Publication Cover
Biofouling
The Journal of Bioadhesion and Biofilm Research
Volume 30, 2014 - Issue 7
297
Views
15
CrossRef citations to date
0
Altmetric
Articles

Presence and function of a thick mucous layer rich in polysaccharides around Bacillus subtilis spores

, , , , , & show all
Pages 845-858 | Received 24 Feb 2014, Accepted 21 Jun 2014, Published online: 04 Aug 2014

References

  • Ankolekar C, Labbe RG. 2010. Physical characteristics of spores of food-associated isolates of the Bacillus cereus group. Appl Environ Microbiol. 76:982–984.10.1128/AEM.02116-09
  • Atrih A, Zollner P, Allamier G, Foster SJ. 1996. Structural analysis of Bacillus subtilis 168 endospore peptidoglycan and its role during differentiation. J Bacteriol. 178:6173–6183.
  • Bailey CP, Vonholy A. 1993. Bacillus spore contamination associated with commercial bread manufacture. Food Microbiol. 10:287–294.10.1006/fmic.1993.1033
  • Bauer T, Little S, Stover AG, Driks A. 1999. Functional regions of the Bacillus subtilis spore coat morphogenetic protein CotE. J Bacteriol. 181:7043–7051.
  • Beaman TC, Pankratz HS, Gerhardt P. 1972. Ultrastructure of the exosporium and underlying inclusions in spores of Bacillus megaterium strains. J Bacteriol. 109:1198–1209.
  • Bos R, van des Mei HC, Busscher HJ. 1999. Physico-chemistry of initial microbial adhesive interactions. Its mechanism and methods for study. FEMS Microbiol Rev. 23:179–230.
  • Brown KL. 2000. Control of bacterial spores. Br Med Bull. 56:158–171.10.1258/0007142001902860
  • Buhr TL, McPherson DC, Gutting BW. 2008. Analysis of broth-cultured Bacillus atrophaeus and Bacillus cereus spores. J Appl Microbiol. 105:1604–1613.10.1111/jam.2008.105.issue-5
  • Carroll AM, Plomp M, Malkin AJ, Setlow P. 2008. Protozoal digestion of coat-defective Bacillus subtilis spores produces ‘rinds’ composed of insoluble coat protein. Appl Environ Microbiol. 74:5875–5881.10.1128/AEM.01228-08
  • De Jonghe V, Coorevits A, De Block J, Van Coillie E, Grijspeerdt K, Herman L, De Vos P, Heyndrickx M. 2010. Toxinogenic and spoilage potential of aerobic spore-formers isolated from raw milk. Int J Food Microbiol. 136:318–325.10.1016/j.ijfoodmicro.2009.11.007
  • Driks A. 1999. Bacillus subtilis spore coat. Microbiol Mol Biol Rev. 63:1–20.
  • Driks A. 2003. The dynamic spore. Proc Nat Acad Sci. USA. 100:3007–3009.10.1073/pnas.0730807100
  • Dufrenne J, Soentoro P, Tatini S, Day T, Notermans S. 1994. Characteristics of Bacillus cereus related to safe food production. Int J Food Microbiol. 23:99–109.10.1016/0168-1605(94)90225-9
  • Faille C, Jullien C, Fontaine F, Bellon-Fontaine MN, Slomianny C, Bénézech T. 2002. Adhesion of Bacillus spores and Escherichia coli cells to inert surfaces: role of surface hydrophobicity. Can J Microbiol. 48:728–738.10.1139/w02-063
  • Faille C, Lequette Y, Ronse A, Slomianny C, Garénaux E, Guerardel Y. 2010. Morphology and physico-chemical properties of Bacillus spores surrounded or not with an exosporium: consequences on their ability to adhere to stainless steel. Int J Food Microbiol. 143:125–135.10.1016/j.ijfoodmicro.2010.07.038
  • Faille C, Bénézech T, Blel W, Ronse A, Ronse G, Clarisse M, Slomianny C. 2013. Role of mechanical vs chemical action in the removal of adherent Bacillus spores during CIP procedures. Food Microbiol. 33:149–157.10.1016/j.fm.2012.09.010
  • Fox A, Stewart GC, Waller LN, Fox KF, Harley WM, Price RL. 2003. Carbohydrates and glycoproteins of Bacillus anthracis and related bacilli: targets for biodetection. J Microbiol Methods. 54:143–152.10.1016/S0167-7012(03)00095-2
  • Garcia-Patrone M, Tandecarz JS. 1995. A glycoprotein multimer from Bacillus thuringiensis sporangia: dissociation into subunits and sugar composition. Mol Cell Biochem. 145:29–37.10.1007/BF00925710
  • Gilmore ME, Bandyopadhyay D, Dean AM, Linnstaedt SD, Popham DL. 2004. Production of muramic δ-lactam in Bacillus subtilis spore peptidoglycan. J Bacteriol. 186:80–89.10.1128/JB.186.1.80-89.2004
  • Henriques AO, Moran CP. 2007. Structure, assembly, and function of the spore surface layers. Annu Rev Microbiol. 61:555–588.10.1146/annurev.micro.61.080706.093224
  • Henriques AO, Beall BW, Moran CP. 1997. CotM of Bacillus subtilis, a member of the alpha-crystallin family of stress proteins, is induced during development and participates in spore outer coat formation. J Bacteriol. 179:1887–1897.
