Skip to main content

Long Noncontractile Tail Machines of Bacteriophages

  • Chapter
  • First Online:
Viral Molecular Machines

Part of the book series: Advances in Experimental Medicine and Biology ((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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Abuladze NK, Gingery M, Tsai J et al (1994) Tail length determination in bacteriophage T4. Virology 199:301–310

    Article  PubMed  CAS  Google Scholar 

  • Ackermann HW (2007a) 5500 Phages examined in the electron microscope. Arch Virol 152:227–243

    Article  PubMed  CAS  Google Scholar 

  • Ackermann HW (2007b) Bacteriophages: tailed, Encyclopedia of life sciences. Wiley, New York

    Google Scholar 

  • Altschul SF, Koonin EV (1998) Iterated profile searches with PSI-BLAST – a tool for discovery in protein databases. Trends Biochem Sci 23:444–447

    Article  PubMed  CAS  Google Scholar 

  • Ambroggio XI, Rees DC, Deshaies RJ (2004) JAMM: a metalloprotease-like zinc site in the proteasome and signalosome. PLoS Biol 2:E2

    Article  PubMed  Google Scholar 

  • 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 190:4989–4996

    Article  PubMed  CAS  Google Scholar 

  • Bebeacua C, Bron P, Lai L et al (2010) Structure and molecular assignment of lactococcal phage TP901-1 baseplate. J Biol Chem 285:39079–39086

    Article  PubMed  CAS  Google Scholar 

  • 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 476:129–133

    Article  PubMed  CAS  Google Scholar 

  • 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 283:13556–13564

    Article  PubMed  CAS  Google Scholar 

  • 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 98:14819–14824

    Article  PubMed  CAS  Google Scholar 

  • 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 107:14384–14389

    Article  PubMed  CAS  Google Scholar 

  • Casjens S, Hendrix R (1974b) Comments on the arrangement of the morphogenetic genes of bacteriophage lambda. J Mol Biol 90:20–25

    Article  PubMed  CAS  Google Scholar 

  • Casjens SR, Hendrix RW (1974a) Locations and amounts of major structural proteins in bacteriophage lambda. J Mol Biol 88:535–545

    Article  PubMed  CAS  Google Scholar 

  • Christie GE, Temple LM, Bartlett BA et al (2002) Programmed translational frameshift in the bacteriophage P2 FETUD tail gene operon. J Bacteriol 184:6522–6531

    Article  PubMed  CAS  Google Scholar 

  • 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 365:175–186

    Article  PubMed  CAS  Google Scholar 

  • Effantin G, Boulanger P, Neumann E et al (2006) Bacteriophage T5 structure reveals similarities with HK97 and T4 suggesting evolutionary relationships. J Mol Biol 361:993–1002

    Article  PubMed  CAS  Google Scholar 

  • 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 161:1–8

    Article  PubMed  CAS  Google Scholar 

  • Feucht A, Schmid A, Benz R et al (1990) Pore formation associated with the tail-tip protein pb2 of bacteriophage T5. J Biol Chem 265:18561–18567

    PubMed  CAS  Google Scholar 

  • Finn RD, Mistry J, Tate J et al (2010) The Pfam protein families database. Nucleic Acids Res 38:D211–D222

    Article  PubMed  CAS  Google Scholar 

  • 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 188:6101–6114

    Article  PubMed  CAS  Google Scholar 

  • Fraser JS, Maxwell KL, Davidson AR (2007) Immunoglobulin-like domains on bacteriophage: weapons of modest damage? Curr Opin Microbiol 10:382–387

    Article  PubMed  CAS  Google Scholar 

  • Fraser JS, Yu Z, Maxwell KL et al (2006) Ig-like domains on bacteriophages: a tale of promiscuity and deceit. J Mol Biol 359:496–507

    Article  PubMed  CAS  Google Scholar 

  • Grundy FJ, Howe MM (1985) Morphogenetic structures present in lysates of amber mutants of bacteriophage Mu. Virology 143:485–504

    Article  PubMed  CAS  Google Scholar 

  • 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 41:222–227

    PubMed  CAS  Google Scholar 

  • 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 162:621–625

    PubMed  CAS  Google Scholar 

  • Heller KJ (1984) Identification of the phage gene for host receptor specificity by analyzing hybrid phages of T5 and BF23. Virology 139:11–21

    Article  PubMed  CAS  Google Scholar 

  • Hendrix RW, Duda RL (1992) Bacteriophage lambda PaPa: not the mother of all lambda phages. Science 258:1145–1148

    Article  PubMed  CAS  Google Scholar 

  • 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 96:2192–2197

    Article  PubMed  CAS  Google Scholar 

  • Inamdar MM, Gelbart WM, Phillips R (2006) Dynamics of DNA ejection from bacteriophage. Biophys J 91:411–420

