Tubulin homolog TubZ in a phage-encoded partition system
10.1073/pnas.1121546109
Crossref journal-article
Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences (341)
Abstract

Partition systems are responsible for the process whereby large and essential plasmids are accurately positioned to daughter cells during bacterial division. They are typically made of three components: a centromere-like DNA zone, an adaptor protein, and an assembling protein that is either a Walker-box ATPase (type I) or an actin-like ATPase (type II). A recently described type III segregation system has a tubulin/FtsZ-like protein, called TubZ, for plasmid movement. Here, we present the 2.3 Å structure and dynamic assembly of a TubZ tubulin homolog from a bacteriophage and unravel the Clostridium botulinum phage c-st type III partition system. Using biochemical and biophysical approaches, we prove that a gene upstream from tubZ encodes the partner TubR and localize the centromeric region ( tubS ), both of which are essential for anchoring phage DNA to the motile TubZ filaments. Finally, we describe a conserved fourth component, TubY, which modulates the TubZ-R- S complex interaction.

Bibliography

Oliva, M. A., Martin-Galiano, A. J., Sakaguchi, Y., & Andreu, J. M. (2012). Tubulin homolog TubZ in a phage-encoded partition system. Proceedings of the National Academy of Sciences, 109(20), 7711–7716.

Authors 4
  1. María A. Oliva (first)
  2. Antonio J. Martin-Galiano (additional)
  3. Yoshihiko Sakaguchi (additional)
  4. José M. Andreu (additional)
References 31 Referenced 54
  1. K Gerdes, J Møller-Jensen, R Bugge Jensen, Plasmid and chromosome partitioning: Surprises from phylogeny. Mol Microbiol 37, 455–466 (2000). (10.1046/j.1365-2958.2000.01975.x) / Mol Microbiol / Plasmid and chromosome partitioning: Surprises from phylogeny by Gerdes K (2000)
  2. E Nogales, KH Downing, LA Amos, J Löwe, Tubulin and FtsZ form a distinct family of GTPases. Nat Struct Biol 5, 451–458 (1998). (10.1038/nsb0698-451) / Nat Struct Biol / Tubulin and FtsZ form a distinct family of GTPases by Nogales E (1998)
  3. MA Oliva, SC Cordell, J Löwe, Structural insights into FtsZ protofilament formation. Nat Struct Mol Biol 11, 1243–1250 (2004). (10.1038/nsmb855) / Nat Struct Mol Biol / Structural insights into FtsZ protofilament formation by Oliva MA (2004)
  4. E Tinsley, SA Khan, A novel FtsZ-like protein is involved in replication of the anthrax toxin-encoding pXO1 plasmid in Bacillus anthracis. J Bacteriol 188, 2829–2835 (2006). (10.1128/JB.188.8.2829-2835.2006) / J Bacteriol / A novel FtsZ-like protein is involved in replication of the anthrax toxin-encoding pXO1 plasmid in Bacillus anthracis by Tinsley E (2006)
  5. M Tang, DK Bideshi, HW Park, BA Federici, Minireplicon from pBtoxis of Bacillus thuringiensis subsp. israelensis. Appl Environ Microbiol 72, 6948–6954 (2006). (10.1128/AEM.00976-06) / Appl Environ Microbiol / Minireplicon from pBtoxis of Bacillus thuringiensis subsp. israelensis by Tang M (2006)
  6. RA Larsen, et al., Treadmilling of a prokaryotic tubulin-like protein, TubZ, required for plasmid stability in Bacillus thuringiensis. Genes Dev 21, 1340–1352 (2007). (10.1101/gad.1546107) / Genes Dev / Treadmilling of a prokaryotic tubulin-like protein, TubZ, required for plasmid stability in Bacillus thuringiensis by Larsen RA (2007)
  7. L Ni, W Xu, M Kumaraswami, MA Schumacher, Plasmid protein TubR uses a distinct mode of HTH-DNA binding and recruits the prokaryotic tubulin homolog TubZ to effect DNA partition. Proc Natl Acad Sci USA 107, 11763–11768 (2010). (10.1073/pnas.1003817107) / Proc Natl Acad Sci USA / Plasmid protein TubR uses a distinct mode of HTH-DNA binding and recruits the prokaryotic tubulin homolog TubZ to effect DNA partition by Ni L (2010)
  8. CH Aylett, Q Wang, KA Michie, LA Amos, J Löwe, Filament structure of bacterial tubulin homologue TubZ. Proc Natl Acad Sci USA 107, 19766–19771 (2010). (10.1073/pnas.1010176107) / Proc Natl Acad Sci USA / Filament structure of bacterial tubulin homologue TubZ by Aylett CH (2010)
  9. Y Chen, HP Erickson, In vitro assembly studies of FtsZ/tubulin-like proteins (TubZ) from Bacillus plasmids: Evidence for a capping mechanism. J Biol Chem 283, 8102–8109 (2008). (10.1074/jbc.M709163200) / J Biol Chem / In vitro assembly studies of FtsZ/tubulin-like proteins (TubZ) from Bacillus plasmids: Evidence for a capping mechanism by Chen Y (2008)
