{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,16]],"date-time":"2026-03-16T11:31:52Z","timestamp":1773660712552,"version":"3.50.1"},"reference-count":35,"publisher":"American Society for Microbiology","issue":"18","license":[{"start":{"date-parts":[[2009,9,15]],"date-time":"2009-09-15T00:00:00Z","timestamp":1252972800000},"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":[[2009,9,15]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n          <jats:p>\n            The bacterial spore cortex is critical for spore stability and dormancy and must be hydrolyzed by germination-specific lytic enzymes (GSLEs), which allows complete germination and vegetative cell outgrowth. We created in-frame deletions of three genes that encode GSLEs that have been shown to be active in\n            <jats:italic>Bacillus anthracis<\/jats:italic>\n            germination:\n            <jats:italic>sleB<\/jats:italic>\n            ,\n            <jats:italic>cwlJ1<\/jats:italic>\n            , and\n            <jats:italic>cwlJ2<\/jats:italic>\n            . Phenotypic analysis of individual null mutations showed that the removal of any one of these genes was not sufficient to disrupt spore germination in nutrient-rich media. This finding indicates that these genes have partially redundant functions. Double and triple deletions of these genes resulted in more significant defects. Although a small subset of \u0394\n            <jats:italic>sleB<\/jats:italic>\n            \u0394\n            <jats:italic>cwlJ1<\/jats:italic>\n            spores germinate with wild-type kinetics, for the overall population there is a 3-order-of-magnitude decrease in the colony-forming efficiency compared with wild-type spores. \u0394\n            <jats:italic>sleB<\/jats:italic>\n            \u0394\n            <jats:italic>cwlJ1<\/jats:italic>\n            \u0394\n            <jats:italic>cwlJ2<\/jats:italic>\n            spores are unable to complete germination in nutrient-rich conditions in vitro. Both \u0394\n            <jats:italic>sleB<\/jats:italic>\n            \u0394\n            <jats:italic>cwlJ1<\/jats:italic>\n            and \u0394\n            <jats:italic>sleB<\/jats:italic>\n            \u0394\n            <jats:italic>cwlJ1<\/jats:italic>\n            \u0394\n            <jats:italic>cwlJ2<\/jats:italic>\n            spores are significantly attenuated, but are not completely devoid of virulence, in a mouse model of inhalation anthrax. Although unable to germinate in standard nutrient-rich media, spores lacking SleB, CwlJ1, and CwlJ2 are able to germinate in whole blood and serum in vitro, which may explain the persistent low levels of virulence observed in mouse infections. This work contributes to our understanding of GSLE activation and function during germination. This information may result in identification of useful therapeutic targets for the disease anthrax, as well as provide insights into ways to induce the breakdown of the protective cortex layer, facilitating easier decontamination of resistant spores.\n          <\/jats:p>","DOI":"10.1128\/jb.00408-09","type":"journal-article","created":{"date-parts":[[2009,7,7]],"date-time":"2009-07-07T01:06:32Z","timestamp":1246928792000},"page":"5569-5576","update-policy":"https:\/\/doi.org\/10.1128\/asmj-crossmark-policy-page","source":"Crossref","is-referenced-by-count":49,"title":["The Germination-Specific Lytic Enzymes SleB, CwlJ1, and CwlJ2 Each Contribute to\n            <i>Bacillus anthracis<\/i>\n            Spore Germination and Virulence"],"prefix":"10.1128","volume":"191","author":[{"given":"Jonathan D.","family":"Giebel","sequence":"first","affiliation":[{"name":"Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor, Michigan 48109"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Katherine A.","family":"Carr","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor, Michigan 48109"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Erica C.","family":"Anderson","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor, Michigan 48109"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Philip C.","family":"Hanna","sequence":"additional","affiliation":[{"name":"Department of Microbiology and Immunology, University of Michigan Medical School, Ann Arbor, Michigan 48109"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"235","reference":[{"key":"e_1_3_2_2_2","doi-asserted-by":"publisher","DOI":"10.1128\/br.25.3.268-273.1961"},{"key":"e_1_3_2_3_2","doi-asserted-by":"crossref","first-page":"2925","DOI":"10.1099\/00221287-147-11-2925","volume":"147","year":"2001","unstructured":"Atrih, A., and S. J. Foster. 