  • Holt SC, Leadbetter ER. 1969. Comparative ultrastructure of selected aerobic spore-forming bacteria: a freeze-etching study. Bacteriol Rev. 33:346–378.
  • Hong HA, Khaneja R, Tam NMK, Cazzato A, Tan S, Urdaci M, Brisson A, Gasbarrini A, Barnes I, Cutting SM. 2009. Bacillus subtilis isolated from the human gastrointestinal tract. Res Microbiol. 160:134–143.10.1016/j.resmic.2008.11.002
  • Joshi LT, Phillips DS, Williams CF, Alyousef A, Baillie L. 2012. Contribution of spores to the ability of Clostridium difficile to adhere to surfaces. Appl Environ Microbiol. 78:7671–7679.10.1128/AEM.01862-12
  • Koshikawa T, Yamazaki M, Yoshimi M, Ogawa S, Yamada A, Watabe K, Torii M. 1989. Surface hydrophobicity of spores of Bacillus spp. J Gen Microbiol. 135:2717–2722.
  • Lequette Y, Garénaux E, Combrouse T, Lima Dias TD, Ronse A, Slomianny C, Trivelli X, Guerardel Y, Faille C. 2011a. Domains of BclA, the major surface glycoprotein of the B. cereus exosporium: glycosylation patterns and role in spore surface properties. Biofouling. 27:751–761.10.1080/08927014.2011.599842
  • Lequette Y, Garenaux E, Tauveron G, Dumez S, Perchat S, Slomianny C, Lereclus D, Guerardel Y, Faille C. 2011b. Role played by exosporium glycoproteins in the surface properties of Bacillus cereus spores and in their adhesion to stainless steel. Appl Environ Microbiol. 77:4905–4911.10.1128/AEM.02872-10
  • Lindsay D, Brozel VS, von Holy A. 2006. Biofilm-spore response in Bacillus cereus and Bacillus subtilis during nutrient limitation. J Food Prot. 69:1168–1172.
  • Lindsay D, Brözel VS, Mostert JF, von Holy A. 2000. Physiology of dairy-associated Bacillus spp. over a wide pH range. Int J Food Microbiol. 54:49–62.10.1016/S0168-1605(99)00178-6
  • Logan NA. 2012. Bacillus and relatives in foodborne illness. J Appl Microbiol. 112:417–429.10.1111/jam.2012.112.issue-3
  • Nanasaki Y, Hagiwara T, Watanabe H, Sakiyama T. 2010. Removability of bacterial spores made adherent to solid surfaces from suspension with and without drying. Food Control. 21:1472–1477.10.1016/j.foodcont.2010.04.016
  • Popham DL, Helin J, Costello CE, Setlow P. 1996. Muramic lactam in peptidoglycan of Bacillus subtilis spores is required for spores outgrowth but not for spore dehydration or heat resistance. Proc Nat Acad Sci. USA. 93:15405–15410.10.1073/pnas.93.26.15405
  • Reynolds ES. 1963. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol. 17:208–212.10.1083/jcb.17.1.208
  • Rönner U, Husmark U, Henriksson A. 1990. Adhesion of Bacillus spores in relation to hydrophobicity. J Appl Bacteriol. 69:550–556.10.1111/jam.1990.69.issue-4
  • Salkinoja-Salonen MS, Vuorio R, Andersson MA, Kampfer P, Andersson MC, Honkanen-Buzalski T, Scoging AC. 1999. Toxigenic strains of Bacillus licheniformis related to food poisoning. Appl Environ Microbiol. 65:4637–4645.
