Abstract
A family of tubulin-related proteins (TubZs) has been identified in prokaryotes as being important for the inheritance of virulence plasmids of several pathogenic Bacilli and also being implicated in the lysogenic life cycle of several bacteriophages. Cell biological studies and reconstitution experiments revealed that TubZs function as prokaryotic cytomotive filaments, providing one-dimensional motive forces. Plasmid-borne TubZ filaments most likely transport plasmid centromeric complexes by depolymerisation, pulling on the plasmid DNA, in vitro. In contrast, phage-borne TubZ (PhuZ) pushes bacteriophage particles (virions) to mid cell by filament growth. Structural studies by both crystallography and electron cryo-microscopy of multiple proteins, both from the plasmid partitioning sub-group and the bacteriophage virion centring group of TubZ homologues, allow a detailed consideration of the structural phylogeny of the group as a whole, while complete structures of both crystallographic protofilaments at high resolution and fully polymerised filaments at intermediate resolution by cryo-EM have revealed details of the polymerisation behaviour of both TubZ sub-groups.
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References
Akhtar P, Anand SP, Watkins SC, Khan SA (2009) The tubulin-like RepX protein encoded by the pXO1 plasmid forms polymers in vivo in Bacillus anthracis. J Bacteriol 191:2493–2500
Anand SP, Akhtar P, Tinsley E, Watkins SC, Khan SA (2008) GTP-dependent polymerization of the tubulin-like RepX replication protein encoded by the pXO1 plasmid of Bacillus anthracis. Mol Microbiol 67:881–890
Aylett CH, Lowe J (2012) Superstructure of the centromeric complex of TubZRC plasmid partitioning systems. Proc Natl Acad Sci U S A 109:16522–16527
Aylett CH, Wang Q, Michie KA, Amos LA, Lowe J (2010) Filament structure of bacterial tubulin homologue TubZ. Proc Natl Acad Sci U S A 107:19766–19771
Aylett CH, Izore T, Amos LA, Lowe J (2013) Structure of the tubulin/FtsZ-like protein TubZ from Pseudomonas bacteriophage PhiKZ. J Mol Biol 425:2164–2173
Barilla D (2010) One-way ticket to the cell pole: plasmid transport by the prokaryotic tubulin homolog TubZ. Proc Natl Acad Sci U S A 107:12061–12062
Berry C, O’neil S, Ben-Dov E, Jones AF, Murphy L, Quail MA, Holden MT, Harris D, Zaritsky A, Parkhill J (2002) Complete sequence and organization of pBtoxis, the toxin-coding plasmid of Bacillus thuringiensis subsp. israelensis. Appl Environ Microbiol 68:5082–5095
Chen Y, Erickson HP (2008) In vitro assembly studies of FtsZ/tubulin-like proteins (TubZ) from Bacillus plasmids: evidence for a capping mechanism. J Biol Chem 283:8102–8109
Duggin IG, Aylett CH, Walsh JC, Michie KA, Wang Q, Turnbull L, Dawson EM, Harry EJ, Whitchurch CB, Amos LA, Lowe J (2015) CetZ tubulin-like proteins control archaeal cell shape. Nature 519:362–365
Erb ML, Kraemer JA, Coker JK, Chaikeeratisak V, Nonejuie P, Agard DA, Pogliano J (2014) A bacteriophage tubulin harnesses dynamic instability to center DNA in infected cells. Elife:3
Fink G, Lowe J (2015) Reconstitution of a prokaryotic minus end-tracking system using TubRC centromeric complexes and tubulin-like protein TubZ filaments. Proc Natl Acad Sci U S A 112:E1845–E1850
Garner EC, Campbell CS, Mullins RD (2004) Dynamic instability in a DNA-segregating prokaryotic actin homolog. Science 306:1021–1025
Garner EC, Campbell CS, Weibel DB, Mullins RD (2007) Reconstitution of DNA segregation driven by assembly of a prokaryotic actin homolog. Science 315:1270–1274
Gayathri P, Fujii T, Moller-Jensen J, van Den Ent F, Namba K, Lowe J (2012) A bipolar spindle of antiparallel ParM filaments drives bacterial plasmid segregation. Science 338:1334–1337
Ge Y, Hu X, Zhao N, Shi T, Cai Q, Yuan Z (2014a) A new tubRZ operon involved in the maintenance of the Bacillus sphaericus mosquitocidal plasmid pBsph. Microbiology 160:1112–1124
Ge Y, Zhao N, Hu X, Shi T, Cai Q, Yuan Z (2014b) A novel transcriptional activator, tubX, is required for the stability of Bacillus sphaericus mosquitocidal plasmid pBsph. J Bacteriol 196:4304–4314
