Adsorption of bacteriophages on bacterial cells

Biochemistry (Moscow)

Volumn 82, Issue 13, 2017, Pages 1632-1658

  Letarov, A V ^a,b   Kulikov, E E ^a,c  

^a Federal Research Centre Fundamentals of Biotechnology   (Russian Federation)

^b MOSCOW STATE UNIVERSITY   (Russian Federation)

^c MOSCOW INSTITUTE OF PHYSICS AND TECHNOLOGY   (Russian Federation)

Author keywords

bacteriophage adsorption; bacteriophage adsorption kinetics; bacteriophage receptors; bacteriophages; modulation of bacteriophage adsorption; receptor binding proteins

Indexed keywords

ADSORPTION; BACTERIOPHAGE; BACTERIUM; CYTOLOGY; PHYSIOLOGY; VIRION; VIROLOGY; VIRUS ENTRY;

ADSORPTION; BACTERIA; BACTERIOPHAGES; VIRION; VIRUS INTERNALIZATION;

EID: 85039996016     PISSN: 00062979     EISSN: 16083040     Source Type: Journal    
DOI: 10.1134/s0006297917130053     Document Type: Review

References (193)

1. Knoll, A. H. (2015) Paleobiological perspectives on early microbial evolution, Cold Spring Harb. Perspect. Biol., 7, a018093.
2. Postler, T. S., and Ghosh, S. (2017) Understanding the holobiont: how microbial metabolites affect human health and shape the immune system, Cell Metab., 26, 110–130.
3. Putnam, H. M., Barott, K. L., Ainsworth, T. D., and Gates, R. D. (2017) The vulnerability and resilience of reef-building corals, Curr. Biol., 27, R528–R540.
4. Martin, F. M., Uroz, S., and Barker, D. G. (2017) Ancestral alliances: plant mutualistic symbioses with fungi and bacteria, Science, 356.
5. Takeshita, K., and Kikuchi, Y. (2017) Riptortus pedestris and Burkholderia symbiont: an ideal model system for insect-microbe symbiotic associations, Res. Microbiol., 168, 175–187.
6. Clokie, M. R., Millard, A. D., Letarov, A. V., and Heaphy, S. (2011) Phages in nature, Bacteriophage, 1, 31–45.
7. Sime-Ngando, T. (2014) Environmental bacteriophages: viruses of microbes in aquatic ecosystems, Front. Microbiol., 5, 355.
8. Weinbauer, M. G. (2004) Ecology of prokaryotic viruses, FEMS Microbiol. Rev., 28, 127–181.
9. Weinbauer, M. G., and Rassoulzadegan, F. (2004) Are viruses driving microbial diversification and diversity? Environ. Microbiol., 6, 1–11.
10. Weinbauer, M. G., Bettarel, Y., Cattaneo, R., Luef, B., Maier, C., Motegi, C., Peduzzi, P., and Mari, X. (2009) Viral ecology of organic and inorganic particles in aquatic systems: avenues for further research, Aquat. Microb. Ecol., 57, 321–341.
11. Shabbir, M. A., Hao, H., Shabbir, M. Z., Wu, Q., Sattar, A., and Yuan, Z. (2016) Bacteria vs. bacteriophages: parallel evolution of immune arsenals, Front. Microbiol., 7, 1292.
12. Dy, R. L., Richter, C., Salmond, G. P., and Fineran, P. C. (2014) Remarkable mechanisms in microbes to resist phage infections, Annu. Rev. Virol., 1, 307–331.
13. Samson, J. E., Magadan, A. H., Sabri, M., and Moineau, S. (2013) Revenge of the phages: defeating bacterial defences, Nat. Rev. Microbiol., 11, 675–687.
14. Touchon, M., Moura de Sousa, J. A., and Rocha, E. P. (2017) Embracing the enemy: the diversification of microbial gene repertoires by phage-mediated horizontal gene transfer, Curr. Opin. Microbiol., 38, 66–73.
15. King, A. M. Q., Adams, M. J., Carstens, E. B., and Lefkowitz, E. J. (2012) Virus Taxonomy: Classification and Nomenclature of Viruses. Ninth Report of the International Committee on Taxonomy of Viruses, Academic Press, London-Waltham-San Diego.
16. Bertozzi Silva, J., Storms, Z., and Sauvageau, D. (2016) Host receptors for bacteriophage adsorption, FEMS Microbiol. Lett., 363, fnw002.
17. Storms, Z. J., and Sauvageau, D. (2015) Modeling tailed bacteriophage adsorption: insight into mechanisms, Virology, 485, 355–362.
18. Casjens, S. R., and Molineux, I. J. (2012) Short noncontractile tail machines: adsorption and DNA delivery by podoviruses, Adv. Exp. Med. Biol., 726, 143–179.
19. Davidson, A. R., Cardarelli, L., Pell, L. G., Radford, D. R., and Maxwell, K. L. (2012) Long noncontractile tail machines of bacteriophages, Adv. Exp. Med. Biol., 726, 115–142.
20. Leiman, P. G., and Shneider, M. M. (2012) Contractile tail machines of bacteriophages, Adv. Exp. Med. Biol., 726, 93–114.
21. Mahony, J., and Van Sinderen, D. (2015) Novel strategies to prevent or exploit phages in fermentations, insights from phage–host interactions, Curr. Opin. Biotechnol., 32, 8–13.
22. Letarov, A. V., Golomidova, A. K., and Tarasyan, K. K. (2010) Ecological basis for rational phage therapy, Acta Naturae, 2, 60–72.
23. Auer, G. K., and Weibel, D. B. (2017) Bacterial cell mechanics, Biochemistry, 56, 3710–3724.
24. Jankute, M., Cox, J. A., Harrison, J., and Besra, G. S. (2015) Assembly of the mycobacterial cell wall, Annu. Rev. Microbiol., 69, 405–423.
25. Knirel, Y. A., and Valvano, M. A. (2011) Bacterial Lipopolysaccharides: Structure, Chemical Synthesis, Biogenesis, and Interaction with Host Cells, Springer, Wien.
