{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,24]],"date-time":"2026-04-24T06:05:28Z","timestamp":1777010728168,"version":"3.51.4"},"reference-count":44,"publisher":"American Society for Microbiology","issue":"14","license":[{"start":{"date-parts":[[2008,7,15]],"date-time":"2008-07-15T00:00:00Z","timestamp":1216080000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/journals.asm.org\/non-commercial-tdm-license"}],"content-domain":{"domain":["journals.asm.org"],"crossmark-restriction":true},"short-container-title":["J Bacteriol"],"published-print":{"date-parts":[[2008,7,15]]},"abstract":"<jats:title>ABSTRACT<\/jats:title><jats:p>Bacteriophage SPP1 targets the host cell membrane protein YueB to irreversibly adsorb and infect<jats:italic>Bacillus subtilis<\/jats:italic>. Interestingly, SPP1 still binds to the surface of<jats:italic>yueB<\/jats:italic>mutants, although in a completely reversible way. We evaluated here the relevance of a reversible step in SPP1 adsorption and identified the receptor(s) involved. We show that reversible adsorption is impaired in<jats:italic>B. subtilis<\/jats:italic>mutants defective in the glucosylation pathway of teichoic acids or displaying a modified chemical composition of these polymers. The results indicate that glucosylated poly(glycerolphosphate) cell wall teichoic acid is the major target for SPP1 reversible binding. Interaction with this polymer is characterized by a fast adsorption rate showing low-temperature dependence, followed by a rapid establishment of an equilibrium state between adsorbed and free phages. This equilibrium is basically determined by the rate of phage dissociation, which exhibits a strong dependence on temperature compatible with an Arrhenius law. This allowed us to determine an activation energy of 22.6 kcal\/mol for phage release. Finally, we show that SPP1 reversible interaction strongly accelerates irreversible binding to YueB. Our results support a model in which fast SPP1 adsorption to and desorption from teichoic acids allows SPP1 to scan the bacterial surface for rapid YueB recognition.<\/jats:p>","DOI":"10.1128\/jb.00349-08","type":"journal-article","created":{"date-parts":[[2008,5,17]],"date-time":"2008-05-17T00:45:48Z","timestamp":1210985148000},"page":"4989-4996","update-policy":"https:\/\/doi.org\/10.1128\/asmj-crossmark-policy-page","source":"Crossref","is-referenced-by-count":121,"title":["Phage SPP1 Reversible Adsorption to<i>Bacillus subtilis<\/i>Cell Wall Teichoic Acids Accelerates Virus Recognition of Membrane Receptor YueB"],"prefix":"10.1128","volume":"190","author":[{"given":"Catarina","family":"Baptista","sequence":"first","affiliation":[{"name":"Instituto de Cie\u0302ncia Aplicada e Tecnologia and Departamento de Biologia Vegetal, Faculdade de Cie\u0302ncias da Universidade de Lisboa, Ed. ICAT, 1749-016 Lisbon, Portugal"}]},{"given":"Ma\u0301rio A.","family":"Santos","sequence":"additional","affiliation":[{"name":"Instituto de Cie\u0302ncia Aplicada e Tecnologia and Departamento de Biologia Vegetal, Faculdade de Cie\u0302ncias da Universidade de Lisboa, Ed. ICAT, 1749-016 Lisbon, Portugal"}]},{"given":"Carlos","family":"Sa\u0303o-Jose\u0301","sequence":"additional","affiliation":[{"name":"Instituto de Cie\u0302ncia Aplicada e Tecnologia and Departamento de Biologia Vegetal, Faculdade de Cie\u0302ncias da Universidade de Lisboa, Ed. ICAT, 1749-016 Lisbon, Portugal"}]}],"member":"235","reference":[{"key":"e_1_3_2_2_2","first-page":"198","year":"1968","unstructured":"Adam, G., and M. Delbruck. 1968. Reduction of dimensionality in biological diffusion processes, p. 198-215. In A. Rich and N. Davidson (ed.), Structural chemistry and molecular biology. W. H. Freeman & Company, San Francisco, CA.","journal-title":"Structural chemistry and molecular biology."},{"key":"e_1_3_2_3_2","unstructured":"Bacteriophages. 1959"},{"key":"e_1_3_2_4_2","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1016\/S0006-3495(77)85544-6","volume":"20","year":"1977","unstructured":"Berg, H. C., and E. M. Purcell. 1977. Physics of chemoreception. Biophys. J. 20 : 193-219.","journal-title":"Biophys. J."