Long Noncontractile Tail Machines of Bacteriophages

  • Alan R. Davidson
  • Lia Cardarelli
  • Lisa G. Pell
  • Devon R. Radford
  • Karen L. Maxwell
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 726)

Abstract

In this chapter, we describe the structure, assembly, function, and evolution of the long, noncontractile tail of the siphophages, which comprise ∼60% of the phages on earth. We place ­particular emphasis on features that are conserved among all siphophages, and trace evolutionary connections between these phages and myophages, which possess long contractile tails. The large number of high-resolution structures of tail proteins solved recently coupled to studies of tail-related complexes by electron microscopy have provided many new insights in this area. In addition, the availability of thousands of phage and prophage genome sequences has allowed the delineation of several large families of tail proteins that were previously unrecognized. We also summarize current knowledge pertaining to the mechanisms by which siphophage tails recognize the bacterial cell surface and mediate DNA injection through the cell envelope. We show that phages infecting Gram-positive and Gram-negative bacteria possess distinct families of proteins at their tail tips that are involved in this process. Finally, we speculate on the evolutionary advantages provided by long phage tails.

Keywords

Hydrolysis Sucrose Carbohydrate Recombination Bacillus 

Notes

Acknowledgments

The authors thank Christian Cambillau for supplying the image used in Fig. 6.7. We also thank Petr Leiman for his encouragement during the writing of this chapter and for reading the final version. Work in our labs is supported by operating grants from the Canadian Institutes of Health Research to A.R.D. (Fund No. MOP-77680) and to K.L.M. (Fund No. MOP-6279).