26. Steimle, A., Autenrieth, I. B., and Frick, J. S. (2016) Structure and function: lipid A modifications in commensals and pathogens, Int. J. Med. Microbiol., 306, 290–301.
27. Amor, K., Heinrichs, D. E., Frirdich, E., Ziebell, K., Johnson, R. P., and Whitfield, C. (2000) Distribution of core oligosaccharide types in lipopolysaccharides from Escherichia coli, Infect. Immun., 68, 1116–1124.
28. Nikaido, H., and Vaara, M. (1985) Molecular basis of bacterial outer membrane permeability, Microbiol. Rev., 49, 1–32.
29. Andres, D., Baxa, U., Hanke, C., Seckler, R., and Barbirz, S. (2010) Carbohydrate binding of Salmonella phage P22 tailspike protein and its role during host cell infection, Biochem. Soc. Trans., 38, 1386–1389.
30. Andres, D., Hanke, C., Baxa, U., Seul, A., Barbirz, S., and Seckler, R. (2010) Tailspike interactions with lipopolysac-charide effect DNA ejection from phage P22 particles in vitro, J. Biol. Chem., 285, 36768–36775.
31. Ranjit, D. K., and Young, K. D. (2016) Colanic acid intermediates prevent de novo shape recovery of Escherichia coli spheroplasts, calling into question biological roles previously attributed to colanic acid, J. Bacteriol., 198, 1230–1240.
32. Ren, G., Wang, Z., Li, Y., Hu, X., and Wang, X. (2016) Effects of lipopolysaccharide core sugar deficiency on colanic acid biosynthesis in Escherichia coli, J. Bacteriol., 198, 1576–1584.
33. Porter, N. T., and Martens, E. C. (2017) The critical roles of polysaccharides in gut microbial ecology and physiology, Annu. Rev. Microbiol., doi: 10.1146/annurev-micro-102215-095316.
34. Kuhn, H. M., Meier-Dieter, U., and Mayer, H. (1988) ECA, the enterobacterial common antigen, FEMS Microbiol. Rev., 4, 195–222.
35. Gozdziewicz, T. K., Lugowski, C., and Lukasiewicz, J. (2014) First evidence for a covalent linkage between enter-obacterial common antigen and lipopolysaccharide in Shigella sonnei phase II ECALPS, J. Biol. Chem., 289, 2745–2754.
36. Slusky, J. S. (2016) Outer membrane protein design, Curr. Opin. Struct. Biol., 45, 45–52.
37. Power, M. L., Ferrari, B. C., Littlefield-Wyer, J., Gordon, D. M., Slade, M. B., and Veal, D. A. (2006) A naturally occurring novel allele of Escherichia coli outer membrane protein A reduces sensitivity to bacteriophage, Appl. Environ. Microbiol., 72, 7930–7932.
38. Smith, S. G., Mahon, V., Lambert, M. A., and Fagan, R. P. (2007) A molecular Swiss army knife: OmpA structure, function and expression, FEMS Microbiol. Lett., 273, 1–11.
39. Choi, K. H., McPartland, J., Kaganman, I., Bowman, V. D., Rothman-Denes, L. B., and Rossmann, M. G. (2008) Insight into DNA and protein transport in double-stranded DNA viruses: the structure of bacteriophage N4, J. Mol. Biol., 378, 726–736.
40. Szewczyk, J., and Collet, J. F. (2016) The journey of lipoproteins through the cell: one birthplace, multiple destinations, Adv. Microb. Physiol., 69, 1–50.
41. Hooda, Y., Lai, C. C. L., and Moraes, T. F. (2017) Identification of a large family of slam-dependent surface lipoproteins in gram-negative bacteria, Front. Cell Infect. Microbiol., 7, 207.
42. Wegrzyn, G., and Thomas, M. S. (2002) Modulation of the susceptibility of intestinal bacteria to bacteriophages in response to Ag43 phase variation–a hypothesis, Med. Sci. Monit., 8, HY15–18.
43. Baldvinsson, S. B., Sorensen, M. C., Vegge, C. S., Clokie, M. R., and Brondsted, L. (2014) Campylobacter jejuni motility is required for infection of the flagellotropic bacteriophage F341, Appl. Environ. Microbiol., 80, 7096–7106.
44. Sorensen, M. C., Gencay, Y. E., Birk, T., Baldvinsson, S. B., Jackel, C., Hammerl, J. A., Vegge, C. S., Neve, H., and Brondsted, L. (2015) Primary isolation strain determines both phage type and receptors recognised by Campylobacter jejuni bacteriophages, PLoS One, 10, e0116287.
45. Choi, Y., Shin, H., Lee, J. H., and Ryu, S. (2013) Identification and characterization of a novel flagellum-dependent Salmonella-infecting bacteriophage, iEPS5, Appl. Environ. Microbiol., 79, 4829–4837.
46. Lee, T. J., Schwartz, C., and Guo, P. (2009) Construction of bacteriophage phi29 DNA packaging motor and its applications in nanotechnology and therapy, Ann. Biomed. Eng., 37, 2064–2081.
47. Shin, H., Lee, J. H., Kim, H., Choi, Y., Heu, S., and Ryu, S. (2012) Receptor diversity and host interaction of bacte-riophages infecting Salmonella enterica serovar typhimurium, PLoS One, 7, e43392.
48. Yen, J. Y., Broadway, K. M., and Scharf, B. E. (2012) Minimum requirements of flagellation and motility for infection of Agrobacterium sp. strain H13-3 by flagellotropic bacteriophage 7-7-1, Appl. Environ. Microbiol., 78, 7216–7222.
49. Siegel, S. D., Liu, J., and Ton-That, H. (2016) Biogenesis of the Gram-positive bacterial cell envelope, Curr. Opin. Microbiol., 34, 31–37.
50. Van der Es, D., Hogendorf, W. F., Overkleeft, H. S., Van der Marel, G. A., and Codee, J. D. (2017) Teichoic acids: synthesis and applications, Chem. Soc. Rev., 46, 1464–1482.