  • Shaheen R, Svensson B, Andersson MA, Christiansson A, Salkinoja-Salonen M. 2010. Persistence strategies of Bacillus cereus spores isolated from dairy silo tanks. Food Microbiol. 27:347–355.10.1016/j.fm.2009.11.004
  • Sharma M, Anand SK. 2002. Characterization of constitutive microflora of biofilms in dairy processing lines. Food Microbiol. 19:627–636.10.1006/fmic.2002.0472
  • Taylor JMW, Sutherland AD, Aidoo KE, Logan NA. 2005. Heat-stable toxin production by strains of Bacillus cereus, Bacillus firmus, Bacillus megaterium, Bacillus simplex and Bacillus licheniformis. FEMS Microbiol Lett. 242:313–317.10.1016/j.femsle.2004.11.022
  • te Giffel MC, Beumer RR, Leijendekkers S, Rombouts FM. 1996. Incidence of Bacillus cereus and Bacillus subtilis in foods in the Netherlands. Food Microbiol. 13:53–58.10.1006/fmic.1996.0007
  • Todd SJ, Moir AJ, Johnson MJ, Moir A. 2003. Genes of Bacillus cereus and Bacillus anthracis encoding proteins of the exosporium. J Bacteriol. 185:3373–3378.10.1128/JB.185.11.3373-3378.2003
  • Traag BA, Driks A, Stragier P, Bitter W, Broussard G, Hatfull G, Chu F, Adams KN, Ramakrishnan L, Losick R. 2010. Do mycobacteria produce endospores? Proc Nat Acad Sci. 107:878–881.10.1073/pnas.0911299107
  • Waller LN, Fox N, Fox KF, Fox A, Price RL. 2004. Ruthenium red staining for ultrastructural visualization of a glycoprotein layer surrounding the spore of Bacillus anthracis and Bacillus subtilis. J Microbiol Methods. 58:23–30.10.1016/j.mimet.2004.02.012
  • Warth AD, Strominger JL. 1969. Structure of the peptidoglycan of bacterial spores: occurrence of the lactam muramic acid. Proc Nat Acad Sci. 64:528–535.10.1073/pnas.64.2.528
  • Warth AD, Strominger JL. 1972. Structure of the peptidoglycan from spores of Bacillus subtilis. Biochem. 11:1389–1396.10.1021/bi00758a010
  • Whiton RS, Lau P, Morgan SL, Gilbart J, Fox A. 1985. Modifications in the alditol acetate method for analysis of muramic acid and other neutral and amino sugars by capillary gas chromatography – mass spectrometry with selected ion monitoring. J Chromatogr A. 347:109–120.10.1016/S0021-9673(01)95474-3
  • Wiencek KM, Klapes NA, Foegeding PM. 1990. Hydrophobicity of Bacillus and Clostridium spores. Appl Environ Microbiol. 56:2600–2605.
  • Wiencek KM, Klapes NA, Foegeding PM. 1991. Adhesion of Bacillus spores to inanimate materials: effects of substratum and spore hydrophobicity. Biofouling. 3:139–149.10.1080/08927019109378168
  • Wunschel D, Fox KF, Black GE, Fox A. 1994. Discimination among the B. cereus group, in comparison to B. subtilis, by structural carbohydrate profiles and ribosomal RNA spacer region PCR. Syst Appl Microbiol. 17:625–635.
  • Zaman MS, Goyal A, Dubey GP, Gupta PK, Chandra H, Das TK, Ganguli M, Singh Y. 2005. Imaging and analysis of Bacillus anthracis spore germination. Microsc Res Tech. 66:307–311.10.1002/(ISSN)1097-0029
  • Zheng LB, Donovan WP, Fitzjames PC, Losick R. 1988. Gene encoding a morphogenic protein required in the assembly of the outer coat of the Bacillus subtilis endospore. Gen Dev. 2:1047–1054.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.