Development of giant bacteriophage φKZ is independent of the host transcription apparatus

Journal of Virology

Volumn 88, Issue 18, 2014, Pages 10501-10510

  Ceyssens, Pieter Jan ^a,h   Minakhin, Leonid ^b   van den Bossche, An ^a   Yakunina, Maria ^c   Klimuk, Evgeny ^c,d,e   Blasdel, Bob ^a   de Smet, Jeroen ^a   Noben, Jean Paul ^f   Bläsi, Udo ^g   Severinov, Konstantin ^b,c,d,e   Lavigne, Rob ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b RUTGERS UNIVERSITY   (United States)

^c PETER THE GREAT ST PETERSBURG POLYTECHNIC UNIVERSITY   (Russian Federation)

^d INSTITUTE OF MOLECULAR GENETICS   (Russian Federation)

^e SKOLKOVO INSTITUTE OF SCIENCE AND TECHNOLOGY   (Russian Federation)

^f HASSELT UNIVERSITY   (Belgium)

^g UNIVERSITY OF VIENNA   (Austria)

^h SCIENTIFIC INSTITUTE OF PUBLIC HEALTH   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

RNA POLYMERASE; BACTERIAL PROTEIN; DNA DIRECTED RNA POLYMERASE; VIRUS PROTEIN;

ARTICLE; BACTERIAL GENETICS; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL INFECTION; BACTERIOPHAGE; BACTERIOPHAGE PHI KAPPA ZETA; CONTROLLED STUDY; CYTOLYSIS; ENZYME ACTIVITY; GENE EXPRESSION; GENE MAPPING; GENETIC TRANSCRIPTION; HOST CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROGENY; PROTEIN SYNTHESIS; PSEUDOMONAS AERUGINOSA; RNA SEQUENCE; SEQUENCE ANALYSIS; VIRION; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; METABOLISM; PHYSIOLOGY; PSEUDOMONAS PHAGE; VIROLOGY; VIRUS GENOME; VIRUS REPLICATION;

BACTERIAL PROTEINS; BACTERIOPHAGES; DNA-DIRECTED RNA POLYMERASES; GENE EXPRESSION REGULATION, VIRAL; GENOME, VIRAL; HOST-PATHOGEN INTERACTIONS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS PHAGES; TRANSCRIPTION, GENETIC; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84906350544     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01347-14     Document Type: Article

References (46)