51. Bielmann, R., Habann, M., Eugster, M. R., Lurz, R., Calendar, R., Klumpp, J., and Loessner, M. J. (2015) Receptor binding proteins of Listeria monocytogenes bacte-riophages A118 and P35 recognize serovar-specific teichoic acids, Virology, 477, 110–118.
52. Chang, Y., Shin, H., Lee, J. H., Park, C. J., Paik, S. Y., and Ryu, S. (2015) Isolation and genome characterization of the virulent Staphylococcus aureus bacteriophage SA97, Viruses, 7, 5225–5242.
53. Uchiyama, J., Takemura-Uchiyama, I., Kato, S., Sato, M., Ujihara, T., Matsui, H., Hanaki, H., Daibata, M., and Matsuzaki, S. (2014) In silico analysis of AHJD-like viruses, Staphylococcus aureus phages S24-1 and S13′, and study of phage S24-1 adsorption, Microbiology Open, 3, 257–270.
54. Xia, G., Corrigan, R. M., Winstel, V., Goerke, C., Grundling, A., and Peschel, A. (2011) Wall teichoic acid-dependent adsorption of staphylococcal siphovirus and myovirus, J. Bacteriol., 193, 4006–4009.
55. Baptista, C., Santos, M. A., and 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.
56. Ainsworth, S., Sadovskaya, I., Vinogradov, E., Courtin, P., Guerardel, Y., Mahony, J., Grard, T., Cambillau, C., Chapot-Chartier, M. P., and Van Sinderen, D. (2014) Differences in lactococcal cell wall polysaccharide structure are major determining factors in bacteriophage sensitivity, MBio, 5, e00880–00814.
57. Plaut, R. D., Beaber, J. W., Zemansky, J., Kaur, A. P., George, M., Biswas, B., Henry, M., Bishop-Lilly, K. A., Mokashi, V., Hannah, R. M., Pope, R. K., Read, T. D., Stibitz, S., Calendar, R., and Sozhamannan, S. (2014) Genetic evidence for the involvement of the S-layer protein gene sap and the sporulation genes spo0A, spo0B, and spo0F in phage AP50c infection of Bacillus anthracis, J. Bacteriol., 196, 1143–1154.
58. Edwards, P., and Smit, J. (1991) A transducing bacteriophage for Caulobacter crescentus uses the paracrystalline surface layer protein as a receptor, J. Bacteriol., 173, 5568–5572.
59. Callegari, M. L., Riboli, B., Sanders, J. W., Cocconcelli, P. S., Kok, J., Venema, G., and Morelli, L. (1998) The S-layer gene of Lactobacillus helveticus CNRZ 892: cloning, sequence and heterologous expression, Microbiology, 144, 719–726.
60. Abrahams, K. A., and Besra, G. S. (2016) Mycobacterial cell wall biosynthesis: a multifaceted antibiotic target, Parasitology, doi: 10.1017/S0031182016002377.1-18.
61. Chen, J., Kriakov, J., Singh, A., Jacobs, W. R., Jr., Besra, G. S., and Bhatt, A. (2009) Defects in glycopeptidolipid biosynthesis confer phage I3 resistance in Mycobacterium smegmatis, Microbiology, 155, 4050–4057.
62. Garcia-Doval, C., Caston, J. R., Luque, D., Granell, M., Otero, J. M., Llamas-Saiz, A. L., Renouard, M., Boulanger, P., and Van Raaij, M. J. (2015) Structure of the receptor-binding carboxy-terminal domain of the bacterio-phage T5 L-shaped tail fibre with and without its intramolecular chaperone, Viruses, 7, 6424–6440.
63. Granell, M., Namura, M., Alvira, S., Kanamaru, S., and Van Raaij, M. J. (2017) Crystal structure of the carboxy-terminal region of the bacteriophage T4 proximal long tail fiber protein Gp34, Viruses, 9, 168.
64. Taylor, N. M., Prokhorov, N. S., Guerrero-Ferreira, R. C., Shneider, M. M., Browning, C., Goldie, K. N., Stahlberg, H., and Leiman, P. G. (2016) Structure of the T4 baseplate and its function in triggering sheath contraction, Nature, 533, 346–352.
65. Koc, C., Xia, G., Kuhner, P., Spinelli, S., Roussel, A., Cambillau, C., and Stehle, T. (2016) Structure of the host-recognition device of Staphylococcus aureus phage varphi11, Sci. Rep., 6, 27581.
66. Sciara, G., Bebeacua, C., Bron, P., Tremblay, D., Ortiz-Lombardia, M., Lichiere, J., Van Heel, M., Campanacci, V., Moineau, S., and Cambillau, C. (2010) Structure of lactococcal phage p2 baseplate and its mechanism of activation, Proc. Natl. Acad. Sci. USA, 107, 6852–6857.
67. Garcia-Doval, C., and Van Raaij, M. J. (2012) Structure of the receptor-binding carboxy-terminal domain of bacteriophage T7 tail fibers, Proc. Natl. Acad. Sci. USA, 109, 9390–9395.
68. Chatterjee, S., and Rothenberg, E. (2012) Interaction of bacteriophage l with its E. coli receptor, LamB, Viruses, 4, 3162–3178.
69. Zivanovic, Y., Confalonieri, F., Ponchon, L., Lurz, R., Chami, M., Flayhan, A., Renouard, M., Huet, A., Decottignies, P., Davidson, A. R., Breyton, C., and Boulanger, P. (2014) Insights into bacteriophage T5 structure from analysis of its morphogenesis genes and protein components, J. Virol., 88, 1162–1174.
70. Gallet, R., Shao, Y., and Wang, I. N. (2009) High adsorption rate is detrimental to bacteriophage fitness in a biofilm-like environment, BMC Evol. Biol., 9, 241.
71. Heller, K., and Braun, V. (1979) Accelerated adsorption of bacteriophage T5 to Escherichia coli F, resulting from reversible tail fiber-lipopolysaccharide binding, J. Bacteriol., 139, 32–38.