References

  1. Abuladze NK, Gingery M, Tsai J et al (1994) Tail length determination in bacteriophage T4. Virology 199:301–310PubMedCrossRefGoogle Scholar
  2. Ackermann HW (2007a) 5500 Phages examined in the electron microscope. Arch Virol 152:227–243PubMedCrossRefGoogle Scholar
  3. Ackermann HW (2007b) Bacteriophages: tailed, Encyclopedia of life sciences. Wiley, New YorkGoogle Scholar
  4. Altschul SF, Koonin EV (1998) Iterated profile searches with PSI-BLAST – a tool for discovery in protein databases. Trends Biochem Sci 23:444–447PubMedCrossRefGoogle Scholar
  5. Ambroggio XI, Rees DC, Deshaies RJ (2004) JAMM: a metalloprotease-like zinc site in the proteasome and signalosome. PLoS Biol 2:E2PubMedCrossRefGoogle Scholar
  6. Baptista C, Santos MA, Sao-Jose C (2008) Phage SPP1 reversible adsorption to Bacillus subtilis cell wall teichoic acids accelerates virus recognition of membrane receptor YueB. J Bacteriol 190:4989–4996PubMedCrossRefGoogle Scholar
  7. Bebeacua C, Bron P, Lai L et al (2010) Structure and molecular assignment of lactococcal phage TP901-1 baseplate. J Biol Chem 285:39079–39086PubMedCrossRefGoogle Scholar
  8. Berrier C, Bonhivers M, Letellier L et al (2000) High-conductance channel induced by the interaction of phage lambda with its receptor maltoporin. FEBS Lett 476:129–133PubMedCrossRefGoogle Scholar
  9. Boulanger P, Jacquot P, Plancon L et al (2008) Phage T5 straight tail fiber is a multifunctional protein acting as a tape measure and carrying fusogenic and muralytic activities. J Biol Chem 283:13556–13564PubMedCrossRefGoogle Scholar
  10. Bradley P, Cowen L, Menke M et al (2001) BETAWRAP: successful prediction of parallel beta-helices from primary sequence reveals an association with many microbial pathogens. Proc Natl Acad Sci USA 98:14819–14824PubMedCrossRefGoogle Scholar
  11. Cardarelli L, Pell LG, Neudecker P et al (2010) Phages have adapted the same protein fold to fulfill multiple functions in virion assembly. Proc Natl Acad Sci USA 107:14384–14389PubMedCrossRefGoogle Scholar
  12. Casjens S, Hendrix R (1974b) Comments on the arrangement of the morphogenetic genes of bacteriophage lambda. J Mol Biol 90:20–25PubMedCrossRefGoogle Scholar
  13. Casjens SR, Hendrix RW (1974a) Locations and amounts of major structural proteins in bacteriophage lambda. J Mol Biol 88:535–545PubMedCrossRefGoogle Scholar
  14. Christie GE, Temple LM, Bartlett BA et al (2002) Programmed translational frameshift in the bacteriophage P2 FETUD tail gene operon. J Bacteriol 184:6522–6531PubMedCrossRefGoogle Scholar
  15. Edmonds L, Liu A, Kwan JJ et al (2007) The NMR structure of the gpU tail-terminator protein from bacteriophage lambda: identification of sites contributing to Mg(II)-mediated oligomerization and biological function. J Mol Biol 365:175–186PubMedCrossRefGoogle Scholar
  16. Effantin G, Boulanger P, Neumann E et al (2006) Bacteriophage T5 structure reveals similarities with HK97 and T4 suggesting evolutionary relationships. J Mol Biol 361:993–1002PubMedCrossRefGoogle Scholar
  17. Elliott J, Arber W (1978) E. coli K-12 pel mutants, which block phage lambda DNA injection, coincide with ptsM, which determines a component of a sugar transport system. Mol Gen Genet 161:1–8PubMedCrossRefGoogle Scholar
  18. Feucht A, Schmid A, Benz R et al (1990) Pore formation associated with the tail-tip protein pb2 of bacteriophage T5. J Biol Chem 265:18561–18567PubMedGoogle Scholar
  19. Finn RD, Mistry J, Tate J et al (2010) The Pfam protein families database. Nucleic Acids Res 38:D211–D222PubMedCrossRefGoogle Scholar
  20. Fortier LC, Bransi A, Moineau S (2006) Genome sequence and global gene expression of Q54, a new phage species linking the 936 and c2 phage species of Lactococcus lactis. J Bacteriol 188:6101–6114PubMedCrossRefGoogle Scholar
  21. Fraser JS, Maxwell KL, Davidson AR (2007) Immunoglobulin-like domains on bacteriophage: weapons of modest damage? Curr Opin Microbiol 10:382–387PubMedCrossRefGoogle Scholar