Hoshino S, Hayashi I (2012) Filament formation of the FtsZ/tubulin-like protein TubZ from the Bacillus cereus pXO1 plasmid. J Biol Chem 287:32103–32112
Kraemer JA, Erb ML, Waddling CA, Montabana EA, Zehr EA, Wang H, Nguyen K, Pham DS, Agard DA, Pogliano J (2012) A phage tubulin assembles dynamic filaments by an atypical mechanism to center viral DNA within the host cell. Cell 149:1488–1499
Larsen RA, Cusumano C, Fujioka A, Lim-Fong G, Patterson P, Pogliano J (2007) Treadmilling of a prokaryotic tubulin-like protein, TubZ, required for plasmid stability in Bacillus thuringiensis. Genes Dev 21:1340–1352
Lowe J, Li H, Downing KH, Nogales E (2001) Refined structure of alpha beta-tubulin at 3.5 A resolution. J Mol Biol 313:1045–1057
Montabana EA, Agard DA (2014) Bacterial tubulin TubZ-Bt transitions between a two-stranded intermediate and a four-stranded filament upon GTP hydrolysis. Proc Natl Acad Sci U S A 111:3407–3412
Ni L, Xu W, Kumaraswami M, Schumacher MA (2010) 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 U S A 107:11763–11768
Okinaka RT, Cloud K, Hampton O, Hoffmaster AR, Hill KK, Keim P, Koehler TM, Lamke G, Kumano S, Mahillon J, Manter D, Martinez Y, Ricke D, Svensson R, Jackson PJ (1999) Sequence and organization of pXO1, the large Bacillus anthracis plasmid harboring the anthrax toxin genes. J Bacteriol 181:6509–6515
Oliva MA, Martin-Galiano AJ, Sakaguchi Y, Andreu JM (2012) Tubulin homolog TubZ in a phage-encoded partition system. Proc Natl Acad Sci U S A 109:7711–7716
Sakaguchi Y, Hayashi T, Kurokawa K, Nakayama K, Oshima K, Fujinaga Y, Ohnishi M, Ohtsubo E, Hattori M, Oguma K (2005) The genome sequence of Clostridium botulinum type C neurotoxin-converting phage and the molecular mechanisms of unstable lysogeny. Proc Natl Acad Sci U S A 102:17472–17477
Srinivasan R, Mishra M, Leong FY, Chiam KH, Balasubramanian M (2011) Bacillus anthracis tubulin-related protein Ba-TubZ assembles force-generating polymers. Cytoskeleton (Hoboken) 68:501–511
Szwedziak P, Wang Q, Bharat TA, Tsim M, Lowe J (2014) Architecture of the ring formed by the tubulin homologue FtsZ in bacterial cell division. Elife 3:e04601
Tan CM, Therien AG, Lu J, Lee SH, Caron A, Gill CJ, Lebeau-Jacob C, Benton-Perdomo L, Monteiro JM, Pereira PM, Elsen NL, Wu J, Deschamps K, Petcu M, Wong S, Daigneault E, Kramer S, Liang L, Maxwell E, Claveau D, Vaillancourt J, Skorey K, Tam J, Wang H, Meredith TC, Sillaots S, Wang-Jarantow L, Ramtohul Y, Langlois E, Landry F, Reid JC, Parthasarathy G, Sharma S, Baryshnikova A, Lumb KJ, Pinho MG, Soisson SM, Roemer T (2012) Restoring methicillin-resistant Staphylococcus aureus susceptibility to beta-lactam antibiotics. Sci Transl Med 4:126ra35
Tang M, Bideshi DK, Park HW, Federici BA (2006) Minireplicon from pBtoxis of Bacillus thuringiensis subsp. israelensis. Appl Environ Microbiol 72:6948–6954
Tang M, Bideshi DK, Park HW, Federici BA (2007) 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
Tinsley E, Khan SA (2006) A novel FtsZ-like protein is involved in replication of the anthrax toxin-encoding pXO1 plasmid in Bacillus anthracis. J Bacteriol 188:2829–2835
Vaughan S, Wickstead B, Gull K, Addinall SG (2004) Molecular evolution of FtsZ protein sequences encoded within the genomes of archaea, bacteria, and eukaryota. J Mol Evol 58:19–29
Zehr EA, Kraemer JA, Erb ML, Coker JK, Montabana EA, Pogliano J, Agard DA (2014) The structure and assembly mechanism of a novel three-stranded tubulin filament that centers phage DNA. Structure 22:539–548
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Fink, G., Aylett, C.H.S. (2017). Tubulin-Like Proteins in Prokaryotic DNA Positioning. In: Löwe, J., Amos, L. (eds) Prokaryotic Cytoskeletons. Subcellular Biochemistry, vol 84. Springer, Cham. https://doi.org/10.1007/978-3-319-53047-5_11
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DOI: https://doi.org/10.1007/978-3-319-53047-5_11
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