Function and Horizontal Transfer of the Small Terminase Subunit of the Tailed Bacteriophage Sf6 DNA Packaging Nanomotor

Overview

Journal Virology

Specialty Microbiology

Date 2013 Apr 9

PMID 23562538

Citations 29

Authors

Justin C Leavitt

Eddie B Gilcrease

Kassandra Wilson

Sherwood R Casjens

Affiliations

Soon will be listed here.

Abstract

Bacteriophage Sf6 DNA packaging series initiate at many locations across a 2kbp region. Our in vivo studies show that Sf6 small terminase subunit (TerS) protein recognizes a specific packaging (pac) site near the center of this region, that this site lies within the portion of the Sf6 gene that encodes the DNA-binding domain of TerS protein, that this domain of the TerS protein is responsible for the imprecision in Sf6 packaging initiation, and that the DNA-binding domain of TerS must be covalently attached to the domain that interacts with the rest of the packaging motor. The TerS DNA-binding domain is self-contained in that it apparently does not interact closely with the rest of the motor and it binds to a recognition site that lies within the DNA that encodes the domain. This arrangement has allowed the horizontal exchange of terS genes among phages to be very successful.

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References

Duffy C, Feiss M . The large subunit of bacteriophage lambda's terminase plays a role in DNA translocation and packaging termination. J Mol Biol. 2002; 316(3):547-61. DOI: 10.1006/jmbi.2001.5368. View

Kondabagil K, Zhang Z, Rao V . The DNA translocating ATPase of bacteriophage T4 packaging motor. J Mol Biol. 2006; 363(4):786-99. DOI: 10.1016/j.jmb.2006.08.054. View

Frackman S, Siegele D, Feiss M . A functional domain of bacteriophage lambda terminase for prohead binding. J Mol Biol. 1984; 180(2):283-300. DOI: 10.1016/s0022-2836(84)80005-4. View

Weaver S, Levine M . Replication in situ and DNA encapsulation following induction of an excision-defective lysogen of Salmonella bacteriophage P22. J Mol Biol. 1978; 118(3):389-411. DOI: 10.1016/0022-2836(78)90235-8. View

Groenen M, Van de Putte P . Mapping of a site for packaging of bacteriophage Mu DNA. Virology. 1985; 144(2):520-2. DOI: 10.1016/0042-6822(85)90292-2. View

Lebedev A, Krause M, Isidro A, Vagin A, Orlova E, Turner J . Structural framework for DNA translocation via the viral portal protein. EMBO J. 2007; 26(7):1984-94. PMC: 1847669. DOI: 10.1038/sj.emboj.7601643. View

Lee Y, Park J, Chang H . Genomic sequence analysis of virulent Cronobacter sakazakii bacteriophage ES2. Arch Virol. 2011; 156(11):2105-8. DOI: 10.1007/s00705-011-1096-7. View

Yeo A, Feiss M . Specific interaction of terminase, the DNA packaging enzyme of bacteriophage lambda, with the portal protein of the prohead. J Mol Biol. 1995; 245(2):141-50. DOI: 10.1006/jmbi.1994.0013. View

Liebeschuetz J, Ritchie D . Phage T1-mediated transduction of a plasmid containing the T1 pac site. J Mol Biol. 1986; 192(4):681-92. DOI: 10.1016/0022-2836(86)90021-5. View

10.

Youderian P, Sugiono P, Brewer K, Higgins N, Elliott T . Packaging specific segments of the Salmonella chromosome with locked-in Mud-P22 prophages. Genetics. 1988; 118(4):581-92. PMC: 1203313. DOI: 10.1093/genetics/118.4.581. View

11.

LARKIN M, Blackshields G, Brown N, Chenna R, McGettigan P, McWilliam H . Clustal W and Clustal X version 2.0. Bioinformatics. 2007; 23(21):2947-8. DOI: 10.1093/bioinformatics/btm404. View

12.

Deichelbohrer I, Messer W, Trautner T . Genome of Bacillus subtilis Bacteriophage SPP1: Structure and Nucleotide Sequence of pac, the Origin of DNA Packaging. J Virol. 1982; 42(1):83-90. PMC: 256047. DOI: 10.1128/JVI.42.1.83-90.1982. View

13.

Oliveira L, Henriques A, Tavares P . Modulation of the viral ATPase activity by the portal protein correlates with DNA packaging efficiency. J Biol Chem. 2006; 281(31):21914-21923. DOI: 10.1074/jbc.M603314200. View

14.

Parent K, Khayat R, Tu L, Suhanovsky M, Cortines J, Teschke C . P22 coat protein structures reveal a novel mechanism for capsid maturation: stability without auxiliary proteins or chemical crosslinks. Structure. 2010; 18(3):390-401. PMC: 2951021. DOI: 10.1016/j.str.2009.12.014. View

15.

Casjens S, Huang W . Linear chromosomal physical and genetic map of Borrelia burgdorferi, the Lyme disease agent. Mol Microbiol. 1993; 8(5):967-80. DOI: 10.1111/j.1365-2958.1993.tb01641.x. View

16.

Wu C, BLACK L . Mutational analysis of the sequence-specific recombination box for amplification of gene 17 of bacteriophage T4. J Mol Biol. 1995; 247(4):604-17. View

17.

Casjens S, Winn-Stapley D, Gilcrease E, Morona R, Kuhlewein C, Chua J . The chromosome of Shigella flexneri bacteriophage Sf6: complete nucleotide sequence, genetic mosaicism, and DNA packaging. J Mol Biol. 2004; 339(2):379-94. DOI: 10.1016/j.jmb.2004.03.068. View

18.

SCHMIEGER H . pac sites are indispensable for in vivo packaging of DNA by phage P22. Mol Gen Genet. 1984; 195(1-2):252-5. DOI: 10.1007/BF00332755. View

19.

Cortines J, Weigele P, Gilcrease E, Casjens S, Teschke C . Decoding bacteriophage P22 assembly: identification of two charged residues in scaffolding protein responsible for coat protein interaction. Virology. 2011; 421(1):1-11. PMC: 3208733. DOI: 10.1016/j.virol.2011.09.005. View

20.

Linderoth N, Ziermann R, Haggard-Ljungquist E, Christie G, Calendar R . Nucleotide sequence of the DNA packaging and capsid synthesis genes of bacteriophage P2. Nucleic Acids Res. 1991; 19(25):7207-14. PMC: 332578. DOI: 10.1093/nar/19.25.7207. View