    Article  PubMed  CAS  Google Scholar 

  • Jeembaeva M, Castelnovo M, Larsson F et al (2008) Osmotic pressure: resisting or promoting DNA ejection from phage? J Mol Biol 381:310–323

    Article  PubMed  CAS  Google Scholar 

  • 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 299:27–51

    Article  PubMed  CAS  Google Scholar 

  • 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 48:10129–10135

    Article  PubMed  CAS  Google Scholar 

  • Katsura I (1976) Morphogenesis of bacteriophage lambda tail. Polymorphism in the assembly of the major tail protein. J Mol Biol 107:307–326

    Article  PubMed  CAS  Google Scholar 

  • 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 146:493–512

    Article  PubMed  CAS  Google Scholar 

  • Katsura I (1983) Tail assembly and injection. In: Hendrix RW et al (eds) Lambda II. Cold Spring Harbor, New York

    Google Scholar 

  • Katsura I (1987) Determination of bacteriophage lambda tail length by a protein ruler. Nature 327:73–75

    Article  PubMed  CAS  Google Scholar 

  • Katsura I, Kuhl PW (1975) Morphogenesis of the tail of bacteriophage lambda. III. Morphogenetic pathway. J Mol Biol 91:257–273

    Article  PubMed  CAS  Google Scholar 

  • Katsura I, Hendrix RW (1984) Length determination in bacteriophage lambda tails. Cell 39:691–698

    Article  PubMed  CAS  Google Scholar 

  • Katsura I, Tsugita A (1977) Purification and characterization of the major protein and the terminator protein of the bacteriophage lambda tail. Virology 76:129–145

    Article  PubMed  CAS  Google Scholar 

  • Kanamaru S, Ishiwata Y, Suzuki T et al (2005) Control of bacteriophage T4 tail lysozyme activity during the infection process. J Mol Biol 346:1013–1020

    Article  PubMed  CAS  Google Scholar 

  • Kenny JG, McGrath S, Fitzgerald GF et al (2004) Bacteriophage Tuc 2009 encodes a tail-associated cell wall-­degrading activity. J Bacteriol 186:3480–3491

    Article  PubMed  CAS  Google Scholar 

  • 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 352:976–985

    Article  PubMed  CAS  Google Scholar 

  • 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 43:729–733

    Article  PubMed  CAS  Google Scholar 

  • Lang AS, Taylor TA, Beatty JT (2002) Evolutionary implications of phylogenetic analyses of the gene transfer agent (GTA) of Rhodobacter capsulatus. J Mol Evol 55:534–543

    Article  PubMed  CAS  Google Scholar 

  • Lengyel JA, Goldstein RN, Marsh M et al (1974) Structure of the bacteriophage P2 tail. Virology 62:161–174

    Article  PubMed  CAS  Google Scholar 

  • 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 106:4154–4159

    Article  PubMed  CAS  Google Scholar 

  • Leiman PG, Shneider MM, Mesyanzhinov VV et al (2006) Evolution of bacteriophage tails: structure of T4 gene product 10. J Mol Biol 358:912–921

    Article  PubMed  CAS  Google Scholar 

  • 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 234:124–139

    Article  PubMed  CAS  Google Scholar 

  • 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 35:324–340

    Article  PubMed  CAS  Google Scholar 

  • Mc Grath S, Neve H, Seegers JF et al (2006) Anatomy of a lactococcal phage tail. J Bacteriol 188:3972–3982

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Moak M, Molineux IJ (2004) Peptidoglycan hydrolytic activities associated with bacteriophage virions. Mol Microbiol 51:1169–1183

    Article  PubMed  CAS  Google Scholar 

  • 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 169:5884–5886

    PubMed  CAS  Google Scholar 

  • 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 171:4378–4384

    PubMed  CAS  Google Scholar 

  • 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 48:785–823

    Article  PubMed  CAS  Google Scholar 

  • Panja D, Molineux IJ (2010) Dynamics of bacteriophage genome ejection in vitro and in vivo. Phys Biol 7:045006

    Article  PubMed  Google Scholar 

  • Parker ML, Eiserling FA (1983) Bacteriophage SPO1 structure and morphogenesis. I. Tail structure and length regulation. J Virol 46:239–249

    PubMed  CAS  Google Scholar 

  • 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 276:315–328

    Article  PubMed  CAS  Google Scholar 

  • 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 403:468–479

    Article  PubMed  CAS  Google Scholar 

  • 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 106:4160–4165

    Article  PubMed  CAS  Google Scholar 

  • 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 389:938–951

    Article  PubMed  CAS  Google Scholar 

  • 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 318:557–569

    Article  PubMed  CAS  Google Scholar 

  • Plisson C, White HE, Auzat I et al (2007) Structure of bacteriophage SPP1 tail reveals trigger for DNA ejection. EMBO J 26:3720–3728

    Article  PubMed  CAS  Google Scholar 

  • 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 62:1569–1585

    Article  PubMed  CAS  Google Scholar 

  • Roessner CA, Struck DK, Ihler GM (1983) Morphology of complexes formed between bacteriophage lambda and structures containing the lambda receptor. J Bacteriol 153:1528–1534