1. Cramer P. 2002. Multisubunit RNA polymerases. Curr. Opin. Struct. Biol. 12:89-97. http://dx.doi.org/10.1016/S0959-440X(02)00294-4.
2. Darst SA. 2001. Bacterial DNA polymerase. Curr. Opin. Struct. Biol. 11:155-162. http://dx.doi.org/10.1016/S0959-440X(00)00185-8.
3. Lane WJ, Darst SA. 2010. Molecular evolution of multisubunit RNA polymerases: structural analysis. J. Mol. Biol. 395:686-704. http://dx.doi .org/10.1016/j.jmb.2009.10.063.
4. Lane WJ, Darst SA. 2010. Molecular evolution of multisubunit RNA polymerases: sequence analysis. J. Mol. Biol. 395:671-685. http://dx.doi .org/10.1016/j.jmb.2009.10.062.
5. Iyer LM, Koonin EV, Aravind L. 2003. Evolutionary connection between the catalytic subunits of DNA-dependent RNA polymerases and eukaryotic RNA-dependentRNApolymerases and the origin ofRNApolymerases.BMC Struct. Biol. 28:1. http://dx.doi.org/10.1186/1472-6807-3-1.
6. Cermakian N, Ikeda TM, Miramontes P, Lang BF, Gray MW, Cedergren R. 1997. On the evolution of the single-subunit RNA polymerases. J. Mol. Evol. 45:671-681. http://dx.doi.org/10.1007/PL00006271.
7. Cheetham GM, Steitz TA. 1999. Structure of a transcribing T7 RNA polymerase initiation complex. Science 286:2305-2309. http://dx.doi.org /10.1126/science.286.5448.2305.
8. Campbell EA, Korzheva N, Mustaev A, Murakami K, Nair S, Goldfarb A, Darst SA. 2001. Structural mechanism for rifampicin inhibition of bacterial RNA polymerase. Cell 104:901-912. http://dx.doi.org/10.1016 /S0092-8674(01)00286-0.
9. Nechaev S, Severinov K. 2003. Bacteriophage-induced modifications of host RNA polymerase. Annu. Rev. Microbiol. 57:301-322. http://dx.doi .org/10.1146/annurev.micro.57.030502.090942.
10. Nechaev S, Severinov K. 2008. The elusive object of desire-interactions of bacteriophages and their hosts. Curr. Opin. Microbiol. 11:186-193. http: //dx.doi.org/10.1016/j.mib.2008.02.009.
11. Steitz TA. 2004. The structural basis of the transition from initiation to elongation phases of transcription, as well as translocation and strand separation, by T7 RNA polymerase. Curr. Opin. Struct. Biol. 14:4-9. http: //dx.doi.org/10.1016/j.sbi.2004.01.006.
12. Kazmierczak KM, Davydova EK, Mustaev AA, Rothman-Denes LB. 2002. The phage N4 virion RNA polymerase catalytic domain is related to single-subunit RNA polymerases. EMBO J. 21:5815-5823. http://dx.doi .org/10.1093/emboj/cdf584.
13. Jamalludeen N, Kropinski AM, Johnson RP, Lingohr E, Harel J, Gyles CL. 2008. Complete genomic sequence of bacteriophage phiEcoM-GJ1, a novel phage that has myovirus morphology and a podovirus-like RNA polymerase. Appl. Environ. Microbiol. 74:516-525. http://dx.doi.org/10 .1128/AEM.00990-07.
14. Semenova E, Djordjevic M, Shraiman B, Severinov K. 2005. The tale of two RNA polymerases: transcription profiling and gene expression strategy of bacteriophage Xp10. Mol. Microbiol. 55:764-777. http://dx.doi.org /10.1111/j.1365-2958.2004.04442.x.
15. Sousa R, Mukherjee S. 2003. T7 RNA polymerase. Prog. Nucleic Acid Res. Mol. Biol. 73:1-41. http://dx.doi.org/10.1016/S0079-6603(03)01001-8.
16. Savalia D, Robins W, Nechaev S, Molineux I, Severinov K. 2010. The role of the T7 Gp2 inhibitor of host RNA polymerase in phage development. J. Mol. Biol. 402:118-126. http://dx.doi.org/10.1016/j.jmb.2010.07 .012.
17. Falco SC, Laan KV, Rothman-Denes LB. 1977. Virion-associated RNA polymerase required for bacteriophage N4 development. Proc. Natl. Acad. Sci. U. S. A. 74:520-523. http://dx.doi.org/10.1073/pnas.74.2.520.