72. Golomidova, A. K., Kulikov, E. E., Prokhorov, N. S., Guerrero-Ferreira, R., Knirel, Y. A., Kostryukova, E. S., Tarasyan, K. K., and Letarov, A. V. (2016) Branched lateral tail fiber organization in T5-like bacteriophages DT57C and DT571/2 is revealed by genetic and functional analysis, Viruses, 8, 26.
73. Leiman, P. G., Battisti, A. J., Bowman, V. D., Stummeyer, K., Muhlenhoff, M., Gerardy-Schahn, R., Scholl, D., and Molineux, I. J. (2007) The structures of bacteriophages K1E and K1-5 explain processive degradation of polysaccharide capsules and evolution of new host specificities, J. Mol. Biol., 371, 836–849.
74. Prokhorov, N. S., Riccio, C., Zdorovenko, E. L., Shneider, M. M., Browning, C., Knirel, Y. A., Leiman, P. G., and Letarov, A. V. (2017) Function of bacteriophage G7C esterase tailspike in host cell adsorption, Mol. Microbiol., doi: 10.1111/mmi.13710.
75. Dai, W., Hodes, A., Hui, W. H., Gingery, M., Miller, J. F., and Zhou, Z. H. (2010) Three-dimensional structure of tropism-switching Bordetella bacteriophage, Proc. Natl. Acad. Sci. USA, 107, 4347–4352.
76. Veesler, D., Spinelli, S., Mahony, J., Lichiere, J., Blangy, S., Bricogne, G., Legrand, P., Ortiz-Lombardia, M., Campanacci, V., Van Sinderen, D., and Cambillau, C. (2012) Structure of the phage TP901-1 1.8 MDa baseplate suggests an alternative host adhesion mechanism, Proc. Natl. Acad. Sci. USA, 109, 8954–8958.
77. Bebeacua, C., Tremblay, D., Farenc, C., Chapot-Chartier, M. P., Sadovskaya, I., Van Heel, M., Veesler, D., Moineau, S., and Cambillau, C. (2013) Structure, adsorption to host, and infection mechanism of virulent lactococcal phage p2, J. Virol., 87, 12302–12312.
78. Dieterle, M. E., Spinelli, S., Sadovskaya, I., Piuri, M., and Cambillau, C. (2017) Evolved distal tail carbohydrate binding modules of Lactobacillus phage J-1: a novel type of antireceptor widespread among lactic acid bacteria phages, Mol. Microbiol., 104, 608–620.
79. Steinbacher, S., Baxa, U., Miller, S., Weintraub, A., Seckler, R., and Huber, R. (1996) Crystal structure of phage P22 tailspike protein complexed with Salmonella sp. Oantigen receptors, Proc. Natl. Acad. Sci. USA, 93, 10584–10588.
80. Lubkowski, J., Hennecke, F., Pluckthun, A., and Wlodawer, A. (1999) Filamentous phage infection: crystal structure of g3p in complex with its coreceptor, the C-terminal domain of TolA, Structure, 7, 711–722.
81. Mondigler, M., Holz, T., and Heller, K. J. (1996) Identification of the receptor-binding regions of pb5 proteins of bacteriophages T5 and BF23, Virology, 219, 19–28.
82. Broeker, N. K., and Barbirz, S. (2017) Not a barrier but a key: how bacteriophages exploit host’s O-antigen as an essential receptor to initiate infection, Mol. Microbiol., doi: 10.1111/mmi.13729.
83. Zaccheus, M. V., Broeker, N. K., Lundborg, M., Uetrecht, C., Barbirz, S., and Widmalm, G. (2012) Structural studies of the O-antigen polysaccharide from Escherichia coli TD2158 having O18 serogroup specificity and aspects of its interaction with the tailspike endoglycosidase of the infecting bacteriophage HK620, Carbohydr. Res., 357, 118–125.
84. Fischetti, V. A. (2010) Bacteriophage endolysins: a novel anti-infective to control Gram-positive pathogens, Int. J. Med. Microbiol., 300, 357–362.
85. Fischetti, V. A. (2005) Bacteriophage lytic enzymes: novel anti-infectives, Trends Microbiol., 13, 491–496.
86. Pires, D. P., Oliveira, H., Melo, L. D., Sillankorva, S., and Azeredo, J. (2016) Bacteriophage-encoded depolymerases: their diversity and biotechnological applications, Appl. Microbiol. Biotechnol., 100, 2141–2151.
87. Delbruck, M. (1940) The growth of bacteriophage and lysis of the host, J. Gen. Physiol., 23, 643–660.
88. Krueger, A. P. (1931) The sorption of bacteriophage by living and dead susceptible bacteria. I. Equilibrium conditions, J. Gen. Physiol., 14, 493–516.
89. Clokie, M. R. J., and Kropinski, A. M. (2009) Bacteriophages: Methods and Protocols, Humana Press, New York.
90. Gallet, R., Kannoly, S., and Wang, I. N. (2011) Effects of bacteriophage traits on plaque formation, BMC Microbiol., 11, 181.
91. Wiggins, B. A., and Alexander, M. (1985) Minimum bacterial density for bacteriophage replication: implications for significance of bacteriophages in natural ecosystems, Appl. Environ. Microbiol., 49, 19–23.
92. Kasman, L. M., Kasman, A., Westwater, C., Dolan, J., Schmidt, M. G., and Norris, J. S. (2002) Overcoming the phage replication threshold: a mathematical model with implications for phage therapy, J. Virol., 76, 5557–5564.
93. Abedon, S. (2011) Phage therapy pharmacology: calculating phage dosing, Adv. Appl. Microbiol., 77, 1–40.
94. Payne, R. J., and Jansen, V. A. (2001) Understanding bacteriophage therapy as a density-dependent kinetic process, J. Theor. Biol., 208, 37–48.
95. Kazi, M., and Annapure, U. S. (2016) Bacteriophage biocontrol of foodborne pathogens, J. Food Sci. Technol., 53, 1355–1362.
96. Sulakvelidze, A. (2013) Using lytic bacteriophages to eliminate or significantly reduce contamination of food by foodborne bacterial pathogens, J. Sci. Food Agric., 93, 3137–3146.
