Bacillus cereus Biofilms-same, only different

Frontiers in Microbiology

Volumn 7, Issue JUL, 2016, Pages

  Majed, Racha ^a,b   Faille, Christine ^c   Kallassy, Mireille ^b   Gohar, Michel ^a  

^a UNIVERSITÉ PARIS SACLAY   (France)

^b SAINT JOSEPH UNIVERSITY   (Lebanon)

^c UNIV LILLE   (France)

Author keywords

Anthracis; Bacillus; Biofilm; Cereus; Ecology; Food; Regulation; Thuringiensis

Indexed keywords

BACTERIOCIN; ENZYME; QUATERNARY AMMONIUM DERIVATIVE; SURFACTANT; TOXIN;

BACILLUS ANTHRACIS; BACILLUS CEREUS; BACILLUS SUBTILIS; BACILLUS THURINGIENSIS; BACTERIAL SPORE; BIOFILM; CELL HETEROGENEITY; CELL SURFACE; FLAGELLUM; FOOD INDUSTRY; FOOD SPOILAGE; METABOLITE; NONHUMAN; REGULATORY MECHANISM; REVIEW; SECRETION (PROCESS); SPOROGENESIS; STRESS;

EID: 84983063586     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.01054     Document Type: Review

References (150)

1. Abee, T., Kovács, A. T., Kuipers, O. P., and Van Der Veen, S. (2011). Biofilm formation and dispersal in Gram-positive bacteria. Curr. Opin. Biotechnol. 22, 172-179. doi: 10.1016/j.copbio.2010.10.016
2. Ahern, M., Verschueren, S., and Van Sinderen, D. (2003). Isolation and characterisation of a novel bacteriocin produced by Bacillus thuringiensis strain B439. FEMS Microbiol. Lett. 220, 127-131. doi: 10.1016/S0378-1097(03)00086-7
3. Andersson, A., Ronner, U., and Granum, P. E. (1995). What problems does the food industry have with the spore-forming pathogens Bacillus cereus and Clostridium perfringens? Int. J. Food Microbiol. 28, 145-155.
4. Anjum, R., and Krakat, N. (2016). Detection of multiple resistances, biofilm formation and conjugative transfer of Bacillus cereus from contaminated soils. Curr. Microbiol. 72, 321-328. doi: 10.1007/s00284-015-0952-1
5. Asally, M., Kittisopikul, M., Rue, P., Du, Y., Hu, Z., çagatay, T., et al. (2012). Localized cell death focuses mechanical forces during 3D patterning in a biofilm. Proc. Natl. Acad. Sci. U.S.A. 109, 18891-18896. doi: 10.1073/pnas.1212429109
6. Auger, S., Krin, E., Aymerich, S., and Gohar, M. (2006). Autoinducer 2 affects biofilm formation by Bacillus cereus. Appl. Environ. Microbiol. 72, 937-941. doi: 10.1128/AEM.72.1.937-941.2006
7. Auger, S., Ramarao, N., Faille, C., Fouet, A., Aymerich, S., and Gohar, M. (2009). Biofilm formation and cell surface properties among pathogenic and nonpathogenic strains of the Bacillus cereus group. Appl. Environ. Microbiol. 75, 6616-6618. doi: 10.1128/AEM.00155-09
8. Austin, J. W., and Bergeron, G. (1995). Development of bacterial biofilms in dairy processing lines. J. Dairy Res. 62, 509-519. doi: 10.1017/S0022029900031204
9. Bennett, S. D., Walsh, K. A., and Gould, L. H. (2013). Foodborne disease outbreaks caused by Bacillus cereus, Clostridium perfringens, and Staphylococcus aureus-United States, 1998-2008. Clin. Infect. Dis. 57, 425-433. doi: 10.1093/cid/cit244
10. Branda, S. S., Gonzalez-Pastor, J. E., Ben Yehuda, S., Losick, R., and Kolter, R. (2001). Fruiting body formation by Bacillus subtilis. Proc. Natl. Acad. Sci. U.S.A. 98, 11621-11626. doi: 10.1073/pnas.191384198