},{"key":"e_1_3_2_5_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.113.1.198-202.1973"},{"key":"e_1_3_2_6_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.186.12.3970-3979.2004"},{"key":"e_1_3_2_7_2","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1016\/0022-2836(80)90283-1","volume":"138","year":"1980","unstructured":"Casadaban, M. J., and S. N. Cohen. 1980. Analysis of gene control signals by DNA fusion and cloning in Escherichia coli. J. Mol. Biol. 138 : 179-207.","journal-title":"J. Mol. Biol."},{"key":"e_1_3_2_8_2","doi-asserted-by":"crossref","first-page":"2172","DOI":"10.1073\/pnas.86.7.2172","volume":"86","year":"1989","unstructured":"Chung, C. T., S. L. Niemela, and R. H. Miller. 1989. One-step preparation of competent Escherichia coli: transformation and storage of bacterial cells in the same solution. Proc. Natl. Acad. Sci. USA 86 : 2172-2175.","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"e_1_3_2_9_2","doi-asserted-by":"crossref","first-page":"2385","DOI":"10.1021\/bi00846a048","volume":"7","year":"1968","unstructured":"Coyette, J., and J.-M. Ghuysen. 1968. Structure of the cell wall of Staphylococcus aureus, strain Copenhagen. IX. Teichoic acid and phage adsorption. Biochemistry 7 : 2385-2389.","journal-title":"Biochemistry"},{"key":"e_1_3_2_10_2","doi-asserted-by":"crossref","first-page":"1551","DOI":"10.1021\/bi00785a007","volume":"10","year":"1971","unstructured":"Douglas, L. J., and M. J. Wolin. 1971. Cell wall polymers and phage lysis of Lactobacillus plantarum. Biochemistry 10 : 1551-1555.","journal-title":"Biochemistry"},{"key":"e_1_3_2_11_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.109.2.652-658.1972"},{"key":"e_1_3_2_12_2","doi-asserted-by":"crossref","first-page":"1709","DOI":"10.1099\/mic.0.28814-0","volume":"152","year":"2006","unstructured":"Freymond, P. P., V. Lazarevic, B. Soldo, and D. Karamata. 2006. Poly(glucosyl-N-acetylgalactosamine 1-phosphate), a wall teichoic acid of Bacillus subtilis 168: its biosynthetic pathway and mode of attachment to peptidoglycan. Microbiology 152 : 1709-1718.","journal-title":"Microbiology"},{"key":"e_1_3_2_13_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.175.17.5510-5519.1993"},{"key":"e_1_3_2_14_2","doi-asserted-by":"crossref","first-page":"318","DOI":"10.1007\/BF00521298","volume":"133","year":"1982","unstructured":"Givan, A. L., K. Glassey, R. S. Green, W. K. Lang, A. J. Anderson, and A. R. Archibald. 1982. Relation between wall teichoic acid content of Bacillus subtilis and efficiency of adsorption of bacteriophages SP50 and \u03c625. Arch. Microbiol. 133 : 318-322.","journal-title":"Arch. Microbiol."},{"key":"e_1_3_2_15_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.139.1.32-38.1979"},{"key":"e_1_3_2_16_2","doi-asserted-by":"publisher","DOI":"10.1128\/jvi.41.1.222-227.1982"},{"key":"e_1_3_2_17_2","doi-asserted-by":"publisher","DOI":"10.1128\/jvi.21.3.1223-1227.1977"},{"key":"e_1_3_2_18_2","doi-asserted-by":"crossref","first-page":"419","DOI":"10.1046\/j.1365-2958.1998.00930.x","volume":"29","year":"1998","unstructured":"Jorasch, P., F. P. Wolter, U. Z\u00e4hringer, and E. Heinz. 1998. A UDP glucosyltransferase from Bacillus subtilis successively transfers up to four glucose residues to 1,2-diacylglycerol: expression of ypfP in Escherichia coli and structural analysis of its reaction products. Mol. Microbiol. 29 : 419-430.","journal-title":"Mol. Microbiol."},{"key":"e_1_3_2_19_2","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1007\/BF00331493","volume":"207","year":"1987","unstructured":"Karamata, D., H. M. Pooley, and M. Monod. 1987. Expression of heterologous genes for wall teichoic acid in Bacillus subtilis 168. Mol. Gen. Genet. 207 : 73-81.","journal-title":"Mol. Gen. Genet."},{"key":"e_1_3_2_20_2","doi-asserted-by":"crossref","first-page":"739","DOI":"10.1111\/j.1365-2958.2004.04440.x","volume":"55","year":"2005","unstructured":"Kearns, D. B., F. Chu, S. S. Branda, R. Kolter, and R. Losick. 2005. A master regulator for biofilm formation by Bacillus subtilis. Mol. Microbiol. 55 : 739-749.","journal-title":"Mol. Microbiol."},{"key":"e_1_3_2_21_2","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1016\/j.virol.2005.06.039","volume":"340","year":"2005","unstructured":"Kemp, P., L. R. Garcia, and I. J. Molineux. 