The Phage Nucleus and Tubulin Spindle Are Conserved among Large Pseudomonas Phages

Cell Reports

Volumn 20, Issue 7, 2017, Pages 1563-1571

  Chaikeeratisak, Vorrapon ^a   Nguyen, Katrina ^a   Egan, MacKennon E ^a   Erb, Marcella L ^a   Vavilina, Anastasia ^a   Pogliano, Joe ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

compartmentalization; nucleus; nucleus origin; nucleus positioning; phage; PhuZ; spindle; tubulin; viral eukaryogenesis

Indexed keywords

PROTEIN PHUZ; TUBULIN; UNCLASSIFIED DRUG; VIRAL PROTEIN; VIRUS DNA;

ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; EUKARYOTIC CELL; IN VIVO STUDY; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PSEUDOMONAS PHAGE; VIRUS INFECTION; VIRUS MORPHOLOGY; CLASSIFICATION; CONSERVED SEQUENCE; FLUORESCENCE MICROSCOPY; GENETICS; METABOLISM; PSEUDOMONAS AERUGINOSA; RIBOSOME; ULTRASTRUCTURE; VIROLOGY; VIRUS REPLICATION;

CONSERVED SEQUENCE; DNA, VIRAL; MICROSCOPY, FLUORESCENCE; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS PHAGES; RIBOSOMES; TUBULIN; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 85027877354     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2017.07.064     Document Type: Article

References (22)

1. Aylett, C.H., Wang, Q., Michie, K.A., Amos, L.A., Löwe, J., Filament structure of bacterial tubulin homologue TubZ. Proc. Natl. Acad. Sci. USA 107 (2010), 19766–19771.
2. Aylett, C.H., Izoré, T., Amos, L.A., Löwe, J., Structure of the tubulin/FtsZ-like protein TubZ from Pseudomonas bacteriophage ΦKZ. J. Mol. Biol. 425 (2013), 2164–2173.
3. Bell, P.J., Viral eukaryogenesis: was the ancestor of the nucleus a complex DNA virus?. J. Mol. Evol. 53 (2001), 251–256.
4. Bell, P.J., The viral eukaryogenesis hypothesis: a key role for viruses in the emergence of eukaryotes from a prokaryotic world environment. Ann. N Y Acad. Sci. 1178 (2009), 91–105.
5. Boedeker, C., Schüler, M., Reintjes, G., Jeske, O., van Teeseling, M.C., Jogler, M., Rast, P., Borchert, D., Devos, D.P., Kucklick, M., et al. Determining the bacterial cell biology of Planctomycetes. Nat. Commun., 8, 2017, 14853.
6. Chaikeeratisak, V., Nguyen, K., Khanna, K., Brilot, A.F., Erb, M.L., Coker, J.K., Vavilina, A., Newton, G.L., Buschauer, R., Pogliano, K., et al. Assembly of a nucleus-like structure during viral replication in bacteria. Science 355 (2017), 194–197.
7. Chen, Y., Erickson, H.P., In vitro assembly studies of FtsZ/tubulin-like proteins (TubZ) from Bacillus plasmids: evidence for a capping mechanism. J. Biol. Chem. 283 (2008), 8102–8109.
8. Erb, M.L., Kraemer, J.A., Coker, J.K., Chaikeeratisak, V., Nonejuie, P., Agard, D.A., Pogliano, J., A bacteriophage tubulin harnesses dynamic instability to center DNA in infected cells. eLife, 3, 2014, 3.
9. Forterre, P., The origin of viruses and their possible roles in major evolutionary transitions. Virus Res. 117 (2006), 5–16.
10. Fuerst, J.A., Sagulenko, E., Beyond the bacterium: planctomycetes challenge our concepts of microbial structure and function. Nat. Rev. Microbiol. 9 (2011), 403–413.
11. Koonin, E.V., Viruses and mobile elements as drivers of evolutionary transitions. Philos. Trans. R. Soc. Lond. B Biol. Sci., 371, 2016, 371.
12. Kraemer, J.A., Erb, M.L., Waddling, C.A., Montabana, E.A., Zehr, E.A., Wang, H., Nguyen, K., Pham, D.S., Agard, D.A., Pogliano, J., A phage tubulin assembles dynamic filaments by an atypical mechanism to center viral DNA within the host cell. Cell 149 (2012), 1488–1499.
13. Larsen, R.A., Cusumano, C., Fujioka, A., Lim-Fong, G., Patterson, P., Pogliano, J., Treadmilling of a prokaryotic tubulin-like protein, TubZ, required for plasmid stability in Bacillus thuringiensis. Genes Dev. 21 (2007), 1340–1352.
14. Mesyanzhinov, V.V., Robben, J., Grymonprez, B., Kostyuchenko, V.A., Bourkaltseva, M.V., Sykilinda, N.N., Krylov, V.N., Volckaert, G., The genome of bacteriophage phiKZ of Pseudomonas aeruginosa. J. Mol. Biol. 317 (2002), 1–19.
15. Monson, R., Foulds, I., Foweraker, J., Welch, M., Salmond, G.P., The Pseudomonas aeruginosa generalized transducing phage phiPA3 is a new member of the phiKZ-like group of ‘jumbo' phages, and infects model laboratory strains and clinical isolates from cystic fibrosis patients. Microbiology 157 (2011), 859–867.
16. Montabana, E.A., Agard, D.A., Bacterial tubulin TubZ-Bt transitions between a two-stranded intermediate and a four-stranded filament upon GTP hydrolysis. Proc. Natl. Acad. Sci. USA 111 (2014), 3407–3412.
17. Pogliano, J., Osborne, N., Sharp, M.D., Abanes-De Mello, A., Perez, A., Sun, Y.L., Pogliano, K., A vital stain for studying membrane dynamics in bacteria: a novel mechanism controlling septation during Bacillus subtilis sporulation. Mol. Microbiol. 31 (1999), 1149–1159.
18. Sagulenko, E., Nouwens, A., Webb, R.I., Green, K., Yee, B., Morgan, G., Leis, A., Lee, K.C., Butler, M.K., Chia, N., et al. Nuclear pore-like structures in a compartmentalized bacterium. PLoS ONE, 12, 2017, e0169432.
19. Serwer, P., Hayes, S.J., Zaman, S., Lieman, K., Rolando, M., Hardies, S.C., Improved isolation of undersampled bacteriophages: finding of distant terminase genes. Virology 329 (2004), 412–424.
20. Takemura, M., Poxviruses and the origin of the eukaryotic nucleus. J. Mol. Evol. 52 (2001), 419–425.
21. Villarreal, L.P., DeFilippis, V.R., A hypothesis for DNA viruses as the origin of eukaryotic replication proteins. J. Virol. 74 (2000), 7079–7084.
22. Zehr, E.A., Kraemer, J.A., Erb, M.L., Coker, J.K., Montabana, E.A., Pogliano, J., Agard, D.A., The structure and assembly mechanism of a novel three-stranded tubulin filament that centers phage DNA. Structure 22 (2014), 539–548.