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A peptidoglycan hydrolase motif within the mycobacteriophage TM4 tape measure protein promotes efficient infection of stationary phase cells

Mariana Piuri, Graham F. Hatfull

Molecular Microbiology · 2006

doi:10.1111/j.1365-2958.2006.05473.x

Abstract

Summary The predominant morphotype of mycobacteriophage virions has a DNA‐containing capsid attached to a long flexible non‐contractile tail, features characteristic of the Siphoviridae. Within these phage genomes the tape measure protein ( tmp ) gene can be readily identified due to the well‐established relationship between the length of the gene and the length of the phage tail – because these phages typically have long tails, the tmp gene is usually the largest gene in the genome. Many of these mycobacteriophage Tmp's contain small motifs with sequence similarity to host proteins. One of these motifs (motif 1) corresponds to the Rpf proteins that have lysozyme activity and function to stimulate growth of dormant bacteria, while the others (motifs 2 and 3) are related to proteins of unknown function, although some of the related proteins of the host are predicted to be involved in cell wall catabolism. We show here that motif 3‐containing proteins have peptidoglycan‐hydrolysing activity and that while this activity is not required for phage viability, it facilitates efficient infection and DNA injection into stationary phase cells. Tmp's of mycobacteriophages may thus have acquired these motifs in order to avoid a selective disadvantage that results from changes in peptidoglycan in non‐growing cells.

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References 59

  1. 1.

    Atrih A, Foster SJ. The role of peptidoglycan structure and structural dynamics during endospore dormancy and germination. Antonie Van Leeuwenhoek. 1999;75:299-307.

    Not in our library10.1023/a:1001800507443

  2. 2.

    Atrih A, Bacher G, Allmaier G, Williamson MP, Foster SJ. Analysis of peptidoglycan structure from vegetative cells of Bacillus subtilis 168 and role of PBP 5 in peptidoglycan maturation. J Bacteriol. 1999;181:3956-3966.

    Not in our library10.1128/jb.181.13.3956-3966.1999

  3. 3.

    Bardarov S, Kriakov J, Carriere C, Yu S, Vaamonde C, McAdam RA, et al. Conditionally replicating mycobacteriophages: a system for transposon delivery to Mycobacterium tuberculosis. Proc Natl Acad Sci USA. 1997;94:10961-10966.

    Not in our library10.1073/pnas.94.20.10961

  4. 4.

    Bardarov S, Bardarov S, Pavelka MS, Sambandamurthy V, Larsen M, Tufariello J, et al. Specialized transduction: an efficient method for generating marked and unmarked targeted gene disruptions in Mycobacterium tuberculosis, M. bovis BCG and M. smegmatis. Microbiology. 2002;148:3007-3017.

    Not in our library10.1099/00221287-148-10-3007

  5. 5.

    Barsom EK, Hatfull GF. Characterization of Mycobacterium smegmatis gene that confers resistance to phages L5 and D29 when overexpressed. Mol Microbiol. 1996;21:159-170.

    Not in our library10.1046/j.1365-2958.1996.6291342.x

  6. 6.

    Bendtsen JD, Nielsen H, von Heijne G, Brunak S. Improved prediction of signal peptides: SignalP 3.0. J Mol Biol. 2004;340:783-795.

    Not in our library10.1016/j.jmb.2004.05.028

  7. 7.

    Blokpoel MC, Smeulders MJ, Hubbard JA, Keer J, Williams HD. Global analysis of proteins synthesized by Mycobacterium smegmatis provides direct evidence for physiological heterogeneity in stationary-phase cultures. J Bacteriol. 2005;187:6691-6700.

    Not in our library10.1128/jb.187.19.6691-6700.2005

  8. 8.

    Brennan PJ. Structure, function, and biogenesis of the cell wall of Mycobacterium tuberculosis. Tuberculosis (Edinb). 2003;83:91-97.

    Not in our library10.1016/s1472-9792(02)00089-6

  9. 9.

    Bru C, Courcelle E, Carrere S, Beausse Y, Dalmar S, Kahn D. The ProDom database of protein domain families: more emphasis on 3D. Nucleic Acids Res. 2005;33:D212-D215.