11. Bremer, P. J., Fillery, S., and Mcquillan, A. J. (2006). Laboratory scale Clean-In-Place (CIP) studies on the effectiveness of different caustic and acid wash steps on the removal of dairy biofilms. Int. J. Food Microbiol. 106, 254-262. doi: 10.1016/j.ijfoodmicro.2005.07.004
12. Bridier, A., Meylheuc, T., and Briandet, R. (2013). Realistic representation of Bacillus subtilis biofilms architecture using combined microscopy (CLSM, ESEM and FESEM). Micron 48, 65-69. doi: 10.1016/j.micron.2013.02.013
13. Brown, K. L. (2000). Control of bacterial spores. Br. Med. Bull. 56, 158-171. doi: 10.1258/0007142001902860
14. Cairns, L. S., Hobley, L., and Stanley-Wall, N. R. (2014). Biofilm formation by Bacillus subtilis: new insights into regulatory strategies and assembly mechanisms. Mol. Microbiol. 93, 587-598. doi: 10.1111/mmi.12697
15. Candela, T., Maes, E., Garénaux, E., Rombouts, Y., Krzewinski, F., Gohar, M., et al. (2011). Environmental and biofilm-dependent changes in a Bacillus cereus secondary cell wall polysaccharide. J. Biol. Chem. 286, 31250-31262. doi: 10.1074/jbc.M111.249821
16. Caro-Astorga, J., Pérez-García, A., De Vicente, A., and Romero, D. (2015). A genomic region involved in the formation of adhesin fibers in Bacillus cereus biofilms. Front. Microbiol. 5:745. doi: 10.3389/fmicb.2014.00745
17. Christison, C. A., Lindsay, D., and Von Holy, A. (2007). Cleaning and handling implements as potential reservoirs for bacterial contamination of some ready-to-eat foods in retail delicatessen environments. J. Food Prot. 70, 2878-2883.
18. Cook, L. C., and Dunny, G. M. (2014). The influence of biofilms in the biology of plasmids. Microbiol. Spectr. 2:0012. doi: 10.1128/microbiolspec.plas-0012-2013
19. Costerton, J. W., Lewandowski, Z., Caldwell, D. E., Korber, D. R., and Lappin-Scott, H. M. (1995). Microbial biofilms. Annu. Rev. Microbiol. 49, 711-745. doi: 10.1146/annurev.mi.49.100195.003431
20. Cutting, S. M. (2011). Bacillus probiotics. Food Microbiol. 28, 214-220. doi: 10.1016/j.fm.2010.03.007
21. Czechowski, M. H. (1990). Bacterial attachment to Buna-n gaskets in milk processing equipment. Aust. J. Dairy Technol. 45, 113-114.
22. Davey, M. E., and O'toole, G. A. (2000). Microbial biofilms: from ecology to molecular genetics. Microbiol. Mol. Biol. Rev. 64, 847-867. doi: 10.1128/MMBR.64.4.847-867.2000
23. De Been, M., Francke, C., Moezelaar, R., Abee, T., and Siezen, R. J. (2006). Comparative analysis of two-component signal transduction systems of Bacillus cereus, Bacillus thuringiensis and Bacillus anthracis. Microbiology 152, 3035-3048. doi: 10.1099/mic.0.29137-0
24. Dequeiroz, G. A., and Day, D. F. (2008). Disinfection of Bacillus subtilis spore-contaminated surface materials with a sodium hypochlorite and a hydrogen peroxide-based sanitizer. Lett. Appl. Microbiol. 46, 176-180. doi: 10.1111/j.1472-765X.2007.02283.x
25. De Vries, Y. P., Van Der Voort, M., Wijman, J., Van Schaik, W., Hornstra, L. M., De Vos, W. M., et al. (2004). Progress in food-related research focussing on Bacillus cereus. Microbes Environ. 19, 265-269. doi: 10.1264/jsme2.19.265
26. Duanis-Assaf, D., Steinberg, D., Chai, Y., and Shemesh, M. (2015). The LuxS based quorum sensing governs lactose induced biofilm formation by Bacillus subtilis. Front. Microbiol. 6:1517. doi: 10.3389/fmicb.2015.01517