97. Guerrero-Ferreira, R. C., Viollier, P. H., Ely, B., Poindexter, J. S., Georgieva, M., Jensen, G. J., and Wright, E. R. (2011) Alternative mechanism for bacteriophage adsorption to the motile bacterium Caulobacter crescentus, Proc. Natl. Acad. Sci. USA, 108, 9963–9968.
98. Barr, J. J., Auro, R., Furlan, M., Whiteson, K. L., Erb, M. L., Pogliano, J., Stotland, A., Wolkowicz, R., Cutting, A. S., Doran, K. S., Salamon, P., Youle, M., and Rohwer, F. (2013) Bacteriophage adhering to mucus provide a non-host-derived immunity, Proc. Natl. Acad. Sci. USA, 110, 10771–10776.
99. Fraser, J. S., Maxwell, K. L., and Davidson, A. R. (2007) Immunoglobulin-like domains on bacteriophage: weapons of modest damage? Curr. Opin. Microbiol., 10, 382–387.
100. Fraser, J. S., Yu, Z., Maxwell, K. L., and Davidson, A. R. (2006) Ig-like domains on bacteriophages: a tale of promiscuity and deceit, J. Mol. Biol., 359, 496–507.
101. McPartland, J., and Rothman-Denes, L. B. (2009) The tail sheath of bacteriophage N4 interacts with the Escherichia coli receptor, J. Bacteriol., 191, 525–532.
102. Chan, J. Z., Millard, A. D., Mann, N. H., and Schafer, H. (2014) Comparative genomics defines the core genome of the growing N4-like phage genus and identifies N4-like roseophage specific genes, Front. Microbiol., 5, 506.
103. Knirel, Y. A., Prokhorov, N. S., Shashkov, A. S., Ovchinnikova, O. G., Zdorovenko, E. L., Liu, B., Kostryukova, E. S., Larin, A. K., Golomidova, A. K., and Letarov, A. V. (2015) Variations in O-antigen biosynthesis and O-acetylation associated with altered phage sensitivity in Escherichia coli 4s, J. Bacteriol., 197, 905–912.
104. Hu, B., Margolin, W., Molineux, I. J., and Liu, J. (2015) Structural remodeling of bacteriophage T4 and host membranes during infection initiation, Proc. Natl. Acad. Sci. USA, 112, E4919–4928.
105. Liu, J., Chen, C. Y., Shiomi, D., Niki, H., and Margolin, W. (2011) Visualization of bacteriophage P1 infection by cryo-electron tomography of tiny Escherichia coli, Virology, 417, 304–311.
106. Andres, D., Hanke, C., Baxa, U., Seul, A., Barbirz, S., and Seckler, R. (2010) Tailspike interactions with lipopolysaccharide effect DNA ejection from phage P22 particles in vitro, J. Biol. Chem., 285, 36768–36775.
107. Molineux, I. J. (2006) The T7 group, in The Bacteriophages (Calendar, R., ed.) 2nd Edn., Oxford University Press, Oxford-New York, pp. 277–301.
108. Parent, K. N., Erb, M. L., Cardone, G., Nguyen, K., Gilcrease, E. B., Porcek, N. B., Pogliano, J., Baker, T. S., and Casjens, S. R. (2014) OmpA and OmpC are critical host factors for bacteriophage Sf6 entry in Shigella, Mol. Microbiol., 92, 47–60.
109. Scholl, D., Adhya, S., and Merril, C. (2005) Escherichia coli K1′s capsule is a barrier to bacteriophage T7, Appl. Environ. Microbiol., 71, 4872–4874.
110. Scholl, D., and Merril, C. (2005) The genome of bacteriophage K1F, a T7-like phage that has acquired the ability to replicate on K1 strains of Escherichia coli, J. Bacteriol., 187, 8499–8503.
111. Zhan, L., Wang, S., Guo, Y., Jin, Y., Duan, J., Hao, Z., Lv, J., Qi, X., Hu, L., Chen, L., Kreiswirth, B. N., Zhang, R., Pan, J., Wang, L., and Yu, F. (2017) Outbreak by hypermucoviscous Klebsiella pneumoniae ST11 isolates with carbapenem resistance in a tertiary hospital in China, Front. Cell Infect. Microbiol., 7, 182.
112. Pan, Y. J., Lin, T. L., Chen, C. C., Tsai, Y. T., Cheng, Y. H., Chen, Y. Y., Hsieh, P. F., Lin, Y. T., and Wang, J. T. (2017) Klebsiella phage PhiK64-1 encodes multiple depolymerases for multiple host capsular types, J. Virol., 91, e02457–16.
113. Drulis-Kawa, Z., Majkowska-Skrobek, G., and Maciejewska, B. (2015) Bacteriophages and phage-derived proteins–application approaches, Curr. Med. Chem., 22, 1757–1773.
114. Edgar, R., Rokney, A., Feeney, M., Semsey, S., Kessel, M., Goldberg, M. B., Adhya, S., and Oppenheim, A. B. (2008) Bacteriophage infection is targeted to cellular poles, Mol. Microbiol., 68, 1107–1116.
115. Hu, B., Margolin, W., Molineux, I. J., and Liu, J. (2013) The bacteriophage t7 virion undergoes extensive structural remodeling during infection, Science, 339, 576–579.
116. Comeau, A. M., Bertrand, C., Letarov, A., Tetart, F., and Krisch, H. M. (2007) Modular architecture of the T4 phage superfamily: a conserved core genome and a plastic periphery, Virology, 362, 384–396.
117. Desplats, C., and Krisch, H. M. (2003) The diversity and evolution of the T4-type bacteriophages, Res. Microbiol., 154, 259–267.
118. Mosig, G., and Eiserling, F. (2006) T4 and related phages: structure and development, in The Bacteriophages (Calendar, R., ed.) 2nd Edn., Oxford University Press, Oxford-New York, pp. 225–267.
119. Leptihn, S., Gottschalk, J., and Kuhn, A. (2016) T7 ejectosome assembly: a story unfolds, Bacteriophage, 6, e1128513.
