., MacCallum, P., Russel, D., (2001) Molecular Cloning. 3rd Edn, , Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York; Lee, L.F., Chen, Y.J., Kirby, R., Chen, C., Chen, C.W., A multidrug efflux system is involved in colony growth in Streptomyces lividans (2007) Microbiology, 153, pp. 924-934; Kanehisa, M., Goto, S., Sato, Y., Furumichi, M., Tanabe, M., KEGG for integration and interpretation of large-scale molecular data sets (2012) Nucleic Acids Res., 40, pp. D109-D114; Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., Kumar, S., MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods (2011) Mol. Biol. Evol., 28, pp. 2731-2739; Huang, T.W., Chen, C.W., A recA null mutation may be generated in Streptomyces coelicolor (2006) J. Bacteriol, 188, pp. 6771-6779; Huang, T.W., Chen, C.W., DNA polymerase i is not required for replication of linear chromosomes in Streptomyces (2008) J. Bacteriol, 190, pp. 755-758; Hsu, C.C., Chen, C.W., Linear plasmid SLP2 is maintained by partitioning, intrahyphal spread, and conjugal transfer in Streptomyces (2010) J. Bacteriol., 192, pp. 307-315; Redenbach, M., Flett, F., Piendl, W., Glocker, I., Rauland, U., Wafzig, O., Leblond, P., Cullum, J., The Streptomyces lividans 66 chromosome contains a 1 Mb deletogenic region flanked by two amplifiable regions (1993) Mol. Gen. Genet, 241, pp. 255-262; Kato, J.I., Nishimura, Y., Imamura, R., Niki, H., Hiraga, S., Suzuki, H., New topoisomerase essential for chromosome segregation in E. Coli (1990) Cell, 63, pp. 393-404; Chen, C.W., (2007) Microbial Linear Plasmids, pp. 33-61. , Meinhardt, F. and Klassen, R. (eds) Springer Verlag, Berlin, Heidelberg; Holm, C., Goto, T., Wang, J.C., Botstein, D., DNA topoisomerase II is required at the time of mitosis in yeast (1985) Cell, 41, pp. 553-563; Holm, C., Stearns, T., Botstein, D., DNA topoisomerase II must act at mitosis to prevent nondisjunction and chromosome breakage (1989) Mol. Cel. Biol, 9, pp. 159-168; Funabiki, H., Hagan, I., Uzawa, S., Yanagida, M., Cell cycle-dependent specific positioning and clustering of centromeres and telomeres in fission yeast (1993) J. Cell Biol, 121, pp. 961-976; Spell, R.M., Holm, C., Nature and distribution of chromosomal intertwinings in Saccharomyces cerevisiae (1994) Mol. Cell. Biol, 14, pp. 1465-1476; Graeme-Cook, K.A., May, G., Bremer, E., Higgins, C.F., Osmotic regulation of porin expression: A role for DNA supercoiling (1989) Mol. Microbiol, 3, pp. 1287-1294; Higgins, C.F., Dorman, C.J., Stirling, D.A., Waddell, L., Booth, I.R., May, G., Bremer, E., A physiological role for DNA supercoiling in the osmotic regulation of gene expression in S. Typhimurium and E. Coli (1988) Cell, 52, pp. 569-584; Bhriain, N.N., Dorman, C.J., Isolation and characterization of a topA mutant of Shigella flexneri (1993) Mol. Microbiol, 7, pp. 351-358; Zechiedrich, E.L., Khodursky, A.B., Cozzarelli, N.R., Topoisomerase IV, not gyrase, decatenates products of sitespecific recombination in Escherichia coli (1997) Genes Dev, 11, pp. 2580-2592; Lopez, V., Martnez-Robles, M.L., Hernandez, P., Krimer, D.B., Schvartzman, J.B., Topo IV is the topoisomerase that knots and unknots sister duplexes during DNA replication (2012) Nucleic Acids Res., 40, pp. 3563-3573

PY - 2013

Y1 - 2013

N2 - Filamentous bacteria of the genus Streptomyces possess linear chromosomes and linear plasmids. Theoretically, linear replicons may not need a decatenase for post-replicational separation of daughter molecules. Yet, Streptomyces contain parC and parE that encode the subunits for the decatenase topoisomerase IV. The linear replicons of Streptomyces adopt a circular configuration in vivo through telomere-telomere interaction, which would require decatenation, if the circular configuration persists through replication. We investigated whether topoisomerase IV is required for separation of the linear replicons in Streptomyces. Deletion of parE from the Streptomyces coelicolor chromosome was achieved, when parE was provided on a plasmid. Subsequently, the plasmid was eliminated at high temperature, and ΔparE mutants were obtained. These results indicated that topoisomerase IV was not essential for Streptomyces. Presumably, the telomere-telomere association may be resolved during or after replication to separate the daughter chromosomes. Nevertheless, the mutants exhibited retarded growth, defective sporulation and temperature sensitivity. In the mutants, circular plasmids could not replicate, and spontaneous circularization of the chromosome was not observed, indicating that topoisomerase IV was required for decatenation of circular replicons. Moreover, site-specific integration of a plasmid is impaired in the mutants, suggesting the formation of DNA knots during integration, which must be resolved by topoisomerase IV. © 2013 The Author(s).

AB - Filamentous bacteria of the genus Streptomyces possess linear chromosomes and linear plasmids. Theoretically, linear replicons may not need a decatenase for post-replicational separation of daughter molecules. Yet, Streptomyces contain parC and parE that encode the subunits for the decatenase topoisomerase IV. The linear replicons of Streptomyces adopt a circular configuration in vivo through telomere-telomere interaction, which would require decatenation, if the circular configuration persists through replication. We investigated whether topoisomerase IV is required for separation of the linear replicons in Streptomyces. Deletion of parE from the Streptomyces coelicolor chromosome was achieved, when parE was provided on a plasmid. Subsequently, the plasmid was eliminated at high temperature, and ΔparE mutants were obtained. These results indicated that topoisomerase IV was not essential for Streptomyces. Presumably, the telomere-telomere association may be resolved during or after replication to separate the daughter chromosomes. Nevertheless, the mutants exhibited retarded growth, defective sporulation and temperature sensitivity. In the mutants, circular plasmids could not replicate, and spontaneous circularization of the chromosome was not observed, indicating that topoisomerase IV was required for decatenation of circular replicons. Moreover, site-specific integration of a plasmid is impaired in the mutants, suggesting the formation of DNA knots during integration, which must be resolved by topoisomerase IV. © 2013 The Author(s).

KW - DNA topoisomerase IV

KW - protein ParC

KW - protein ParE

KW - article

KW - bacterial chromosome

KW - bacterial gene

KW - chromosome replication

KW - controlled study

KW - DNA integration

KW - gene deletion

KW - gene mutation

KW - in vivo study

KW - nonhuman

KW - parC gene

KW - parE gene

KW - phase partitioning

KW - plasmid

KW - priority journal

KW - replicon

KW - sporogenesis

KW - Streptomyces

KW - telomere

KW - temperature sensitivity

KW - Chromosome Segregation

KW - Chromosomes, Bacterial

KW - DNA Topoisomerase IV

KW - Gene Deletion

KW - Plasmids

U2 - 10.1093/nar/gkt757

DO - 10.1093/nar/gkt757

M3 - Article

VL - 41

SP - 10403

EP - 10413

JO - Nucleic Acids Research

JF - Nucleic Acids Research

SN - 0305-1048

IS - 22

ER -