27. Dubois, T., Faegri, K., Perchat, S., Lemy, C., Buisson, C., Nielsen-Leroux, C., et al. (2012). Necrotrophism is a quorum-sensing-regulated lifestyle in Bacillus thuringiensis. PLoS Pathog. 8:e1002629. doi: 10.1371/journal.ppat.1002629
28. Dubois, T., Perchat, S., Verplaetse, E., Gominet, M., Lemy, C., Aumont-Nicaise, M., et al. (2013). Activity of the Bacillus thuringiensis NprR-NprX cell-cell communication system is co-ordinated to the physiological stage through a complex transcriptional regulation. Mol. Microbiol. 88, 48-63. doi: 10.1111/mmi.12168
29. Ehling-Schulz, M., Frenzel, E., and Gohar, M. (2015). Food-bacteria interplay: pathometabolism of emetic Bacillus cereus. Front. Microbiol. 6:704. doi: 10.3389/fmicb.2015.00704
30. Ekman, J. V., Kruglov, A., Andersson, M. A., Mikkola, R., Raulio, M., and Salkinoja-Salonen, M. (2012). Cereulide produced by Bacillus cereus increases the fitness of the producer organism in low-potassium environments. Microbiology 158, 1106-1116. doi: 10.1099/mic.0.053520-0
31. Elhariry, H. M. (2011). Attachment strength and biofilm forming ability of Bacillus cereus on green-leafy vegetables: cabbage and lettuce. Food Microbiol. 28, 1266-1274. doi: 10.1016/j.fm.2011.05.004
32. Evans, J. A., Russell, S. L., James, C., and Corry, J. E. L. (2004). Microbial contamination of food refrigeration equipment. J. Food Eng. 62, 225-232. doi: 10.1016/S0260-8774(03)00235-8
33. Fagerlund, A., Dubois, T., Økstad, O. A., Verplaetse, E., Gilois, N., Bennaceur, I., et al. (2014). SinR controls enterotoxin expression in Bacillus thuringiensis biofilms. PLoS ONE 9:e87532. doi: 10.1371/journal.pone.0087532
34. Faille, C., Benezech, T., Blel, W., Ronse, A., Ronse, G., Clarisse, M., et al. (2013). Role of mechanical vs. chemical action in the removal of adherent Bacillus spores during CIP procedures. Food Microbiol. 33, 149-157. doi: 10.1016/j.fm.2012.09.010
35. Faille, C., Benezech, T., Midelet-Bourdin, G., Lequette, Y., Clarisse, M., Ronse, G., et al. (2014). Sporulation of Bacillus spp. within biofilms: a potential source of contamination in food processing environments. Food Microbiol. 40, 64-74. doi: 10.1016/j.fm.2013.12.004
36. Faille, C., Bihi, L., Ronse, G., Baudoin, M., and Zoueshtiagh, F. (2016). Increased resistance to detachment of adherent microspheres and Bacillus spores subjected to a drying step. Colloids Surf. B Biointerfaces 143, 293-300. doi: 10.1016/j.colsurfb.2016.03.041
37. Faille, C., Fontaine, F., and Benezech, T. (2001). Potential occurrence of adhering living Bacillus spores in milk product processing lines. J. Appl. Microbiol. 90, 892-900. doi: 10.1046/j.1365-2672.2001.01321.x
38. Fasanella, A., Scasciamacchia, S., Garofolo, G., Giangaspero, A., Tarsitano, E., and Adone, R. (2010). Evaluation of the house fly Musca domestica as a mechanical vector for an anthrax. PLoS ONE 5:e12219. doi: 10.1371/journal.pone.0012219
39. Flach, J., Grzybowski, V., Toniazzo, G., and Corcao, G. (2014). Adhesion and production of degrading enzymes by bacteria isolated from biofilms in raw milk cooling tanks. Food Sci. Technol. 34, 571-576. doi: 10.1590/1678-457x.6374
40. Flemming, H. C., and Wingender, J. (2010). The biofilm matrix. Nat. Rev. Microbiol. 8, 623-633. doi: 10.1038/nrmicro2415
