Role of YpeB in cortex hydrolysis during germination of Bacillus anthracis spores

Journal of Bacteriology

Volumn 196, Issue 19, 2014, Pages 3399-3409

  Bernhards, Casey B ^a   Popham, David L ^a  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; SLEB PROTEIN; UNCLASSIFIED DRUG; YPEB PROTEIN;

ARTICLE; BACILLUS ANTHRACIS; BACTERIAL SPORE; NONHUMAN; PHENOTYPE; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; SITE DIRECTED MUTAGENESIS; SPORE GERMINATION; SPOROGENESIS; CHEMISTRY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HYDROLYSIS; METABOLISM;

BACILLUS ANTHRACIS; BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; HYDROLYSIS; SPORES, BACTERIAL;

EID: 84907016410     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01899-14     Document Type: Article

References (56)

1. Setlow P. 2003. Spore germination. Curr. Opin. Microbiol. 6:550-556. http://dx.doi.org/10.1016/j.mib.2003.10.001.
2. Setlow P. 2006. Spores of Bacillus subtilis: their resistance to and killing by radiation, heat and chemicals. J. Appl. Microbiol. 101:514-525. http://dx .doi.org/10.1111/j.1365-2672.2005.02736.x.
3. Nicholson WL, Munakata N, Horneck G, Melosh HJ, Setlow P. 2000. Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol. Mol. Biol. Rev. 64:548-572. http://dx.doi .org/10.1128/MMBR.64.3.548-572.2000.
4. Gould GW. 2006. History of science-spores. J. Appl. Microbiol. 101: 507-513. http://dx.doi.org/10.1111/j.1365-2672.2006.02888.x.
5. Gerhardt P, Marquis RE. 1989. Spore thermoresistance mechanisms, p 43-63. In Smith I, Slepecky RA, Setlow P (ed), Regulation of prokaryotic development. American Society for Microbiology, Washington, DC.
6. Warth AD, Strominger JL. 1969. Structure of the peptidoglycan of bacterial spores: occurrence of the lactam of muramic acid. Proc. Natl. Acad. Sci. U. S. A. 64:528-535. http://dx.doi.org/10.1073/pnas.64.2.528.
7. Atrih A, Zo¨llner P, Allmaier G, Foster SJ. 1996. Structural analysis of Bacillus subtilis 168 endospore peptidoglycan and its role during differentiation. J. Bacteriol. 178:6173-6183.
8. Popham DL, Helin J, Costello CE, Setlow P. 1996. Analysis of the peptidoglycan structure of Bacillus subtilis endospores. J. Bacteriol. 178: 6451-6458.
9. Atrih A, Bacher G, Ko¨rner R, Allmaier G, Foster SJ. 1999. Structural analysis of Bacillus megaterium KM spore peptidoglycan and its dynamics during germination. Microbiology 145:1033-1041. http://dx.doi.org/10 .1099/13500872-145-5-1033.
10. Dowd MM, Orsburn B, Popham DL. 2008. Cortex peptidoglycan lytic activity in germinating Bacillus anthracis spores. J. Bacteriol. 190:4541- 4548. http://dx.doi.org/10.1128/JB.00249-08.
11. Atrih A, Foster SJ. 2001. Analysis of the role of bacterial endospore cortex structure in resistance properties and demonstration of its conservation amongst species. J. Appl. Microbiol. 91:364-372. http://dx.doi.org/10 .1046/j.1365-2672.2001.01394.x.
12. Mock M, Fouet A. 2001. Anthrax. Annu. Rev. Microbiol. 55:647-671. http://dx.doi.org/10.1146/annurev.micro.55.1.647.
13. Sweeney DA, Hicks CW, Cui X, Li Y, Eichacker PQ. 2011. Anthrax infection. Am. J. Respir. Crit. Care Med. 184:1333-1341. http://dx.doi.org /10.1164/rccm.201102-0209CI.
14. Setlow B, Melly E, Setlow P. 2001. Properties of spores of Bacillus subtilis blocked at an intermediate stage in spore germination. J. Bacteriol. 183: 4894-4899. http://dx.doi.org/10.1128/JB.183.16.4894-4899.2001.