2005. Changes in bacteriophage T7 virion structure at the initiation of infection. Virology 340 : 307-317.","journal-title":"Virology"},{"key":"e_1_3_2_22_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.71.1.39-45.2005"},{"key":"e_1_3_2_23_2","doi-asserted-by":"crossref","first-page":"3437","DOI":"10.1099\/13500872-142-12-3437","volume":"142","year":"1996","unstructured":"Margot, P., and D. Karamata. 1996. The wprA gene of Bacillus subtilis 168, expressed during exponential growth, encodes a cell-wall-associated protease. Microbiology 142 : 3437-3444.","journal-title":"Microbiology"},{"key":"e_1_3_2_24_2","doi-asserted-by":"crossref","first-page":"929","DOI":"10.1099\/00221287-137-4-929","volume":"137","year":"1991","unstructured":"Mau\u00ebl, C., M. Young, and D. Karamata. 1991. Genes concerned with synthesis of poly(glycerol phosphate), the essential teichoic acid in Bacillus subtilis strain 168, are organized in two divergent transcription units. J. Gen. Microbiol. 137 : 929-941.","journal-title":"J. Gen. Microbiol."},{"key":"e_1_3_2_25_2","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1529\/biophysj.106.102962","volume":"93","year":"2007","unstructured":"Moldovan, R., E. Chapman-McQuiston, and X. L. Wu. 2007. On kinetics of phage adsorption. Biophys. J. 93 : 303-315.","journal-title":"Biophys. J."},{"key":"e_1_3_2_26_2","doi-asserted-by":"publisher","DOI":"10.1128\/aem.60.9.3204-3211.1994"},{"key":"e_1_3_2_27_2","doi-asserted-by":"crossref","first-page":"552","DOI":"10.1016\/0042-6822(64)90207-7","volume":"24","year":"1964","unstructured":"Okubo, S., B. Strauss, and M. Stodolsky. 1964. The possible role of recombination in the infection of competent Bacillus subtilis by bacteriophage deoxyribonucleic acid. Virology 24 : 552-562.","journal-title":"Virology"},{"key":"e_1_3_2_28_2","doi-asserted-by":"crossref","first-page":"3720","DOI":"10.1038\/sj.emboj.7601786","volume":"26","year":"2007","unstructured":"Plisson, C., H. E. White, I. Auzat, A. Zafarani, C. S\u00e3o-Jos\u00e9, S. Lhuillier, P. Tavares, and E. V. Orlova. 2007. Structure of bacteriophage SPP1 tail reveals trigger for DNA ejection. EMBO J. 26 : 3720-3728.","journal-title":"EMBO J."},{"key":"e_1_3_2_29_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.179.15.4959-4961.1997"},{"key":"e_1_3_2_30_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.00078-07"},{"key":"e_1_3_2_31_2","doi-asserted-by":"crossref","first-page":"3999","DOI":"10.1529\/biophysj.107.111435","volume":"93","year":"2007","unstructured":"Raspaud, E., T. Forth, C. S\u00e3o-Jos\u00e9, P. Tavares, and M. de Frutos. 2007. A kinetic analysis of DNA ejection from tailed phages revealing the prerequisite activation energy. Biophys. J. 93 : 3999-4005.","journal-title":"Biophys. J."},{"key":"e_1_3_2_32_2","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1016\/S0022-2836(68)80029-4","volume":"35","year":"1968","unstructured":"Riva, S., M. Polsinelli, and A. Falaschi. 1968. A new phage of Bacillus subtilis with infectious DNA having separable strands. J. Mol. Biol. 35 : 347-356.","journal-title":"J. Mol. Biol."},{"key":"e_1_3_2_33_2","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1016\/j.sbi.2004.02.001","volume":"14","year":"2004","unstructured":"Rossmann, M. G., V. V. Mesyanzhinov, F. Arisaka, and P. G. Leiman. 2004. The bacteriophage T4 DNA injection machine. Curr. Opin. Struct. Biol. 14 : 171-180.","journal-title":"Curr. Opin. Struct. Biol."},{"key":"e_1_3_2_34_2","unstructured":"Sambrook J. and D. W. Russell. 2001. Molecular cloning: a laboratory manual 3rd ed. Cold Spring Harbor Laboratory Press Cold Spring Harbor NY."},{"key":"e_1_3_2_35_2","unstructured":"Santos M. A. 1991. Bacteri\u00f3fagos de Bacillus subtilis do grupo SPP1: caracter\u00edsticas gerais especificidade de adsor\u00e7\u00e3o e organiza\u00e7\u00e3o gen\u00f3mica. Ph.D. thesis. University of Lisbon Lisbon Portugal."},{"key":"e_1_3_2_36_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.186.24.8337-8346.2004"},{"key":"e_1_3_2_37_2","doi-asserted-by":"crossref","first-page":"11464","DOI":"10.1074\/jbc.M513625200","volume":"281","year":"2006","unstructured":"S\u00e3o-Jos\u00e9, C., S. Lhuillier, R. Lurz, R. Melki, J. Lepault, M. A. Santos, and P. Tavares. 