18. Gleghorn ML, Davydova EK, Rothman-Denes LB, Murakami KS. 2008. Structural basis for DNA-hairpin promoter recognition by the bacteriophage N4 virionRNApolymerase. Mol. Cell 32:707-717. http://dx.doi.org /10.1016/j.molcel.2008.11.010.
19. Ceyssens PJ, Brabban A, Rogge L, Lewis MS, Pickard D, Goulding D, Dougan G, Noben JP, Kropinski A, Kutter E, Lavigne R. 2010. Molecular and physiological analysis of three Pseudomonas aeruginosa phages belonging to the "N4-like viruses." Virology 405:26-30. http://dx.doi.org /10.1016/j.virol.2010.06.011.
20. Cho NY, Choi M, Rothman-Denes LB. 1995. The bacteriophage N4-coded single-stranded DNA-binding protein, N4SSB, is the transcriptional activator of Escherichia coli RNA polymerase at N4 late promoters. J. Mol. Biol. 246:461-471. http://dx.doi.org/10.1006/jmbi.1994.0098.
21. Price AR, Frabotta M. 1972. Resistance of bacteriophage PBS2 infection to rifampicin, an inhibitor of Bacillus subtilis RNA synthesis. Biochem. Biophys. Res. Commun. 48:1578-1585. http://dx.doi.org/10.1016/0006 -291X(72)90894-7.
22. Clark S. 1978. Transcriptional specificity of a multisubunitRNApolymerase induced by Bacillus subtilis bacteriophage PBS2. J. Virol. 25:224-237.
23. Clark S, Losick R, Pero J. 1974. New RNA polymerase from Bacillus subtilis infected with phage PBS2. Nature 252:21-24. http://dx.doi.org/10 .1038/252021a0.
24. Hendrix RW. 2009. Jumbo bacteriophages. Curr. Top. Microbiol. Immunol. 328:229-240.
25. Mesyanzhinov VV, Robben J, Grymonprez B, Kostyuchenko VA, Bourkaltseva MV, Sykilinda NN, Krylov VN, Volckaert G. 2002. The genome of bacteriophage φ of Pseudomonas aeruginosa. J. Mol. Biol. 317:1-19. http://dx.doi.org/10.1006/jmbi.2001.5396.
26. Thomas JA, Weintraub ST, Wu W, Winkler DC, Cheng N, Steven AC, Black LW. 2012. Extensive proteolysis of head and inner body proteins by a morphogenetic protease in the giant Pseudomonas aeruginosa phage φ. Mol. Microbiol. 84:324-339. http://dx.doi.org/10.1111/j.1365-2958 .2012.08025.x.
27. Lecoutere E, Ceyssens PJ, Miroshnikov KA, Mesyanzhinov VV, Krylov VN, Noben JP, Robben J, Hertveldt K, Volckaert G, Lavigne R. 2009. Identification and comparative analysis of the structural proteomes of φ and EL, two giant Pseudomonas aeruginosa bacteriophages. Proteomics 9:3215-3219. http://dx.doi.org/10.1002/pmic.200800727.
28. Thomas JA, Rolando MR, Carroll CA, Shen PS, Belnap DM, Weintraub ST, Serwer P, Hardies SC. 2008. Characterization of Pseudomonas chlororaphis myovirus 201varphi2-1 via genomic sequencing, mass spectrometry, and electron microscopy. Virology 376:330-338. http://dx.doi.org /10.1016/j.virol.2008.04.004.
29. Skurnik M, Hyytiäinen HJ, Happonen LJ, Kiljunen S, Datta N, Mattinen L, Williamson K, Kristo P, Szeliga M, Kalin-Mänttäri L, Ahola-Iivarinen E, Kalkkinen N, Butcher SJ. 2012. Characterization of the genome, proteome, and structure of yersiniophage _R1-37. J. Virol. 86: 12625-12642. http://dx.doi.org/10.1128/JVI.01783-12.
30. Ceyssens PJ, Lavigne R, Mattheus W, Chibeu A, Hertveldt K, Mast J, Robben J, Volckaert G. 2006. Genomic analysis of Pseudomonas aeruginosa phages LKD16 and LKA1: establishment of the _KMV subgroup within the T7 supergroup. J. Bacteriol. 188:6924-6931. http://dx.doi.org /10.1128/JB.00831-06.
31. Klimuk E, Akulenko N, Makarova KS, Ceyssens PJ, Volchenkov I, Lavigne R, Severinov K. 2013. Host RNA polymerase inhibitors encoded by_KMV-like phages of Pseudomonas. Virology 436:67-74. http://dx.doi .org/10.1016/j.virol.2012.10.021.