15. Makino S, Moriyama R. 2002. Hydrolysis of cortex peptidoglycan during bacterial spore germination. Med. Sci. Monit. 8:RA119-RA127.
16. Popham DL, Bernhards CB. Spore peptidoglycan. In Driks A, Eichenberger P (ed), The bacterial spore: from molecules to systems, in press. ASM Press, Washington, DC.
17. Popham DL, Helin J, Costello CE, Setlow P. 1996. Muramic lactam in peptidoglycan of Bacillus subtilis spores is required for spore outgrowth but not for spore dehydration or heat resistance. Proc. Natl. Acad. Sci. U. S. A. 93:15405-15410. http://dx.doi.org/10.1073/pnas.93.26.15405.
18. Chen Y, Fukuoka S, Makino S. 2000. A novel spore peptidoglycan hydrolase of Bacillus cereus: biochemical characterization and nucleotide sequence of the corresponding gene, sleL. J. Bacteriol. 182:1499-1506. http: //dx.doi.org/10.1128/JB.182.6.1499-1506.2000.
19. Chen Y, Miyata S, Makino S, Moriyama R. 1997. Molecular characterization of a germination-specific muramidase from Clostridium perfringens S40 spores and nucleotide sequence of the corresponding gene. J. Bacteriol. 179:3181-3187.
20. Lambert EA, Sherry N, Popham DL. 2012. In vitro and in vivo analyses of the Bacillus anthracis spore cortex lytic protein SleL. Microbiology 158: 1359-1368. http://dx.doi.org/10.1099/mic.0.056630-0.
21. Heffron JD, Sherry N, Popham DL. 2011. In vitro studies of peptidoglycan binding and hydrolysis by the Bacillus anthracis germination-specific lytic enzyme SleB. J. Bacteriol. 193:125-131. http://dx.doi.org/10.1128/JB .00869-10.
22. Lambert EA, Popham DL. 2008. The Bacillus anthracis SleL (YaaH) protein is anN-acetylglucosaminidase involved in spore cortex depolymerization. J. Bacteriol. 190:7601-7607. http://dx.doi.org/10.1128/JB.01054-08.
23. Heffron JD, Orsburn B, Popham DL. 2009. Roles of germinationspecific lytic enzymes CwlJ and SleB in Bacillus anthracis. J. Bacteriol. 191:2237-2247. http://dx.doi.org/10.1128/JB.01598-08.
24. Heffron JD, Lambert EA, Sherry N, Popham DL. 2010. Contributions of four cortex lytic enzymes to germination of Bacillus anthracis spores. J. Bacteriol. 192:763-770. http://dx.doi.org/10.1128/JB.01380-09.
25. Giebel JD, Carr KA, Anderson EC, Hanna PC. 2009. The germinationspecific lytic enzymes SleB, CwlJ1, and CwlJ2 each contribute to Bacillus anthracis spore germination and virulence. J. Bacteriol. 191:5569-5576. http://dx.doi.org/10.1128/JB.00408-09.
26. Chirakkal H, O'Rourke M, Atrih A, Foster SJ, Moir A. 2002. Analysis of spore cortex lytic enzymes and related proteins in Bacillus subtilis endospore germination. Microbiology 148:2383-2392.
27. 2+- dipicolinate. J. Bacteriol. 183:4886-4893. http://dx.doi.org/10.1128/JB .183.16.4886-4893.2001.
28. Moriyama R, Hattori A, Miyata S, Kudoh S, Makino S. 1996. A gene (sleB) encoding a spore cortex-lytic enzyme from Bacillus subtilis and response of the enzyme to L-alanine-mediated germination. J. Bacteriol. 178:6059-6063.
29. Setlow B, Peng L, Loshon CA, Li YQ, Christie G, Setlow P. 2009. Characterization of the germination of Bacillus megaterium spores lacking enzymes that degrade the spore cortex. J. Appl. Microbiol. 107:318-328. http://dx.doi.org/10.1111/j.1365-2672.2009.04210.x.
30. Moriyama R, Fukuoka H, Miyata S, Kudoh S, Hattori A, Kozuka S, Yasuda Y, Tochikubo K, Makino S. 1999. Expression of a germinationspecific amidase, SleB, of bacilli in the forespore compartment of sporulating cells and its localization on the exterior side of the cortex in dormant spores. J. Bacteriol. 181:2373-2378.