  10. Y Sakaguchi, et al., The genome sequence of Clostridium botulinum type C neurotoxin-converting phage and the molecular mechanisms of unstable lysogeny. Proc Natl Acad Sci USA 102, 17472–17477 (2005). (10.1073/pnas.0505503102) / Proc Natl Acad Sci USA / The genome sequence of Clostridium botulinum type C neurotoxin-converting phage and the molecular mechanisms of unstable lysogeny by Sakaguchi Y (2005)
  11. MW Eklund, FT Poysky, SM Reed, CA Smith, Bacteriophage and the toxigenicity of Clostridium botulinum type C. Science 172, 480–482 (1971). (10.1126/science.172.3982.480) / Science / Bacteriophage and the toxigenicity of Clostridium botulinum type C by Eklund MW (1971)
  12. M Tang, DK Bideshi, HW Park, BA Federici, Iteron-binding ORF157 and FtsZ-like ORF156 proteins encoded by pBtoxis play a role in its replication in Bacillus thuringiensis subsp. israelensis. J Bacteriol 189, 8053–8058 (2007). (10.1128/JB.00908-07) / J Bacteriol / Iteron-binding ORF157 and FtsZ-like ORF156 proteins encoded by pBtoxis play a role in its replication in Bacillus thuringiensis subsp. israelensis by Tang M (2007)
  13. F Long, AA Vagin, P Young, GN Murshudov, BALBES: A molecular-replacement pipeline. Acta Crystallogr D Biol Crystallogr 64, 125–132 (2008). (10.1107/S0907444907050172) / Acta Crystallogr D Biol Crystallogr / BALBES: A molecular-replacement pipeline by Long F (2008)
  14. S Panjikar, V Parthasarathy, VS Lamzin, MS Weiss, PA Tucker, Auto-rickshaw: An automated crystal structure determination platform as an efficient tool for the validation of an X-ray diffraction experiment. Acta Crystallogr D Biol Crystallogr 61, 449–457 (2005). (10.1107/S0907444905001307) / Acta Crystallogr D Biol Crystallogr / Auto-rickshaw: An automated crystal structure determination platform as an efficient tool for the validation of an X-ray diffraction experiment by Panjikar S (2005)
  15. JF Díaz, et al., Activation of cell division protein FtsZ. Control of switch loop T3 conformation by the nucleotide gamma-phosphate. J Biol Chem 276, 17307–17315 (2001). / J Biol Chem / Activation of cell division protein FtsZ. Control of switch loop T3 conformation by the nucleotide gamma-phosphate by Díaz JF (2001)
  16. E Nogales, When cytoskeletal worlds collide. Proc Natl Acad Sci USA 107, 19609–19610 (2010). (10.1073/pnas.1014665107) / Proc Natl Acad Sci USA / When cytoskeletal worlds collide by Nogales E (2010)
  17. SP Anand, P Akhtar, E Tinsley, SC Watkins, SA Khan, GTP-dependent polymerization of the tubulin-like RepX replication protein encoded by the pXO1 plasmid of Bacillus anthracis. Mol Microbiol 67, 881–890 (2008). (10.1111/j.1365-2958.2007.06100.x) / Mol Microbiol / GTP-dependent polymerization of the tubulin-like RepX replication protein encoded by the pXO1 plasmid of Bacillus anthracis by Anand SP (2008)
  18. AA Hyman, S Salser, DN Drechsel, N Unwin, TJ Mitchison, Role of GTP hydrolysis in microtubule dynamics: Information from a slowly hydrolyzable analogue, GMPCPP. Mol Biol Cell 3, 1155–1167 (1992). (10.1091/mbc.3.10.1155) / Mol Biol Cell / Role of GTP hydrolysis in microtubule dynamics: Information from a slowly hydrolyzable analogue, GMPCPP by Hyman AA (1992)
  19. MA Oliva, et al., Assembly of archaeal cell division protein FtsZ and a GTPase-inactive mutant into double-stranded filaments. J Biol Chem 278, 33562–33570 (2003). (10.1074/jbc.M303798200) / J Biol Chem / Assembly of archaeal cell division protein FtsZ and a GTPase-inactive mutant into double-stranded filaments by Oliva MA (2003)
  20. DJ Scheffers, T den Blaauwen, AJ Driessen, Non-hydrolysable GTP-gamma-S stabilizes the FtsZ polymer in a GDP-bound state. Mol Microbiol 35, 1211–1219 (2000). (10.1046/j.1365-2958.2000.01791.x) / Mol Microbiol / Non-hydrolysable GTP-gamma-S stabilizes the FtsZ polymer in a GDP-bound state by Scheffers DJ (2000)
  21. MA Schumacher, Bacterial plasmid partition machinery: A minimalist approach to survival. Curr Opin Struct Biol 22, 72–79 (2012). (10.1016/j.sbi.2011.11.001) / Curr Opin Struct Biol / Bacterial plasmid partition machinery: A minimalist approach to survival by Schumacher MA (2012)