  22. Fraser JS, Yu Z, Maxwell KL et al (2006) Ig-like domains on bacteriophages: a tale of promiscuity and deceit. J Mol Biol 359:496–507PubMedCrossRefGoogle Scholar
  23. Grundy FJ, Howe MM (1985) Morphogenetic structures present in lysates of amber mutants of bacteriophage Mu. Virology 143:485–504PubMedCrossRefGoogle Scholar
  24. Heller K, Braun V (1982) Polymannose O-antigens of Escherichia coli, the binding sites for the reversible adsorption of bacteriophage T5+ via the L-shaped tail fibers. J Virol 41:222–227PubMedGoogle Scholar
  25. Heller KJ, Schwarz H (1985) Irreversible binding to the receptor of bacteriophages T5 and BF23 does not occur with the tip of the tail. J Bacteriol 162:621–625PubMedGoogle Scholar
  26. Heller KJ (1984) Identification of the phage gene for host receptor specificity by analyzing hybrid phages of T5 and BF23. Virology 139:11–21PubMedCrossRefGoogle Scholar
  27. Hendrix RW, Duda RL (1992) Bacteriophage lambda PaPa: not the mother of all lambda phages. Science 258:1145–1148PubMedCrossRefGoogle Scholar
  28. Hendrix RW, Smith MC, Burns RN et al (1999) Evolutionary relationships among diverse bacteriophages and prophages: all the world’s a phage. Proc Natl Acad Sci USA 96:2192–2197PubMedCrossRefGoogle Scholar
  29. Inamdar MM, Gelbart WM, Phillips R (2006) Dynamics of DNA ejection from bacteriophage. Biophys J 91:411–420PubMedCrossRefGoogle Scholar
  30. Jeembaeva M, Castelnovo M, Larsson F et al (2008) Osmotic pressure: resisting or promoting DNA ejection from phage? J Mol Biol 381:310–323PubMedCrossRefGoogle Scholar
  31. Juhala RJ, Ford ME, Duda RL et al (2000) Genomic sequences of bacteriophages HK97 and HK022: pervasive genetic mosaicism in the lambdoid bacteriophages. J Mol Biol 299:27–51PubMedCrossRefGoogle Scholar
  32. Kageyama Y, Murayama M, Onodera T et al (2009) Observation of the membrane binding activity and domain structure of gpV, which comprises the tail spike of bacteriophage P2. Biochemistry 48:10129–10135PubMedCrossRefGoogle Scholar
  33. Katsura I (1976) Morphogenesis of bacteriophage lambda tail. Polymorphism in the assembly of the major tail protein. J Mol Biol 107:307–326PubMedCrossRefGoogle Scholar
  34. Katsura I (1981) Structure and function of the major tail protein of bacteriophage lambda. Mutants having small major tail protein molecules in their virion. J Mol Biol 146:493–512PubMedCrossRefGoogle Scholar
  35. Katsura I (1983) Tail assembly and injection. In: Hendrix RW et al (eds) Lambda II. Cold Spring Harbor, New YorkGoogle Scholar
  36. Katsura I (1987) Determination of bacteriophage lambda tail length by a protein ruler. Nature 327:73–75PubMedCrossRefGoogle Scholar
  37. Katsura I, Kuhl PW (1975) Morphogenesis of the tail of bacteriophage lambda. III. Morphogenetic pathway. J Mol Biol 91:257–273PubMedCrossRefGoogle Scholar
  38. Katsura I, Hendrix RW (1984) Length determination in bacteriophage lambda tails. Cell 39:691–698PubMedCrossRefGoogle Scholar
  39. Katsura I, Tsugita A (1977) Purification and characterization of the major protein and the terminator protein of the bacteriophage lambda tail. Virology 76:129–145PubMedCrossRefGoogle Scholar
  40. Kanamaru S, Ishiwata Y, Suzuki T et al (2005) Control of bacteriophage T4 tail lysozyme activity during the infection process. J Mol Biol 346:1013–1020PubMedCrossRefGoogle Scholar
  41. Kenny JG, McGrath S, Fitzgerald GF et al (2004) Bacteriophage Tuc 2009 encodes a tail-associated cell wall-­degrading activity. J Bacteriol 186:3480–3491PubMedCrossRefGoogle Scholar
  42. Kondou Y, Kitazawa D, Takeda S et al (2005) Structure of the central hub of bacteriophage Mu baseplate determined by X-ray crystallography of gp44. J Mol Biol 352:976–985PubMedCrossRefGoogle Scholar
  43. Konopa G, Taylor K (1979) Coliphage lambda ghosts obtained by osmotic shock or LiCl treatment are devoid of J- and H-gene products. J Gen Virol 43:729–733PubMedCrossRefGoogle Scholar