    Not in our library10.1093/nar/gki034

  10. 10.

    Caldentey J, Bamford DH. The lytic enzyme of the Pseudomonas phage phi 6. Purification and biochemical characterization. Biochim Biophys Acta. 1992;1159:44-50.

    Not in our library10.1016/0167-4838(92)90073-m

  11. 11.

    Carriere C, Riska PF, Zimhony O, Kriakov J, Bardarov S, Burns J, et al. Conditionally replicating luciferase reporter phages: improved sensitivity for rapid detection and assessment of drug susceptibility of Mycobacterium tuberculosis. J Clin Microbiol. 1997;35:3232-3239.

    Not in our library10.1128/jcm.35.12.3232-3239.1997

  12. 12.

    Cha RS, Zarbl H, Keohavong P, Thilly WG. Mismatch amplification mutation assay (MAMA): application to the c-H-ras gene. PCR Methods Appl. 1992;2:14-20.

    Not in our library10.1101/gr.2.1.14

  13. 13.

    Cohen-Gonsaud M, Barthe P, Bagneris C, Henderson B, Ward J, Roumestand C, Keep NH. The structure of a resuscitation-promoting factor domain from Mycobacterium tuberculosis shows homology to lysozymes. Nat Struct Mol Biol. 2005;12:270-273.

    Not in our library10.1038/nsmb905

  14. 14.

    Court DL, Sawitzke JA, Thomason LC. Genetic engineering using homologous recombination. Annu Rev Genet. 2002;36:361-388.

    Not in our library10.1146/annurev.genet.36.061102.093104

  15. 15.

    Ford ME, Stenstrom C, Hendrix RW, Hatfull GF. Mycobacteriophage TM4: genome structure and gene expression. Tuber Lung Dis. 1998;79:63-73.

    Not in our library10.1054/tuld.1998.0007

  16. 16.

    Fordham WD, Gilvarg C. Kinetics of cross-linking of peptidoglycan in Bacillus megaterium. J Biol Chem. 1974;249:2478-2482.

    Not in our library

  17. 17.
  18. 18.

    Jacobs WR, Barletta RG, Udani R, Chan J, Kalkut G, Sosne G, et al. Rapid assessment of drug susceptibilities of Mycobacterium tuberculosis by means of luciferase reporter phages. Science. 1993;260:819-822.

    Not in our library10.1126/science.8484123

  19. 19.

    Kanamaru S, Leiman PG, Kostyuchenko VA, Chipman PR, Mesyanzhinov VV, Arisaka F, Rossmann MG. Structure of the cell-puncturing device of bacteriophage T4. Nature. 2002;415:553-557.

    Not in our library10.1038/415553a

  20. 20.

    Kanamaru S, Ishiwata Y, Suzuki T, Rossmann MG, Arisaka F. Control of bacteriophage T4 tail lysozyme activity during the infection process. J Mol Biol. 2005;346:1013-1020.

    Not in our library10.1016/j.jmb.2004.12.042

  21. 21.

    Katsura I. Determination of bacteriophage lambda tail length by a protein ruler. Nature. 1987;327:73-75.

    Not in our library10.1038/327073a0

  22. 22.

    Katsura I, Hendrix RW. Length determination in bacteriophage lambda tails. Cell. 1984;39:691-698.

    Not in our library10.1016/0092-8674(84)90476-8

  23. 23.

    Keep NH, Ward JM, Cohen-Gonsaud M, Henderson B. Wake up! Peptidoglycan lysis and bacterial non-growth states. Trends Microbiol. 2006;14:271-276.

    Not in our library10.1016/j.tim.2006.04.003

  24. 24.

    Kenny JG, McGrath S, Fitzgerald GF, van Sinderen D. Bacteriophage Tuc2009 encodes a tail-associated cell wall-degrading activity. J Bacteriol. 2004;186:3480-3491.

    Not in our library10.1128/jb.186.11.3480-3491.2004

  25. 25.

    Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680-685.

    Not in our library10.1038/227680a0

  26. 26.