2001. In vivo roles of the germination-specific lytic enzymes of Bacillus subtilis 168. Microbiology 147 : 2925-2932.","journal-title":"Microbiology"},{"key":"e_1_3_2_4_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.184.4.1219-1224.2002"},{"key":"e_1_3_2_5_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.00723-06"},{"key":"e_1_3_2_6_2","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1099\/00221287-146-1-57","volume":"146","year":"2000","unstructured":"Boland, F. M., A. Atrih, H. Chirakkal, S. J. Foster, and A. Moir. 2000. Complete spore-cortex hydrolysis during germination of Bacillus subtilis 168 requires SleB and YpeB. Microbiology 146 : 57-64.","journal-title":"Microbiology"},{"key":"e_1_3_2_7_2","doi-asserted-by":"crossref","first-page":"2383","DOI":"10.1099\/00221287-148-8-2383","volume":"148","year":"2002","unstructured":"Chirakkal, H., M. O'Rourke, A. Atrih, S. J. Foster, and A. Moir. 2002. Analysis of spore cortex lytic enzymes and related proteins in Bacillus subtilis endospore germination. Microbiology 148 : 2383-2392.","journal-title":"Microbiology"},{"key":"e_1_3_2_8_2","doi-asserted-by":"crossref","first-page":"453","DOI":"10.1046\/j.1462-5822.2000.00067.x","volume":"2","year":"2000","unstructured":"Dixon, T. C., A. A. Fadl, T. M. Koehler, J. A. Swanson, and P. C. Hanna. 2000. Early Bacillus anthracis-macrophage interactions: intracellular survival and escape. Cell. Microbiol. 2 : 453-463.","journal-title":"Cell. Microbiol."},{"key":"e_1_3_2_9_2","doi-asserted-by":"crossref","first-page":"815","DOI":"10.1056\/NEJM199909093411107","volume":"341","year":"1999","unstructured":"Dixon, T. C., M. Meselson, J. Guillemin, and P. C. Hanna. 1999. Anthrax. N. Engl. J. Med. 341 : 815-826.","journal-title":"N. Engl. J. Med."},{"key":"e_1_3_2_10_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.187.23.8055-8062.2005"},{"key":"e_1_3_2_11_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.188.4.1301-1309.2006"},{"key":"e_1_3_2_12_2","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1046\/j.1365-2958.1999.01137.x","volume":"31","year":"1999","unstructured":"Guidi-Rontani, C., M. Weber-Levy, E. Labruyere, and M. Mock. 1999. Germination of Bacillus anthracis spores within alveolar macrophages. Mol. Microbiol. 31 : 9-17.","journal-title":"Mol. Microbiol."},{"key":"e_1_3_2_13_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.73.7.4420-4422.2005"},{"key":"e_1_3_2_14_2","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1111\/j.1574-6968.2007.00713.x","volume":"271","year":"2007","unstructured":"Heffernan, B. J., B. Thomason, A. Herring-Palmer, and P. Hanna. 2007. Bacillus anthracis anthrolysin O and three phospholipases C are functionally redundant in a murine model of inhalation anthrax. FEMS Microbiol. Lett. 271 : 98-105.","journal-title":"FEMS Microbiol. Lett."},{"key":"e_1_3_2_15_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.01598-08"},{"key":"e_1_3_2_16_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.180.6.1375-1380.1998"},{"key":"e_1_3_2_17_2","doi-asserted-by":"publisher","DOI":"10.1128\/IAI.74.3.1949-1953.2006"},{"key":"e_1_3_2_18_2","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1111\/j.1365-2672.1974.tb00438.x","volume":"37","year":"1974","unstructured":"Kim, H. U., and J. M. Goepfert. 1974. A sporulation medium for Bacillus anthracis. J. Appl. Bacteriol. 37 : 265-267.","journal-title":"J. Appl. Bacteriol."},{"key":"e_1_3_2_19_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.01526-06"},{"key":"e_1_3_2_20_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.186.1.164-178.2004"},{"key":"e_1_3_2_21_2","doi-asserted-by":"crossref","first-page":"526","DOI":"10.1111\/j.1365-2672.2006.02885.x","volume":"101","year":"2006","unstructured":"Moir, A. 2006. How do spores germinate? J. Appl. Microbiol. 101 : 526-530.","journal-title":"J. Appl. Microbiol."},{"key":"e_1_3_2_22_2","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1007\/s00018-002-8432-8","volume":"59","year":"2002","unstructured":"Moir, A., B. M. Corfe, and J. Behravan. 2002. Spore germination. Cell. Mol. Life Sci. 59 : 403-409.","journal-title":"Cell. Mol. Life Sci."