31. Christie G, U¨stok FI, Lu Q, Packman LC, Lowe CR. 2010. Mutational analysis of Bacillus megaterium QM B1551 cortex-lytic enzymes. J. Bacteriol. 192:5378-5389. http://dx.doi.org/10.1128/JB.00830-10.
32. Popham DL, Heffron JD, Lambert EA. 2012. Degradation of spore peptidoglycan during germination, p 121-142. In Abel-Santos E (ed), Bacterial spores: current research and applications. Caister Academic Press, Norwich, United Kingdom.
33. Moriyama R, Kudoh S, Miyata S, Nonobe S, Hattori A, Makino S. 1996. A germination-specific spore cortex-lytic enzyme from Bacillus cereus spores: cloning and sequencing of the gene and molecular characterization of the enzyme. J. Bacteriol. 178:5330-5332.
34. Boland FM, Atrih A, Chirakkal H, Foster SJ, Moir A. 2000. Complete spore-cortex hydrolysis during germination of Bacillus subtilis 168 requires SleB and YpeB. Microbiology 146:57-64.
35. Hu K, Yang H, Liu G, Tan H. 2007. Cloning and identification of a gene encoding spore cortex-lytic enzyme in Bacillus thuringiensis. Curr. Microbiol. 54:292-295. http://dx.doi.org/10.1007/s00284-006-0430-x.
36. Li Y, Butzin XY, Davis A, Setlow B, Korza G, U¨stok FI, Christie G, Setlow P, Hao B. 2013. Activity and regulation of various forms of CwlJ, SleB, and YpeB proteins in degrading cortex peptidoglycan of spores of Bacillus species in vitro and during spore germination. J. Bacteriol. 195: 2530-2540. http://dx.doi.org/10.1128/JB.00259-13.
37. Masayama A, Fukuoka H, Kato S, Yoshimura T, Moriyama M, Moriyama R. 2006. Subcellular localization of a germination-specific cortex- lytic enzyme, SleB, of bacilli during sporulation. Genes Genet. Syst. 81:163-169. http://dx.doi.org/10.1266/ggs.81.163.
38. Li Y, Jin K, Setlow B, Setlow P, Hao B. 2012. Crystal structure of the catalytic domain of the Bacillus cereus SleB protein, important in cortex peptidoglycan degradation during spore germination. J. Bacteriol. 194: 4537-4545. http://dx.doi.org/10.1128/JB.00877-12.
39. Jing X, Robinson HR, Heffron JD, Popham DL, Schubot FD. 2012. The catalytic domain of the germination-specific lytic transglycosylase SleB from Bacillus anthracis displays a unique active site topology. Proteins 80:2469-2475. http://dx.doi.org/10.1002/prot.24140.
40. Yeats C, Rawlings ND, Bateman A. 2004. The PepSY domain: a regulator of peptidase activity in the microbial environment? Trends Biochem. Sci. 29:169-172. http://dx.doi.org/10.1016/j.tibs.2004.02.004.
41. Janes BK, Stibitz S. 2006. Routine markerless gene replacement in Bacillus anthracis. Infect. Immun. 74:1949-1953. http://dx.doi.org/10.1128 /IAI.74.3.1949-1953.2006.
42. Hunter S, Jones P, Mitchell A, Apweiler R, Attwood TK, Bateman A, Bernard T, Binns D, Bork P, Burge S, de Castro E, Coggill P, Corbett M, Das U, Daugherty L, Duquenne L, Finn RD, Fraser M, Gough J, Haft D, Hulo N, Kahn D, Kelly E, Letunic I, Lonsdale D, Lopez R, Madera M, Maslen J, McAnulla C, McDowall J, McMenamin C, Mi H, Mutowo-Muellenet P, Mulder N, Natale D, Orengo C, Pesseat S, Punta M, Quinn AF, Rivoire C, Sangrador-Vegas A, Selengut JD, Sigrist CJ, Scheremetjew M, Tate J, Thimmajanarthanan M, Thomas PD, Wu CH, Yeats C, Yong SY. 2012. InterPro in 2011: new developments in the family and domain prediction database. Nucleic Acids Res. 40:D306-D312. http: //dx.doi.org/10.1093/nar/gkr948.