120. Jin, Y., Sdao, S. M., Dover, J. A., Porcek, N. B., Knobler, C. M., Gelbart, W. M., and Parent, K. N. (2015) Bacteriophage P22 ejects all of its internal proteins before its genome, Virology, 485, 128–134.
121. Moak, M., and Molineux, I. J. (2004) Peptidoglycan hydrolytic activities associated with bacteriophage virions, Mol. Microbiol., 51, 1169–1183.
122. Davydova, E. K., Kazmierczak, K. M., and Rothman-Denes, L. B. (2003) Bacteriophage N4-coded, virion-encapsulated DNA-dependent RNA polymerase, Methods Enzymol., 370, 83–94.
123. Sun, L., Rossmann, M. G., and Fane, B. A. (2014) High-resolution structure of a virally encoded DNA-translocating conduit and the mechanism of DNA penetration, J. Virol., 88, 10276–10279.
124. Xu, J., Gui, M., Wang, D., and Xiang, Y. (2016) The bacteriophage varphi29 tail possesses a pore-forming loop for cell membrane penetration, Nature, 534, 544–547.
125. Cumby, N., Reimer, K., Mengin-Lecreulx, D., Davidson, A. R., and Maxwell, K. L. (2015) The phage tail tape measure protein, an inner membrane protein and a periplasmic chaperone play connected roles in the genome injection process of E. coli phage HK97, Mol. Microbiol., 96, 437–447.
126. Molineux, I. J., and Panja, D. (2013) Popping the cork: mechanisms of phage genome ejection, Nat. Rev. Microbiol., 11, 194–204.
127. Foster, T. J. (2005) Immune evasion by staphylococci, Nat. Rev. Microbiol., 3, 948–958.
128. Nordstrom, K., and Forsgren, A. (1974) Effect of protein A on adsorption of bacteriophages to Staphylococcus aureus, J. Virol., 14, 198–202.
129. Pedruzzi, I., Rosenbusch, J. P., and Locher, K. P. (1998) Inactivation in vitro of the Escherichia coli outer membrane protein FhuA by a phage T5-encoded lipoprotein, FEMS Microbiol. Lett., 168, 119–125.
130. Riede, I., and Eschbach, M. L. (1986) Evidence that TraT interacts with OmpA of Escherichia coli, FEBS Lett., 205, 241–245.
131. Uhl, M. A., and Miller, J. F. (1996) Integration of multiple domains in a two-component sensor protein: the Bordetella pertussis BvgAS phosphorelay, EMBO J., 15, 1028–1036.
132. Beier, D., Fuchs, T. M., Graeff-Wohlleben, H., and Gross, R. (1996) Signal transduction and virulence regulation in Bordetella pertussis, Microbiologia, 12, 185–196.
133. Liu, M., Deora, R., Doulatov, S. R., Gingery, M., Eiserling, F. A., Preston, A., Maskell, D. J., Simons, R. W., Cotter, P. A., Parkhill, J., and Miller, J. F. (2002) Reverse transcriptase-mediated tropism switching in Bordetella bacteriophage, Science, 295, 2091–2094.
134. Stummeyer, K., Schwarzer, D., Claus, H., Vogel, U., Gerardy-Schahn, R., and Muhlenhoff, M. (2006) Evolution of bacteriophages infecting encapsulated bacteria: lessons from Escherichia coli K1-specific phages, Mol. Microbiol., 60, 1123–1135.
135. Kennedy, L., and Sutherland, I. W. (1994) Gellan lyases–novel polysaccharide lyases, Microbiology, 140, 3007–3013.
136. Sutherland, I. W. (1995) Polysaccharide lyases, FEMS Microbiol. Rev., 16, 323–347.
137. Sutherland, I. W. (1987) Xanthan lyases–novel enzymes found in various bacterial species, J. Gen. Microbiol., 133, 3129–3134.
138. Sutherland, I. W., Hughes, K. A., Skillman, L. C., and Tait, K. (2004) The interaction of phage and biofilms, FEMS Microbiol. Lett., 232, 1–6.
139. Hynes, W. L., Hancock, L., and Ferretti, J. J. (1995) Analysis of a second bacteriophage hyaluronidase gene from Streptococcus pyogenes: evidence for a third hyaluronidase involved in extracellular enzymatic activity, Infect. Immun., 63, 3015–3020.
140. McClean, D. (1941) Studies on diffusing factors: the hyaluronidase activity of testicular extracts, bacterial culture filtrates and other agents that increase tissue permeability, Biochem. J., 35, 159–183.
141. Kjems, E. (1955) Studies on streptococcal bacteriophages. I. Technique of isolating phage-producing strains, Acta Pathol. Microbiol. Scand., 36, 433–440.
142. Benchetrit, L. C., Gray, E. D., and Wannamaker, L. W. (1977) Hyaluronidase activity of bacteriophages of group A streptococci, Infect. Immun., 15, 527–532.
143. Destoumieux-Garzon, D., Duquesne, S., Peduzzi, J., Goulard, C., Desmadril, M., Letellier, L., Rebuffat, S., and Boulanger, P. (2005) The iron-siderophore transporter FhuA is the receptor for the antimicrobial peptide microcin J25: role of the microcin Val11-Pro16 beta-hairpin region in the recognition mechanism, Biochem. J., 389, 869–876.
144. Meyer, J. R., Dobias, D. T., Weitz, J. S., Barrick, J. E., Quick, R. T., and Lenski, R. E. (2012) Repeatability and contingency in the evolution of a key innovation in phage lambda, Science, 335, 428–432.
145. Burmeister, A. R., Lenski, R. E., and Meyer, J. R. (2016) Host coevolution alters the adaptive landscape of a virus, Proc. R. Soc. Lond. Ser. B Biol. Sci., 283, 20161528.
146. Morita, M., Fischer, C. R., Mizoguchi, K., Yoichi, M., Oda, M., Tanji, Y., and Unno, H. (2002) Amino acid alterations in Gp38 of host range mutants of PP01 and evidence for their infection of an ompC null mutant of Escherichia coli O157:H7, FEMS Microbiol. Lett., 216, 243–248.