  44. Lang AS, Taylor TA, Beatty JT (2002) Evolutionary implications of phylogenetic analyses of the gene transfer agent (GTA) of Rhodobacter capsulatus. J Mol Evol 55:534–543PubMedCrossRefGoogle Scholar
  45. Lengyel JA, Goldstein RN, Marsh M et al (1974) Structure of the bacteriophage P2 tail. Virology 62:161–174PubMedCrossRefGoogle Scholar
  46. Leiman PG, Basler M, Ramagopal UA et al (2009) Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin. Proc Natl Acad Sci USA 106:4154–4159PubMedCrossRefGoogle Scholar
  47. Leiman PG, Shneider MM, Mesyanzhinov VV et al (2006) Evolution of bacteriophage tails: structure of T4 gene product 10. J Mol Biol 358:912–921PubMedCrossRefGoogle Scholar
  48. Levin ME, Hendrix RW, Casjens SR (1993) A programmed translational frameshift is required for the synthesis of a bacteriophage lambda tail assembly protein. J Mol Biol 234:124–139PubMedCrossRefGoogle Scholar
  49. Loessner MJ, Inman RB, Lauer P et al (2000) Complete nucleotide sequence, molecular analysis and genome structure of bacteriophage A118 of Listeria monocytogenes: implications for phage evolution. Mol Microbiol 35:324–340PubMedCrossRefGoogle Scholar
  50. Mc Grath S, Neve H, Seegers JF et al (2006) Anatomy of a lactococcal phage tail. J Bacteriol 188:3972–3982PubMedCrossRefGoogle Scholar
  51. Moak M, Molineux IJ (2000) Role of the Gp16 lytic transglycosylase motif in bacteriophage T7 virions at the initiation of infection. Mol Microbiol 37:345–355PubMedCrossRefGoogle Scholar
  52. Moak M, Molineux IJ (2004) Peptidoglycan hydrolytic activities associated with bacteriophage virions. Mol Microbiol 51:1169–1183PubMedCrossRefGoogle Scholar
  53. Montag D, Henning U (1987) An open reading frame in the Escherichia coli bacteriophage lambda genome encodes a protein that functions in assembly of the long tail fibers of bacteriophage T4. J Bacteriol 169:5884–5886PubMedGoogle Scholar
  54. Montag D, Schwarz H, Henning U (1989) A component of the side tail fiber of Escherichia coli bacteriophage lambda can functionally replace the receptor-recognizing part of a long tail fiber protein of the unrelated bacteriophage T4. J Bacteriol 171:4378–4384PubMedGoogle Scholar
  55. Murialdo H, Siminovitch L (1972) The morphogenesis of bacteriophage lambda. IV. Identification of gene products and control of the expression of the morphogenetic information. Virology 48:785–823PubMedCrossRefGoogle Scholar
  56. Panja D, Molineux IJ (2010) Dynamics of bacteriophage genome ejection in vitro and in vivo. Phys Biol 7:045006PubMedCrossRefGoogle Scholar
  57. Parker ML, Eiserling FA (1983) Bacteriophage SPO1 structure and morphogenesis. I. Tail structure and length regulation. J Virol 46:239–249PubMedGoogle Scholar
  58. Pedersen M, Ostergaard S, Bresciani J et al (2000) Mutational analysis of two structural genes of the temperate lactococcal bacteriophage TP901-1 involved in tail length determination and baseplate assembly. Virology 276:315–328PubMedCrossRefGoogle Scholar
  59. Pell LG, Gasmi-Seabrook GM, Morais M et al (2010) The solution structure of the C-terminal Ig-like domain of the bacteriophage λ tail tube protein. J Mol Biol 403:468–479PubMedCrossRefGoogle Scholar
  60. Pell LG, Kanelis V, Donaldson LW et al (2009b) The phage lambda major tail protein structure reveals a common evolution for long-tailed phages and the type VI bacterial secretion system. Proc Natl Acad Sci USA 106:4160–4165PubMedCrossRefGoogle Scholar
  61. Pell LG, Liu A, Edmonds L et al (2009a) The X-ray crystal structure of the phage lambda tail terminator protein reveals the biologically relevant hexameric ring structure and demonstrates a conserved mechanism of tail termination among diverse long-tailed phages. J Mol Biol 389:938–951PubMedCrossRefGoogle Scholar