41. Flint, S. H., Bremer, P. J., and Brooks, J. D. (1997). Biofilms in dairy manufacturing plant - Description, current concerns and methods of control. Biofouling 11, 81-97. doi: 10.1080/08927019709378321
42. Frenzel, E., Doll, V., Pauthner, M., Lucking, G., Scherer, S., and Ehling-Schulz, M. (2012). CodY orchestrates the expression of virulence determinants in emetic Bacillus cereus by impacting key regulatory circuits. Mol. Microbiol. 85, 67-88. doi: 10.1111/j.1365-2958.2012.08090.x
43. Fromm, H. I., and Boor, K. J. (2004). Characterization of pasteurized fluid milk shelf-life attributes. J. Food Sci. 69, M207-M214. doi: 10.1111/j.1365-2621.2004.tb09889.x
44. Gao, T., Foulston, L., Chai, Y., Wang, Q., and Losick, R. (2015). Alternative modes of biofilm formation by plant-associated Bacillus cereus. Microbiologyopen 4, 452-464. doi: 10.1002/mbo3.251
45. Gélis-Jeanvoine, S., Canette, A., Gohar, M., Gominet, M., Slamti, L., and Lereclus, D. (2016). Genetic and functional analyses of kurstakin, a lipopeptide produced by Bacillus thuringiensis. Res. Microbiol. doi: 10.1016/j.resmic.2016.06.002. [Epub ahead of print].
46. Ghigo, J. M. (2001). Natural conjugative plasmids induce bacterial biofilm development. Nature 412, 442-445. doi: 10.1038/35086581
47. Gillis, A., and Mahillon, J. (2014). Influence of lysogeny of Tectiviruses GIL01 and GIL16 on Bacillus thuringiensis growth, biofilm formation, and swarming motility. Appl. Environ. Microbiol. 80, 7620-7630. doi: 10.1128/AEM.01869-14
48. Gohar, M., Faegri, K., Perchat, S., Ravnum, S., Okstad, O. A., Gominet, M., et al. (2008). The PlcR virulence regulon of Bacillus cereus. PLoS ONE 3:e2793. doi: 10.1371/journal.pone.0002793
49. Gohar, M., Økstad, O. A., Gilois, N., Sanchis, V., Kolsto, A. B., and Lereclus, D. (2002). Two-dimensional electrophoresis analysis of the extracellular proteome of Bacillus cereus reveals the importance of the PlcR regulon. Proteomics 2, 784-791. doi: 10.1002/1615-9861(200206)2:6<784::AID-PROT784>3.0.CO;2-R
50. Gunduz, G. T., and Tuncel, G. (2006). Biofilm formation in an ice cream plant. Antonie Van Leeuwenhoek 89, 329-336. doi: 10.1007/s10482-005-9035-9
51. Hamon, M. A., and Lazazzera, B. A. (2001). The sporulation transcription factor Spo0A is required for biofilm development in Bacillus subtilis. Mol. Microbiol. 42, 1199-1210. doi: 10.1046/j.1365-2958.2001.02709.x
52. Hayrapetyan, H., Abee, T., and Nierop Groot, M. (2016). Sporulation dynamics and spore heat resistance in wet and dry biofilms of Bacillus cereus. Food Control 60, 493-499. doi: 10.1016/j.foodcont.2015.08.027
53. Hayrapetyan, H., Muller, L., Tempelaars, M., Abee, T., and Nierop Groot, M. (2015a). Comparative analysis of biofilm formation by Bacillus cereus reference strains and undomesticated food isolates and the effect of free iron. Int. J. Food Microbiol. 200, 72-79. doi: 10.1016/j.ijfoodmicro.2015.02.005
54. Hayrapetyan, H., Tempelaars, M., Nierop Groot, M., and Abee, T. (2015b). Bacillus cereus ATCC 14579 RpoN (Sigma 54) Is a pleiotropic regulator of growth, carbohydrate metabolism, motility, biofilm formation and toxin production. PLoS ONE 10:e0134872. doi: 10.1371/journal.pone.0134872