  22. J Lawrence, Selfish operons: The evolutionary impact of gene clustering in prokaryotes and eukaryotes. Curr Opin Genet Dev 9, 642–648 (1999). (10.1016/S0959-437X(99)00025-8) / Curr Opin Genet Dev / Selfish operons: The evolutionary impact of gene clustering in prokaryotes and eukaryotes by Lawrence J (1999)
  23. P Montero Llopis, et al., Spatial organization of the flow of genetic information in bacteria. Nature 466, 77–81 (2010). (10.1038/nature09152) / Nature / Spatial organization of the flow of genetic information in bacteria by Montero Llopis P (2010)
  24. AE Simpson, RA Skurray, N Firth, A single gene on the staphylococcal multiresistance plasmid pSK1 encodes a novel partitioning system. J Bacteriol 185, 2143–2152 (2003). (10.1128/JB.185.7.2143-2152.2003) / J Bacteriol / A single gene on the staphylococcal multiresistance plasmid pSK1 encodes a novel partitioning system by Simpson AE (2003)
  25. F Hayes, D Barillà, The bacterial segrosome: A dynamic nucleoprotein machine for DNA trafficking and segregation. Nat Rev Microbiol 4, 133–143 (2006). (10.1038/nrmicro1342) / Nat Rev Microbiol / The bacterial segrosome: A dynamic nucleoprotein machine for DNA trafficking and segregation by Hayes F (2006)
  26. TD Dunham, W Xu, BE Funnell, MA Schumacher, Structural basis for ADP-mediated transcriptional regulation by P1 and P7 ParA. EMBO J 28, 1792–1802 (2009). (10.1038/emboj.2009.120) / EMBO J / Structural basis for ADP-mediated transcriptional regulation by P1 and P7 ParA by Dunham TD (2009)
  27. Y Sakaguchi, et al., Molecular analysis of an extrachromosomal element containing the C2 toxin gene discovered in Clostridium botulinum type C. J Bacteriol 191, 3282–3291 (2009). (10.1128/JB.01797-08) / J Bacteriol / Molecular analysis of an extrachromosomal element containing the C2 toxin gene discovered in Clostridium botulinum type C by Sakaguchi Y (2009)
  28. PS Lee, AD Grossman, The chromosome partitioning proteins Soj (ParA) and Spo0J (ParB) contribute to accurate chromosome partitioning, separation of replicated sister origins, and regulation of replication initiation in Bacillus subtilis. Mol Microbiol 60, 853–869 (2006). (10.1111/j.1365-2958.2006.05140.x) / Mol Microbiol / The chromosome partitioning proteins Soj (ParA) and Spo0J (ParB) contribute to accurate chromosome partitioning, separation of replicated sister origins, and regulation of replication initiation in Bacillus subtilis by Lee PS (2006)
  29. NS Baliga, et al., Genome sequence of Haloarcula marismortui: A halophilic archaeon from the Dead Sea. Genome Res 14, 2221–2234 (2004). (10.1101/gr.2700304) / Genome Res / Genome sequence of Haloarcula marismortui: A halophilic archaeon from the Dead Sea by Baliga NS (2004)
  30. TJ Fothergill, D Barillà, F Hayes, Protein diversity confers specificity in plasmid segregation. J Bacteriol 187, 2651–2661 (2005). (10.1128/JB.187.8.2651-2661.2005) / J Bacteriol / Protein diversity confers specificity in plasmid segregation by Fothergill TJ (2005)
  31. N Fujii, K Oguma, N Yokosawa, K Kimura, K Tsuzuki, Characterization of bacteriophage nucleic acids obtained from Clostridium botulinum types C and D. Appl Environ Microbiol 54, 69–73 (1988). (10.1128/aem.54.1.69-73.1988) / Appl Environ Microbiol / Characterization of bacteriophage nucleic acids obtained from Clostridium botulinum types C and D by Fujii N (1988)
Dates
Type When
Created 13 years, 4 months ago (April 26, 2012, 8:49 p.m.)
Deposited 3 years, 2 months ago (June 7, 2022, 4:32 a.m.)
Indexed 1 day, 12 hours ago (Aug. 31, 2025, 6:13 a.m.)
Issued 13 years, 4 months ago (April 26, 2012)
Published 13 years, 4 months ago (April 26, 2012)
Published Online 13 years, 4 months ago (April 26, 2012)
Published Print 13 years, 3 months ago (May 15, 2012)
Funders 0

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@article{Oliva_2012, title={Tubulin homolog TubZ in a phage-encoded partition system}, volume={109}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.1121546109}, DOI={10.1073/pnas.1121546109}, number={20}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Oliva, María A. and Martin-Galiano, Antonio J. and Sakaguchi, Yoshihiko and Andreu, José M.}, year={2012}, month=apr, pages={7711–7716} }