32. Qiu D, Damron FH, Mima T, Schweizer HP, Yu HD. 2008. PBAD-based shuttle vectors for functional analysis of toxic and highly regulated genes in Pseudomonas and Burkholderia spp. and other bacteria. Appl. Environ. Microbiol. 74:7422-7426. http://dx.doi.org/10.1128/AEM.01369-08.
33. Sevostyanova A, Djordjevic M, Kuznedelov K, Naryshkina T, Gelfand MS, Severinov K, Minakhin L. 2007. Temporal regulation of viral transcription during development of Thermus thermophilus bacteriophage phiYS40. J. Mol. Biol. 366:420-435. http://dx.doi.org/10.1016/j.jmb.2006 .11.050.
34. Cenens W, Mebrhatu MT, Makumi A, Ceyssens PJ, Lavigne R, Van Houdt R, Taddei F, Aertsen A. 2013. Expression of a novel P22 ORFan gene reveals the phage carrier state in Salmonella Typhimurium. PLoS Genet. 9:e1003269. http://dx.doi.org/10.1371/journal.pgen.1003269.
35. Monson R, Foulds I, Foweraker J, Welch M, Salmond GP. 2011. The Pseudomonas aeruginosa generalized transducing phage phiPA3 is a new member of the φ-like group of "jumbo" phages, and infects model laboratory strains and clinical isolates from cystic fibrosis patients. Microbiology 157:859-867. http://dx.doi.org/10.1099/mic.0.044701-0.
36. Toledo-Arana A, Dussurget O, Nikitas G, Sesto N, Guet-Revillet H, Balestrino D, Loh E, Gripenland J, Tiensuu T, Vaitkevicius K. 2009. The Listeria transcriptional landscape from saprophytism to virulence. Nature 459:950-956. http://dx.doi.org/10.1038/nature08080.
37. Stazic D, Lindell D, Steglich C. 2011. Antisense RNA protects mRNA from RNase E degradation by RNA-RNA duplex formation during phage infection. Nucleic Acids Res. 39:4890-4899. http://dx.doi.org/10.1093 /nar/gkr037.
38. Kawano M, Aravind L, Storz G. 2007. An antisense RNA controls synthesis of an SOS-induced toxin evolved from an antitoxin. Mol. Microbiol. 64:738-754. http://dx.doi.org/10.1111/j.1365-2958.2007.05688.x.
39. Cornelissen A, Hardies SC, Shaburova OV, Krylov VN, Mattheus W, Kropinski AM, Lavigne R. 2012. Complete genome sequence of the giant virus OBP and comparative genome analysis of the diverse φ-related phages. J. Virol. 86:1844-1852. http://dx.doi.org/10.1128/JVI.06330-11.
40. Hertveldt K, Lavigne R, Pleteneva E, Sernova N, Kurochkina L, Korchevskii R, Robben J, Mesyanzhinov V, Krylov VN, Volckaert G. 2005. Genome comparison of Pseudomonas aeruginosa large phages. J. Mol. Biol. 354:536-545. http://dx.doi.org/10.1016/j.jmb.2005.08.075.
41. Dömötör D, Becságh P, Rákhely G, Schneider G, Kovács T. 2012. Complete genomic sequence of Erwinia amylovora phage phiEaH2. J. Virol. 86:10899. http://dx.doi.org/10.1128/JVI.01870-12.
42. Ceyssens PJ, Glonti T, Kropinski NM, Lavigne R, Chanishvili N, Kulakov L, Lashkhi N, Tediashvili M, Merabishvili M. 2011. Phenotypic and genotypic variations within a single bacteriophage species. Virol. J. 8:134. http://dx.doi.org/10.1186/1743-422X-8-134.
43. Severinov K. 2000. RNA polymerase structure-function: insights into points of transcriptional regulation. Curr. Opin. Microbiol. 3:118-125. http://dx.doi.org/10.1016/S1369-5274(00)00062-X.
44. Xie WQ, Jäger Potts KM. 1989. Cyanobacterial RNA polymerase genes rpoC1 and rpoC2 correspond to rpoC of Escherichia coli. J. Bacteriol. 171:1967-1973.
45. Young BA, Gruber TM, Gross CA. 2004. Minimal machinery of RNA polymerase holoenzyme sufficient for promoter melting. Science 303: 1382-1384. http://dx.doi.org/10.1126/science.1092462.
46. Jatsenko T, Tover A, Tegova R, Kivisaar M. 2010. Molecular characterization of Rifr mutations in Pseudomonas aeruginosa and Pseudomonas putida. Mutat. Res. 683:106-114. http://dx.doi.org/10.1016/j.mrfmmm .2009.10.015.