55. Helgason, E., Tourasse, N. J., Meisal, R., Caugant, D. A., and Kolsto, A. B. (2004). Multilocus sequence typing scheme for bacteria of the Bacillus cereus group. Appl. Environ. Microbiol 70, 191-201. doi: 10.1128/AEM.70.1.191-201.2004
56. Hendriksen, N. B., and Carstensen, J. (2013). Long-term survival of Bacillus thuringiensis subsp. kurstaki in a field trial. Can. J. Microbiol. 59, 34-38. doi: 10.1139/cjm-2012-0380
57. Hendriksen, N. B., and Hansen, B. M. (2002). Long-term survival and germination of Bacillus thuringiensis var. kurstaki in a field trial. Can. J. Microbiol. 48, 256-261. doi: 10.1139/w02-009
58. Hobley, L., Ostrowski, A., Rao, F. V., Bromley, K. M., Porter, M., Prescott, A. R., et al. (2013). BslA is a self-assembling bacterial hydrophobin that coats the Bacillus subtilis biofilm. Proc. Natl. Acad. Sci. U.S.A. 110, 13600-13605. doi: 10.1073/pnas.1306390110
59. Houry, A., Briandet, R., Aymerich, S., and Gohar, M. (2010). Involvement of motility and flagella in Bacillus cereus biofilm formation. Microbiology 156, 1009-1018. doi: 10.1099/mic.0.034827-0
60. Houry, A., Gohar, M., Deschamps, J., Tischenko, E., Aymerich, S., Gruss, A., et al. (2012). Bacterial swimmers that infiltrate and take over the biofilm matrix. Proc. Natl. Acad. Sci. U.S.A. 109, 13088-13093. doi: 10.1073/pnas.1200791109
61. Hsueh, Y. H., Somers, E. B., Lereclus, D., and Wong, A. C. (2006). Biofilm formation by Bacillus cereus is influenced by PlcR, a pleiotropic regulator. Appl. Environ. Microbiol. 72, 5089-5092. doi: 10.1128/AEM.00573-06
62. Hsueh, Y. H., Somers, E. B., and Wong, A. C. (2008). Characterization of the codY gene and its influence on biofilm formation in Bacillus cereus. Arch. Microbiol. 189, 557-568. doi: 10.1007/s00203-008-0348-8
63. Hu, J. Y., Fan, Y., Lin, Y. H., Zhang, H. B., Ong, S. L., Dong, N., et al. (2003). Microbial diversity and prevalence of virulent pathogens in biofilms developed in a water reclamation system. Res. Microbiol 154, 623-629. doi: 10.1016/j.resmic.2003.09.004
64. Irnov, I., and Winkler, W. C. (2010). A regulatory RNA required for antitermination of biofilm and capsular polysaccharide operons in Bacillales. Mol. Microbiol. 76, 559-575. doi: 10.1111/j.1365-2958.2010.07131.x
65. Ivanova, N., Sorokin, A., Anderson, I., Galleron, N., Candelon, B., Kapatral, V., et al. (2003). Genome sequence of Bacillus cereus and comparative analysis with Bacillus anthracis. Nature 423, 87-91. doi: 10.1038/nature01582
66. Izano, E. A., Sadovskaya, I., Wang, H., Vinogradov, E., Ragunath, C., Ramasubbu, N., et al. (2008). Poly-N-acetylglucosamine mediates biofilm formation and detergent resistance in Aggregatibacter actinomycetemcomitans. Microb. Pathog. 44, 52-60. doi: 10.1016/j.micpath.2007.08.004
67. Jensen, G. B., Hansen, B. M., Eilenberg, J., and Mahillon, J. (2003). The hidden lifestyles of Bacillus cereus and relatives. Environ. Microbiol. 5, 631-640. doi: 10.1046/j.1462-2920.2003.00461.x
68. Kamar, R., Gohar, M., Jéhanno, I., Rejasse, A., Kallassy, M., Lereclus, D., et al. (2013). Pathogenic potential of Bacillus cereus strains as revealed by phenotypic analysis. J. Clin. Microbiol. 51, 320-323. doi: 10.1128/JCM.02848-12