147. Sandmeier, H. (1994) Acquisition and rearrangement of sequence motifs in the evolution of bacteriophage tail fibres, Mol. Microbiol., 12, 343–350.
148. Buth, S. A., Menin, L., Shneider, M. M., Engel, J., Boudko, S. P., and Leiman, P. G. (2015) Structure and biophysical properties of a triple-stranded beta-helix comprising the central spike of bacteriophage T4, Viruses, 7, 4676–4706.
149. Letarov, A., Manival, X., Desplats, C., and Krisch, H. M. (2005) gpwac of the T4-type bacteriophages: structure, function, and evolution of a segmented coiled-coil protein that controls viral infectivity, J. Bacteriol., 187, 1055–1066.
150. George, D. G., Yeh, L. S., and Barker, W. C. (1983) Unexpected relationships between bacteriophage lambda hypothetical proteins and bacteriophage T4 tail-fiber proteins, Biochem. Biophys. Res. Commun., 115, 1061–1068.
151. Trojet, S. N., Caumont-Sarcos, A., Perrody, E., Comeau, A. M., and Krisch, H. M. (2011) The gp38 adhesins of the T4 superfamily: a complex modular determinant of the phage’s host specificity, Genome Biol. Evol., 3, 674–686.
152. Tetart, F., Desplats, C., Kutateladze, M., Monod, C., Ackermann, H. W., and Krisch, H. M. (2001) Phylogeny of the major head and tail genes of the wide-ranging T4-type bacteriophages, J. Bacteriol., 183, 358–366.
153. Yoichi, M., Abe, M., Miyanaga, K., Unno, H., and Tanji, Y. (2005) Alteration of tail fiber protein gp38 enables T2 phage to infect Escherichia coli O157:H7, J. Biotechnol., 115, 101–107.
154. Kulikov, E., Kropinski, A. M., Golomidova, A., Lingohr, E., Govorun, V., Serebryakova, M., Prokhorov, N., Letarova, M., Manykin, A., Strotskaya, A., and Letarov, A. (2012) Isolation and characterization of a novel indigenous intestinal N4-related coliphage vB_ EcoP_ G7C, Virology, 426, 93–99.
155. Plasterk, R. H., Brinkman, A., and Van de Putte, P. (1983) DNA inversions in the chromosome of Escherichia coli and in bacteriophage Mu: relationship to other site-specific recombination systems, Proc. Natl. Acad. Sci. USA, 80, 5355–5358.
156. Grundy, F. J., and Howe, M. M. (1984) Involvement of the invertible G segment in bacteriophage mu tail fiber biosynthesis, Virology, 134, 296–317.
157. Johnson, R. C. (1991) Mechanism of site-specific DNA inversion in bacteria, Curr. Opin. Genet. Dev., 1, 404-411.
158. Guo, H., Arambula, D., Ghosh, P., and Miller, J. F. (2014) Diversity-generating retroelements in phage and bacterial genomes, Microbiol. Spectr., 2, doi: 10.1128/microbiolspec.MDNA3-0029-2014.
159. Toussaint, A. (2013) Transposable Mu-like phages in Firmicutes: new instances of divergence generating retroelements, Res. Microbiol., 164, 281–287.
160. Ye, Y. (2014) Identification of diversity-generating retroelements in human microbiomes, Int. J. Mol. Sci., 15, 14234–14246.
161. Minot, S., Grunberg, S., Wu, G. D., Lewis, J. D., and Bushman, F. D. (2012) Hypervariable loci in the human gut virome, Proc. Natl. Acad. Sci. USA, 109, 3962–3966.
162. Fokine, A., Zhang, Z., Kanamaru, S., Bowman, V. D., Aksyuk, A. A., Arisaka, F., Rao, V. B., and Rossmann, M. G. (2013) The molecular architecture of the bacteriophage T4 neck, J. Mol. Biol., 425, 1731–1744.
163. Stockdale, S. R., Mahony, J., Courtin, P., Chapot-Chartier, M. P., Van Pijkeren, J. P., Britton, R. A., Neve, H., Heller, K. J., Aideh, B., Vogensen, F. K., and Van Sinderen, D. (2013) The lactococcal phages Tuc2009 and TP901-1 incorporate two alternate forms of their tail fiber into their virions for infection specialization, J. Biol. Chem., 288, 5581–5590.
164. Gallet, R., Lenormand, T., and Wang, I. N. (2012) Phenotypic stochasticity protects lytic bacteriophage populations from extinction during the bacterial stationary phase, Evolution, 66, 3485–3494.
165. Storms, Z. J., and Sauvageau, D. (2014) Evidence that the heterogeneity of a T4 population is the result of heritable traits, PLoS One, 9, e116235.
166. Fisher, R. A., Gollan, B., and Helaine, S. (2017) Persistent bacterial infections and persister cells, Nat. Rev. Microbiol., 5, 453–464.
167. Langenscheid, J., Killmann, H., and Braun, V. (2004) A FhuA mutant of Escherichia coli is infected by phage T1-independent of TonB, FEMS Microbiol. Lett., 234, 133–137.
168. Sayers, J. (2006) Bacteriophage T5, in The Bacteriophages (Calendar, R., ed.) 2nd Edn., Oxford University Press, Oxford-New York, pp. 268–276.
169. Andres, D., Roske, Y., Doering, C., Heinemann, U., Seckler, R., and Barbirz, S. (2012) Tail morphology controls DNA release in two Salmonella phages with one lipopolysaccharide receptor recognition system, Mol. Microbiol., 83, 1244–1253.
170. Porcek, N. B., and Parent, K. N. (2015) Key residues of S. flexneri OmpA mediate infection by bacteriophage Sf6, J. Mol. Biol., 427, 1964–1976.
171. Javed, M. A., van Alphen, L. B., Sacher, J., Ding, W., Kelly, J., Nargang, C., Smith, D. F., Cummings, R. D., and Szymanski, C. M. (2015) A receptor-binding protein of Campylobacter jejuni bacteriophage NCTC 12673 recognizes flagellin glycosylated with acetamidino-modified pseudaminic acid, Mol. Microbiol., 95, 101–115.