    PubMed  CAS  Google Scholar 

  • Roessner CA, Ihler GM (1986) Formation of transmembrane channels in liposomes during injection of lambda DNA. J Biol Chem 261:386–390

    PubMed  CAS  Google Scholar 

  • Roessner CA, Ihler GM (1984) Proteinase sensitivity of bacteriophage lambda tail proteins gpJ and pH in complexes with the lambda receptor. J Bacteriol 157:165–170

    PubMed  CAS  Google Scholar 

  • 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 80:9331–9335

    Article  PubMed  CAS  Google Scholar 

  • 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 28:230–234

    Article  PubMed  CAS  Google Scholar 

  • Saigo K (1975) Tail–DNA connection and chromosome structure in bacteriophage T5. Virology 68:154–165

    Article  PubMed  CAS  Google Scholar 

  • 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 153:639–646

    Article  PubMed  CAS  Google Scholar 

  • Sao-Jose C, Baptista C, Santos MA (2004) Bacillus subtilis operon encoding a membrane receptor for bacteriophage SPP1. J Bacteriol 186:8337–8346

    Article  PubMed  CAS  Google Scholar 

  • 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 281:11464–11470

    Article  PubMed  CAS  Google Scholar 

  • Scandella D, Arber W (1974) An Escherichia coli mutant which inhibits the injection of phage lambda DNA. Virology 58:504–513

    Article  PubMed  CAS  Google Scholar 

  • Schwartz M (1975) Reversible interaction between coliphage lambda and its receptor protein. J Mol Biol 99:185–201

    Article  PubMed  CAS  Google Scholar 

  • 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 107:6852–6857

    Article  PubMed  CAS  Google Scholar 

  • 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 69:206–215

    Article  PubMed  CAS  Google Scholar 

  • Shao Y, Wang IN (2008) Bacteriophage adsorption rate and optimal lysis time. Genetics 180:471–482

    Article  PubMed  Google Scholar 

  • 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 191:728–734

    Article  PubMed  CAS  Google Scholar 

  • 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 313:29–32

    Article  PubMed  CAS  Google Scholar 

  • Soding J, Biegert A, Lupas AN (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 33:W244–W248

    Article  PubMed  Google Scholar 

  • 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 281:14256–14262

    Article  PubMed  CAS  Google Scholar 

  • 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 285:41232–41243

    Article  PubMed  CAS  Google Scholar 

  • 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 1804:1738–1742

    PubMed  CAS  Google Scholar 

  • 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 264:954–967

    Article  PubMed  CAS  Google Scholar 

  • Thomas JO (1974) Chemical linkage of the tail to the right-end of bacteriophage lambda DNA. J Mol Biol 87:1–10

    Article  PubMed  CAS  Google Scholar 

  • Thomas JO (1978) Altered arrangement of the DNA in injection-defective lambda bacteriophage. J Mol Biol 123:149–161

    Article  PubMed  CAS  Google Scholar 

  • Tsui LC, Hendrix RW (1983) Proteolytic processing of phage lambda tail protein gpH: timing of the cleavage. Virology 125:257–264

    Article  PubMed  CAS  Google Scholar 

  • 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 314:1137–1146

    Article  PubMed  Google Scholar 

  • 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 285:36666–36673

    Article  PubMed  CAS  Google Scholar 

  • 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 187:4187–4197

    Article  PubMed  CAS  Google Scholar 

  • 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 182:680–688

    Article  PubMed  CAS  Google Scholar 

  • 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 123:253–260

    Article  PubMed  CAS  Google Scholar 

  • 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 188:1419–1436

    Article  PubMed  CAS  Google Scholar 

  • 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 83:8934–8938

    Article  PubMed  CAS  Google Scholar 

  • Xu J (2001) A conserved frameshift strategy in dsDNA long tailed bacteriophages. University of Pittsburgh, Pittsburgh, PA

    Google Scholar 

  • Xu J, Hendrix RW, Duda RL (2004) Conserved translational frameshift in dsDNA bacteriophage tail assembly genes. Mol Cell 16:11–21

    Article  PubMed  CAS  Google Scholar 

  • 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 50:303–317

    Article  PubMed  CAS  Google Scholar 

  • 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 80:505–518

    Article  PubMed  CAS  Google Scholar 

Download references

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).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alan R. Davidson .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Davidson, A.R., Cardarelli, L., Pell, L.G., Radford, D.R., Maxwell, K.L. (2012). Long Noncontractile Tail Machines of Bacteriophages. In: Rossmann, M., Rao, V. (eds) Viral Molecular Machines. Advances in Experimental Medicine and Biology, vol 726. Springer, Boston, MA. https://doi.org/10.1007/978-1-4614-0980-9_6

Download citation

Publish with us

Policies and ethics