  62. Plancon L, Janmot C, le Maire M et al (2002) Characterization of a high-affinity complex between the bacterial outer membrane protein FhuA and the phage T5 protein pb5. J Mol Biol 318:557–569PubMedCrossRefGoogle Scholar
  63. Plisson C, White HE, Auzat I et al (2007) Structure of bacteriophage SPP1 tail reveals trigger for DNA ejection. EMBO J 26:3720–3728PubMedCrossRefGoogle Scholar
  64. Piuri M, Hatfull GF (2006) A peptidoglycan hydrolase motif within the mycobacteriophage TM4 tape measure protein promotes efficient infection of stationary phase cells. Mol Microbiol 62:1569–1585PubMedCrossRefGoogle Scholar
  65. Roessner CA, Struck DK, Ihler GM (1983) Morphology of complexes formed between bacteriophage lambda and structures containing the lambda receptor. J Bacteriol 153:1528–1534PubMedGoogle Scholar
  66. Roessner CA, Ihler GM (1986) Formation of transmembrane channels in liposomes during injection of lambda DNA. J Biol Chem 261:386–390PubMedGoogle Scholar
  67. Roessner CA, Ihler GM (1984) Proteinase sensitivity of bacteriophage lambda tail proteins gpJ and pH in complexes with the lambda receptor. J Bacteriol 157:165–170PubMedGoogle Scholar
  68. Ricagno S, Campanacci V, Blangy S et al (2006) Crystal structure of the receptor-binding protein head domain from Lactococcus lactis phage bIL170. J Virol 80:9331–9335PubMedCrossRefGoogle Scholar
  69. Rigden DJ, Jedrzejas MJ, Galperin MY (2003) Amidase domains from bacterial and phage autolysins define a family of gamma-D, L-glutamate-specific amidohydrolases. Trends Biochem Sci 28:230–234PubMedCrossRefGoogle Scholar
  70. Saigo K (1975) Tail–DNA connection and chromosome structure in bacteriophage T5. Virology 68:154–165PubMedCrossRefGoogle Scholar
  71. Samsonov VV, Sineoky SP (2002) DcrA and dcrB Escherichia coli genes can control DNA injection by phages specific for BtuB and FhuA receptors. Res Microbiol 153:639–646PubMedCrossRefGoogle Scholar
  72. Sao-Jose C, Baptista C, Santos MA (2004) Bacillus subtilis operon encoding a membrane receptor for bacteriophage SPP1. J Bacteriol 186:8337–8346PubMedCrossRefGoogle Scholar
  73. Sao-Jose C, Lhuillier S, Lurz R et al (2006) The ectodomain of the viral receptor YueB forms a fiber that triggers ejection of bacteriophage SPP1 DNA. J Biol Chem 281:11464–11470PubMedCrossRefGoogle Scholar
  74. Scandella D, Arber W (1974) An Escherichia coli mutant which inhibits the injection of phage lambda DNA. Virology 58:504–513PubMedCrossRefGoogle Scholar
  75. Schwartz M (1975) Reversible interaction between coliphage lambda and its receptor protein. J Mol Biol 99:185–201PubMedCrossRefGoogle Scholar
  76. Sciara G, Bebeacua C, Bron P et al (2010) Structure of lactococcal phage p2 baseplate and its mechanism of activation. Proc Natl Acad Sci USA 107:6852–6857PubMedCrossRefGoogle Scholar
  77. Scandella D, Arber W (1976) Phage lambda DNA injection into Escherichia coli pel-mutants is restored by mutations in phage genes V or H. Virology 69:206–215PubMedCrossRefGoogle Scholar
  78. Shao Y, Wang IN (2008) Bacteriophage adsorption rate and optimal lysis time. Genetics 180:471–482PubMedCrossRefGoogle Scholar
  79. Siponen M, Sciara G, Villion M et al (2009) Crystal structure of ORF12 from Lactococcus lactis phage p2 identifies a tape measure protein chaperone. J Bacteriol 191:728–734PubMedCrossRefGoogle Scholar
  80. Smith ML, Avanigadda LN, Liddell PW et al (2010) Identification of the J and K genes in the bacteriophage Mu genome sequence. FEMS Microbiol Lett 313:29–32PubMedCrossRefGoogle Scholar
  81. Soding J, Biegert A, Lupas AN (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 33:W244–W248PubMedCrossRefGoogle Scholar
  82. Spinelli S, Campanacci V, Blangy S et al (2006) Modular structure of the receptor binding proteins of Lactococcus lactis phages. The RBP structure of the temperate phage TP901-1. J Biol Chem 281:14256–14262PubMedCrossRefGoogle Scholar