},{"key":"e_1_3_2_23_2","doi-asserted-by":"publisher","DOI":"10.1128\/jb.178.17.5330-5332.1996"},{"key":"e_1_3_2_24_2","first-page":"391","year":"1990","unstructured":"Nicholson, W. L., and P. Setlow. 1990. Sporulation, germination and outgrowth, p. 391-450. In C. R. Harwood and S. M. Cutting (ed.), Molecular biological methods for Bacillus. John Wiley & Sons Ltd., Chichester, United Kingdom.","journal-title":"Molecular biological methods for Bacillus"},{"key":"e_1_3_2_25_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.183.16.4886-4893.2001"},{"key":"e_1_3_2_26_2","doi-asserted-by":"crossref","first-page":"426","DOI":"10.1007\/s00018-002-8435-5","volume":"59","year":"2002","unstructured":"Popham, D. L. 2002. Specialized peptidoglycan of the bacterial endospore: the inner wall of the lockbox. Cell. Mol. Life Sci. 59 : 426-433.","journal-title":"Cell. Mol. Life Sci."},{"key":"e_1_3_2_27_2","doi-asserted-by":"publisher","DOI":"10.1128\/JB.185.7.2315-2329.2003"},{"key":"e_1_3_2_28_2","first-page":"493","volume":"27","year":"1938","unstructured":"Reed, L. J., and H. Muench. 1938. A simple method of estimating fifty per cent endpoints. Am. J. Hyg. 27 : 493-497.","journal-title":"Am. J. Hyg."},{"key":"e_1_3_2_29_2","first-page":"336","volume":"36","year":"1955","unstructured":"Ross, J. M. 1955. On the histopathology of experimental anthrax in the guinea-pig. Br. J. Exp. Pathol. 36 : 336-339.","journal-title":"Br. J. Exp. Pathol."},{"key":"e_1_3_2_30_2","doi-asserted-by":"crossref","first-page":"485","DOI":"10.1002\/path.1700730219","volume":"73","year":"1957","unstructured":"Ross, J. M. 1957. The pathogenesis of anthrax following the administration of spores by the respiratory route. J. Pathol Bacteriol. 73 : 485-494.","journal-title":"J. Pathol Bacteriol."},{"key":"e_1_3_2_31_2","unstructured":"Molecular cloning: a laboratory manual 2001"},{"key":"e_1_3_2_32_2","doi-asserted-by":"crossref","first-page":"318","DOI":"10.1111\/j.1365-2672.2009.04210.x","volume":"107","year":"2009","unstructured":"Setlow, B., L. Peng, C. A. Loshon, Y. Q. Li, G. Christie, and P. Setlow. 2009. Characterization of the germination of Bacillus megaterium spores lacking enzymes that degrade the spore cortex. J. Appl. Microbiol. 107 : 318-328.","journal-title":"J. Appl. Microbiol."},{"key":"e_1_3_2_33_2","doi-asserted-by":"crossref","first-page":"550","DOI":"10.1016\/j.mib.2003.10.001","volume":"6","year":"2003","unstructured":"Setlow, P. 2003. Spore germination. Curr. Opin. Microbiol. 6 : 550-556.","journal-title":"Curr. Opin. Microbiol."},{"key":"e_1_3_2_34_2","first-page":"313","volume":"13","year":"1939","unstructured":"Sterne, M. 1939. The immunization of laboratory animals against anthrax. J. Vet. Sci. Anim. Ind. 13 : 313-317.","journal-title":"J. Vet. Sci. Anim. Ind."},{"key":"e_1_3_2_35_2","doi-asserted-by":"crossref","first-page":"555","DOI":"10.1111\/j.1462-5822.2006.00866.x","volume":"9","year":"2007","unstructured":"Tournier, J. N., A. Quesnel-Hellmann, A. Cleret, and D. R. Vidal. 2007. Contribution of toxins to the pathogenesis of inhalational anthrax. Cell. Microbiol. 9 : 555-565.","journal-title":"Cell. Microbiol."},{"key":"e_1_3_2_36_2","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/0882-4010(89)90108-3","volume":"7","year":"1989","unstructured":"Welkos, S. L., R. W. Trotter, D. M. Becker, and G. O. Nelson. 1989. Resistance to the Sterne strain of B. anthracis: phagocytic cell responses of resistant and susceptible mice. Microb. Pathog. 7 : 15-35.","journal-title":"Microb. Pathog."}],"container-title":["Journal of Bacteriology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/JB.00408-09","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/JB.00408-09","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,7,29]],"date-time":"2021-07-29T17:09:11Z","timestamp":1627578551000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.asm.org\/doi\/10.1128\/JB.00408-09"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2009,9,15]]},"references-count":35,"journal-issue":{"issue":"18","published-print":{"date-parts":[[2009,9,15]]}},"alternative-id":["10.1128\/JB.00408-09"],"URL":"https:\/\/doi.org\/10.1128\/jb.00408-09","relation":{},"ISSN":["0021-9193","1098-5530"],"issn-type":[{"value":"0021-9193","type":"print"},{"value":"1098-5530","type":"electronic"}],"subject":[],"published":{"date-parts":[[2009,9,15]]},"assertion":[{"value":"2009-03-26","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2009-06-22","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"}}]}}