172. Xu, D., Zhang, J., Liu, J., Xu, J., Zhou, H., Zhang, L., Zhu, J., and Kan, B. (2014) Outer membrane protein OmpW is the receptor for typing phage VP5 in the Vibrio cholerae O1 El Tor biotype, J. Virol., 88, 7109–7111.
173. Beczala, A., Ovchinnikova, O. G., Datta, N., Mattinen, L., Knapska, K., Radziejewska-Lebrecht, J., Holst, O., and Skurnik, M. (2015) Structure and genetic basis of Yersinia similis serotype O:9 O-specific polysaccharide, Innate Immun., 21, 3–16.
174. Kim, M., Kim, S., Park, B., and Ryu, S. (2014) Core lipopolysaccharide-specific phage SSU5 as an auxiliary component of a phage cocktail for Salmonella biocontrol, Appl. Environ. Microbiol., 80, 1026–1034.
175. Marti, R., Zurfluh, K., Hagens, S., Pianezzi, J., Klumpp, J., and Loessner, M. J. (2013) Long tail fibres of the novel broad-host-range T-even bacteriophage S16 specifically recognize Salmonella OmpC, Mol. Microbiol., 87, 818–834.
176. Kvitko, B. H., Cox, C. R., DeShazer, D., Johnson, S. L., Voorhees, K. J., and Schweizer, H. P. (2012) phiX216, a P2-like bacteriophage with broad Burkholderia pseudomallei and B. mallei strain infectivity, BMC Microbiol., 12, 289.
177. Kim, M., and Ryu, S. (2012) Spontaneous and transient defence against bacteriophage by phase-variable glucosylation of O-antigen in Salmonella enterica serovar typhimurium, Mol. Microbiol., 86, 411–425.
178. Kiljunen, S., Datta, N., Dentovskaya, S. V., Anisimov, A. P., Knirel, Y. A., Bengoechea, J. A., Holst, O., and Skurnik, M. (2011) Identification of the lipopolysaccharide core of Yersinia pestis and Yersinia pseudotuberculosis as the receptor for bacteriophage phiA1122, J. Bacteriol., 193, 4963–4972.
179. Turska-Szewczuk, A., Pietras, H., Pawelec, J., Mazur, A., and Russa, R. (2010) Morphology and general characteristics of bacteriophages infectious to Robinia pseudoacacia mesorhizobia, Curr. Microbiol., 61, 315–321.
180. Ricci, V., and Piddock, L. J. (2010) Exploiting the role of TolC in pathogenicity: identification of a bacteriophage for eradication of Salmonella serovars from poultry, Appl. Environ. Microbiol., 76, 1704–1706.
181. Begum, Y. A., Chakraborty, S., Chowdhury, A., Ghosh, A. N., Nair, G. B., Sack, R. B., Svennerholm, A. M., and Qadri, F. (2010) Isolation of a bacteriophage specific for CS7-expressing strains of enterotoxigenic Escherichia coli, J. Med. Microbiol., 59, 266–272.
182. Zhang, J., Li, W., Zhang, Q., Wang, H., Xu, X., Diao, B., Zhang, L., and Kan, B. (2009) The core oligosaccharide and thioredoxin of Vibrio cholerae are necessary for binding and propagation of its typing phage VP3, J. Bacteriol., 191, 2622–2629.
183. Hong, J., Kim, K. P., Heu, S., Lee, S. J., Adhya, S., and Ryu, S. (2008) Identification of host receptor and receptor-binding module of a newly sequenced T5-like phage EPS7, FEMS Microbiol. Lett., 289, 202–209.
184. +, FhuA-dependent phages, Arch. Virol., 153, 1271–1280.
185. Rabsch, W., Ma, L., Wiley, G., Najar, F. Z., Kaserer, W., Schuerch, D. W., Klebba, J. E., Roe, B. A., Laverde Gomez, J. A., Schallmey, M., Newton, S. M., and Klebba, P. E. (2007) FepA-and TonB-dependent bacteriophage H8: receptor binding and genomic sequence, J. Bacteriol., 189, 5658–5674.
186. Ko, Y. T. (2005) The receptor of an oyster juice-borne coliphage OJ367 in the outer membrane of Salmonella derby, J. Microbiol. Immunol. Infect., 38, 399–408.
187. Budzik, J. M., Rosche, W. A., Rietsch, A., and O’Toole, G. A. (2004) Isolation and characterization of a generalized transducing phage for Pseudomonas aeruginosa strains PAO1 and PA14, J. Bacteriol., 186, 3270–3273.
188. German, G. J., and Misra, R. (2001) The TolC protein of Escherichia coli serves as a cell-surface receptor for the newly characterized TLS bacteriophage, J. Mol. Biol., 308, 579–585.
189. Ho, T. D., and Slauch, J. M. (2001) OmpC is the receptor for Gifsy-1 and Gifsy-2 bacteriophages of Salmonella, J. Bacteriol., 183, 1495–1498.
190. Nesper, J., Kapfhammer, D., Klose, K. E., Merkert, H., and Reidl, J. (2000) Characterization of Vibrio cholerae O1 antigen as the bacteriophage K139 receptor and identification of IS1004 insertions aborting O1 antigen biosynthesis, J. Bacteriol., 182, 5097–5104.
191. Traurig, M., and Misra, R. (1999) Identification of bacteriophage K20 binding regions of OmpF and lipopolysaccharide in Escherichia coli K-12, FEMS Microbiol. Lett., 181, 101–108.
192. Sechaud, L., Rousseau, M., Fayard, B., Callegari, M. L., Quenee, P., and Accolas, J. P. (1992) Comparative study of 35 bacteriophages of Lactobacillus helveticus: morphology and host range, Appl. Environ. Microbiol., 58, 1011–1018.
193. Sao-Jose, C., Baptista, C., and Santos, M. A. (2004) Bacillus subtilis operon encoding a membrane receptor for bacteriophage SPP1, J. Bacteriol., 186, 8337–8346.