  83. Sudiarta IP, Fukushima T, Sekiguchi J (2010) Bacillus subtilis CwlP of the SP-{beta} prophage has two novel peptidoglycan hydrolase domains, muramidase and cross-linkage digesting DD-endopeptidase. J Biol Chem 285:41232–41243PubMedCrossRefGoogle Scholar
  84. Suzuki H, Yamada S, Toyama Y et al (2010) The C-terminal domain is sufficient for host-binding activity of the Mu phage tail-spike protein. Biochim Biophys Acta 1804:1738–1742PubMedGoogle Scholar
  85. Tavares P, Lurz R, Stiege A et al (1996) Sequential headful packaging and fate of the cleaved DNA ends in bacteriophage SPP1. J Mol Biol 264:954–967PubMedCrossRefGoogle Scholar
  86. Thomas JO (1974) Chemical linkage of the tail to the right-end of bacteriophage lambda DNA. J Mol Biol 87:1–10PubMedCrossRefGoogle Scholar
  87. Thomas JO (1978) Altered arrangement of the DNA in injection-defective lambda bacteriophage. J Mol Biol 123:149–161PubMedCrossRefGoogle Scholar
  88. Tsui LC, Hendrix RW (1983) Proteolytic processing of phage lambda tail protein gpH: timing of the cleavage. Virology 125:257–264PubMedCrossRefGoogle Scholar
  89. van Raaij MJ, Schoehn G, Burda MR et al (2001) Crystal structure of a heat and protease-stable part of the bacteriophage T4 short tail fibre. J Mol Biol 314:1137–1146PubMedCrossRefGoogle Scholar
  90. Veesler D, Robin G, Lichiere J et al (2010) Crystal structure of bacteriophage SPP1 distal tail protein (gp19.1): a baseplate hub paradigm in gram-positive infecting phages. J Biol Chem 285:36666–36673PubMedCrossRefGoogle Scholar
  91. Vegge CS, Brondsted L, Neve H et al (2005) Structural characterization and assembly of the distal tail structure of the temperate lactococcal bacteriophage TP901-1. J Bacteriol 187:4187–4197PubMedCrossRefGoogle Scholar
  92. Vianelli A, Wang GR, Gingery M et al (2000) Bacteriophage T4 self-assembly: localization of gp3 and its role in determining tail length. J Bacteriol 182:680–688PubMedCrossRefGoogle Scholar
  93. Walker JE, Auffret AD, Carne A et al (1982) Solid-phase sequence analysis of polypeptides eluted from polyacrylamide gels. An aid to interpretation of DNA sequences exemplified by the Escherichia coli unc operon and bacteriophage lambda. Eur J Biochem 123:253–260PubMedCrossRefGoogle Scholar
  94. Wietzorrek A, Schwarz H, Herrmann C et al (2006) The genome of the novel phage Rtp, with a rosette-like tail tip, is homologous to the genome of phage T1. J Bacteriol 188:1419–1436PubMedCrossRefGoogle Scholar
  95. Williams N, Fox DK, Shea C et al (1986) Pel, the protein that permits lambda DNA penetration of Escherichia coli, is encoded by a gene in ptsM and is required for mannose utilization by the phosphotransferase system. Proc Natl Acad Sci USA 83:8934–8938PubMedCrossRefGoogle Scholar
  96. Xu J (2001) A conserved frameshift strategy in dsDNA long tailed bacteriophages. University of Pittsburgh, Pittsburgh, PAGoogle Scholar
  97. Xu J, Hendrix RW, Duda RL (2004) Conserved translational frameshift in dsDNA bacteriophage tail assembly genes. Mol Cell 16:11–21PubMedCrossRefGoogle Scholar
  98. Zimmer M, Sattelberger E, Inman RB et al (2003) Genome and proteome of Listeria monocytogenes phage PSA: an unusual case for programmed + 1 translational frameshifting in structural protein synthesis. Mol Microbiol 50:303–317PubMedCrossRefGoogle Scholar
  99. Zweig M, Cummings DJ (1973) Cleavage of head and tail proteins during bacteriophage T5 assembly: selective host involvement in the cleavage of a tail protein. J Mol Biol 80:505–518PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Alan R. Davidson
    • 1
    • 2
  • Lia Cardarelli
    • 2
  • Lisa G. Pell
    • 1
    • 2
  • Devon R. Radford
    • 1
  • Karen L. Maxwell
    • 3
  1. 1.Department of Molecular GeneticsUniversity of TorontoTorontoCanada
  2. 2.Department of BiochemistryUniversity of TorontoTorontoCanada
  3. 3.The Donnelly Centre for Cellular and Biomolecular Research, Department of Molecular GeneticsUniversity of TorontoTorontoCanada

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