43. Ho SN, Hunt HD, Horton RM, Pullen JK, Pease LR. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59. http://dx.doi.org/10.1016/0378-1119(89)90358-2.
44. van den Ent F, Lo¨we J. 2006. RF cloning: a restriction-free method for inserting target genes into plasmids. J. Biochem. Biophys. Methods 67:67- 74. http://dx.doi.org/10.1016/j.jbbm.2005.12.008.
45. Das D, Finn RD, Carlton D, Miller MD, Abdubek P, Astakhova T, Axelrod HL, Bakolitsa C, Chen C, Chiu HJ, Chiu M, Clayton T, Deller MC, Duan L, Ellrott K, Ernst D, Farr CL, Feuerhelm J, Grant JC, Grzechnik A, Han GW, Jaroszewski L, Jin KK, Klock HE, Knuth MW, Kozbial P, Krishna SS, Kumar A, Marciano D, McMullan D, Morse AT, Nigoghossian E, Nopakun A, Okach L, Puckett C, Reyes R, Rife CL, Sefcovic N, Tien HJ, Trame CB, van den Bedem H, Weekes D, Wooten T, Xu Q, Hodgson KO, Wooley J, Elsliger MA, Deacon AM, Godzik A, Lesley SA, Wilson IA. 2010. The structure of BVU2987 from Bacteroides vulgatus reveals a superfamily of bacterial periplasmic proteins with possible inhibitory function. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 66:1265-1273. http://dx .doi.org/10.1107/S1744309109046788.
46. Gao X, Wang J, Yu DQ, Bian F, Xie BB, Chen XL, Zhou BC, Lai LH, Wang ZX, Wu JW, Zhang YZ. 2010. Structural basis for the autoprocessing of zinc metalloproteases in the thermolysin family. Proc. Natl. Acad. Sci. U. S. A. 107:17569-17574. http://dx.doi.org/10.1073/pnas .1005681107.
47. Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignments through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680. http://dx.doi.org/10.1093/nar /22.22.4673.
48. Kim HU, Goepfert JM. 1974. A sporulation medium for Bacillus anthracis. J. Appl. Bacteriol. 37:265-267. http://dx.doi.org/10.1111/j.1365-2672 .1974.tb00438.x.
49. Nicholson WL, Setlow P. 1990. Sporulation, germination, and outgrowth, p 391-450. In Harwood CR, Cutting SM (ed), Molecular biological methods for Bacillus. John Wiley and Sons Ltd., Chichester, England.
50. Austin BP, Nallamsetty S, Waugh DS. 2009. Hexahistidine-tagged maltose- binding protein as a fusion partner for the production of soluble recombinant proteins in Escherichia coli. Methods Mol. Biol. 498:157-172. http://dx.doi.org/10.1007/978-1-59745-196-3_11.
51. Kapust RB, Tozser J, Fox JD, Anderson DE, Cherry S, Copeland TD, Waugh DS. 2001. Tobacco etch virus protease: mechanism of autolysis and rational design of stable mutants with wild-type catalytic proficiency. Protein Eng. 14:993-1000. http://dx.doi.org/10.1093/protein/14.12.993.
52. Kuwana R, Kasahara Y, Fujibayashi M, Takamatsu H, Ogasawara N, Watabe K. 2002. Proteomics characterization of novel spore proteins of Bacillus subtilis. Microbiology 148:3971-3982.
53. Bagyan I, Noback M, Bron S, Paidhungat M, Setlow P. 1998. Characterization of yhcN, a new forespore-specific gene of Bacillus subtilis. Gene 212:179-188. http://dx.doi.org/10.1016/S0378-1119(98)00172-3.
54. K processing in Bacillus subtilis. Genes Dev. 5:456-466. http://dx.doi.org/10.1101/gad.5.3.456.
55. K processing in Bacillus subtilis. Mol. Microbiol. 36:1336-1348. http://dx.doi.org /10.1046/j.1365-2958.2000.01946.x.
56. Fabret C, Hoch JA. 1998. A two-component signal transduction system essential for growth of Bacillus subtilis: implications for anti-infective therapy. J. Bacteriol. 180:6375-6383.