    Lee MH, Pascopella L, Jacobs WR, Hatfull GF. Site-specific integration of mycobacteriophage L5: integration-proficient vectors for Mycobacterium smegmatis, Mycobacterium tuberculosis, and bacille Calmette–Guerin. Proc Natl Acad Sci USA. 1991;15:3111-3115.

    Not in our library10.1073/pnas.88.8.3111

  27. 27.

    Lewis JA, Hatfull GF. Identification and characterization of mycobacteriophage L5 excisionase. Mol Microbiol. 2000;35:350-360.

    Not in our library10.1046/j.1365-2958.2000.01695.x

  28. 28.

    Li S, Norioka S, Sakiyama F. Bacteriolytic activity and specificity of Achromobacter beta-lytic protease. J Biochem (Tokyo). 1998;124:332-339.

    Not in our library10.1093/oxfordjournals.jbchem.a022116

  29. 29.

    Moak M, Molineux IJ. Role of the Gp16 lytic transglycosylase motif in bacteriophage T7 virions at the initiation of infection. Mol Microbiol. 2000;37:345-355.

    Not in our library10.1046/j.1365-2958.2000.01995.x

  30. 30.

    Moak M, Molineux IJ. Peptidoglycan hydrolytic activities associated with bacteriophage virions. Mol Microbiol. 2004;51:1169-1183.

    Not in our library10.1046/j.1365-2958.2003.03894.x

  31. 31.

    Molineux IJ. No syringes please, ejection of phage T7 DNA from the virion is enzyme driven. Mol Microbiol. 2001;40:1-8.

    Not in our library10.1046/j.1365-2958.2001.02357.x

  32. 32.

    Molineux IJ. Fifty-three years since Hershey and Chase; much ado about pressure but which pressure is it? Virology. 2006;344:221-229.

    Not in our library10.1016/j.virol.2005.09.014

  33. 33.

    Mosig G, Lin GW, Franklin J, Fan WH. Functional relationships and structural determinants of two bacteriophage T4 lysozymes: a soluble (gene e) and a baseplate-associated (gene 5) protein. New Biol. 1989;1:171-179.

    Not in our library

  34. 34.

    Mukamolova GV, Kaprelyants AS, Young DI, Young M, Kell DB. A bacterial cytokine. Proc Natl Acad Sci USA. 1998;95:8916-8921.

    Not in our library10.1073/pnas.95.15.8916

  35. 35.

    Mukamolova GV, Turapov OA, Young DI, Kaprelyants AS, Kell DB, Young M. A family of autocrine growth factors in Mycobacterium tuberculosis. Mol Microbiol. 2002;46:623-635.

    Not in our library10.1046/j.1365-2958.2002.03184.x

  36. 36.

    Mukamolova GV, Murzin AG, Salina EG, Demina GR, Kell DB, Kaprelyants AS, Young M. Muralytic activity of Micrococcus luteus Rpf and its relationship to physiological activity in promoting bacterial growth and resuscitation. Mol Microbiol. 2006;59:84-98.

    Not in our library10.1111/j.1365-2958.2005.04930.x

  37. 37.

    Nakagawa H, Arisaka F, Ishii S. Isolation and characterization of the bacteriophage T4 tail-associated lysozyme. J Virol. 1985;54:460-466.

    Not in our library10.1128/jvi.54.2.460-466.1985

  38. 38.

    Nielsen H, Krogh A. Prediction of signal peptides and signal anchors by a hidden Markov model. Proc Int Conf Intell Syst Mol Biol. 1998;6:122-130.

    Not in our library

  39. 39.

    Nilsen T, Nes IF, Holo H. Enterolysin A, a cell wall-degrading bacteriocin from Enterococcus faecalis LMG 2333. Appl Environ Microbiol. 2003;69:2975-2984.

    Not in our library10.1128/aem.69.5.2975-2984.2003

  40. 40.

    Parish T, Mahenthiralingam E, Draper P, Davis EO, Colston MJ. Regulation of the inducible acetamidase gene of Mycobacterium smegmatis. Microbiology. 1997;143:2267-2276.

    Not in our library10.1099/00221287-143-7-2267

All 59 references

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