2006. The ectodomain of the viral receptor YueB forms a fiber that triggers ejection of bacteriophage SPP1 DNA. J. Biol. Chem. 281 : 11464-11470.","journal-title":"J. Biol. Chem."},{"key":"e_1_3_2_38_2","doi-asserted-by":"crossref","first-page":"346","DOI":"10.1016\/j.jmb.2007.09.045","volume":"374","year":"2007","unstructured":"S\u00e3o-Jos\u00e9, C., M. de Frutos, E. Raspaud, M. A. Santos, and P. Tavares. 2007. Pressure built by DNA packing inside virions: enough to drive DNA ejection in vitro, largely insufficient for delivery into the bacterial cytoplasm. J. Mol. Biol. 374 : 346-355.","journal-title":"J. Mol. Biol."},{"key":"e_1_3_2_39_2","doi-asserted-by":"crossref","first-page":"3185","DOI":"10.1099\/00221287-139-12-3185","volume":"139","year":"1993","unstructured":"Soldo, B., V. Lazarevic, P. Margot, and D. Karamata. 1993. Sequencing and analysis of the divergon comprising gtaB, the structural gene of UDP-glucose pyrophosphorylase of Bacillus subtilis 168. J. Gen. Microbiol. 139 : 3185-3195.","journal-title":"J. Gen. Microbiol."},{"key":"e_1_3_2_40_2","doi-asserted-by":"crossref","first-page":"3097","DOI":"10.1099\/00221287-144-11-3097","volume":"144","year":"1998","unstructured":"Vagner, V., E. Dervyn, and S. D. Ehrlich. 1998. A vector for systematic gene inactivation in Bacillus subtilis. Microbiology 144 : 3097-3104.","journal-title":"Microbiology"},{"key":"e_1_3_2_41_2","first-page":"165","year":"2006","unstructured":"Vinga, I., C. S\u00e3o-Jos\u00e9, M. A. Santos, and P. Tavares. 2006. Bacteriophage entry in the host cell, p. 165-205. In G. Wegrzyn (ed.), Modern bacteriophage biology and biotechnology. Research Signpost, Trivandrum, India.","journal-title":"Modern bacteriophage biology and biotechnology."},{"key":"e_1_3_2_42_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.113.2.540-548.1973"},{"key":"e_1_3_2_43_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.125.3.1120-1126.1976"},{"key":"e_1_3_2_44_2","doi-asserted-by":"crossref","first-page":"2377","DOI":"10.1073\/pnas.58.6.2377","volume":"58","year":"1967","unstructured":"Young, F. E. 1967. Requirement of glucosylated teichoic acid for adsorption of phage in Bacillus subtilis 168. Proc. Natl. Acad. Sci. USA 58 : 2377-2384.","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"e_1_3_2_45_2","doi-asserted-by":"crossref","first-page":"1805","DOI":"10.1111\/j.1365-2958.1989.tb00166.x","volume":"3","year":"1989","unstructured":"Young, M., C. Mau\u00ebl, P. Margot, and D. Karamata. 1989. Pseudo-allelic relationship between non-homologous genes concerned with biosynthesis of polyglycerol phosphate and polyribitol phosphate teichoic acids in Bacillus subtilis strains 168 and W23. Mol. Microbiol. 3 : 1805-1812.","journal-title":"Mol. Microbiol."}],"updated-by":[{"DOI":"10.1128\/jb.01808-08","type":"correction","label":"Correction","source":"publisher","updated":{"date-parts":[[2020,12,20]],"date-time":"2020-12-20T00:00:00Z","timestamp":1608422400000}}],"container-title":["Journal of Bacteriology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/JB.00349-08","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/JB.00349-08","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,2,26]],"date-time":"2024-02-26T11:48:26Z","timestamp":1708948106000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.asm.org\/doi\/10.1128\/JB.00349-08"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2008,7,15]]},"references-count":44,"journal-issue":{"issue":"14","published-print":{"date-parts":[[2008,7,15]]}},"alternative-id":["10.1128\/JB.00349-08"],"URL":"https:\/\/doi.org\/10.1128\/jb.00349-08","relation":{},"ISSN":["0021-9193","1098-5530"],"issn-type":[{"value":"0021-9193","type":"print"},{"value":"1098-5530","type":"electronic"}],"subject":[],"published":{"date-parts":[[2008,7,15]]},"assertion":[{"value":"2008-03-10","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2008-05-08","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2020-12-20","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}