69. Karunakaran, E., and Biggs, C. A. (2011). Mechanisms of Bacillus cereus biofilm formation: an investigation of the physicochemical characteristics of cell surfaces and extracellular proteins. Appl. Microbiol. Biotechnol. 89, 1161-1175. doi: 10.1007/s00253-010-2919-2
70. Kearns, D. B., Chu, F., Branda, S. S., Kolter, R., and Losick, R. (2005). A master regulator for biofilm formation by Bacillus subtilis. Mol. Microbiol. 55, 739-749. doi: 10.1111/j.1365-2958.2004.04440.x
71. Kobayashi, K. (2007a). Bacillus subtilis pellicle formation proceeds through genetically defined morphological changes. J. Bacteriol. 189, 4920-4931. doi: 10.1128/JB.00157-07
72. Kobayashi, K. (2007b). Gradual activation of the response regulator DegU controls serial expression of genes for flagellum formation and biofilm formation in Bacillus subtilis molecular Microbiology 66, 395-409. doi: 10.1111/j.1365-2958.2007.05923.x
73. Kolari, M., Nuutinen, J., Rainey, F. A., and Salkinoja-Salonen, M. S. (2003). Colored moderately thermophilic bacteria in paper-machine biofilms. J. Ind. Microbiol. Biotechnol. 30, 225-238. doi: 10.1007/s10295-003-0047-z
74. Kolari, M., Nuutinen, J., and Salkinoja-Salonen, M. S. (2001). Mechanisms of biofilm formation in paper machine by Bacillus species: the role of Deinococcus geothermalis. J. Ind. Microbiol. Biotechnol. 27, 343-351. doi: 10.1038/sj.jim.7000201
75. Kolenbrander, P. E., Palmer, R. J. Jr., Rickard, A. H., Jakubovics, N. S., Chalmers, N. I., and Diaz, P. I. (2006). Bacterial interactions and successions during plaque development. Periodontol. 2000. 42, 47-79. doi: 10.1111/j.1600-0757.2006.00187.x
76. Kreske, A. C., Ryu, J. H., and Beuchat, L. R. (2006a). Evaluation of chlorine, chlorine dioxide, and a peroxyacetic acid-based sanitizer for effectiveness in killing Bacillus cereus and Bacillus thuringiensis spores in suspensions, on the surface of stainless steel, and on apples. J. Food Prot. 69, 1892-1903.
77. Kreske, A. C., Ryu, J. H., Pettigrew, C. A., and Beuchat, L. R. (2006b). Lethality of chlorine, chlorine dioxide, and a commercial produce sanitizer to Bacillus cereus and Pseudomonas in a liquid detergent, on stainless steel, and in biofilm. J. Food Prot. 69, 2621-2634.
78. Kumari, S., and Sarkar, P. K. (2014). In vitro model study for biofilm formation by Bacillus cereus in dairy chilling tanks and optimization of clean-in-place (CIP) regimes using response surface methodology. Food Control 36, 153-158. doi: 10.1016/j.foodcont.2013.08.014
79. Kuroki, R., Kawakami, K., Qin, L., Kaji, C., Watanabe, K., Kimura, Y., et al. (2009). Nosocomial bacteremia caused by biofilm-forming Bacillus cereus and Bacillus thuringiensis. Intern. Med. 48, 791-796. doi: 10.2169/internalmedicine.48.1885
80. Lakshmanan, V., Kitto, S. L., Caplan, J. L., Hsueh, Y. H., Kearns, D. B., Wu, Y. S., et al. (2012). Microbe-associated molecular patterns-triggered root responses mediate beneficial rhizobacterial recruitment in Arabidopsis. Plant Physiol. 160, 1642-1661. doi: 10.1104/pp.112.200386
81. Langsrud, S., Baardsen, B., and Sundheim, G. (2000). Potentiation of the lethal effect of peroxygen on Bacillus cereus spores by alkali and enzyme wash. Int. J. Food Microbiol. 56, 81-86. doi: 10.1016/S0168-1605(00)00221-X
82. Lecomte, J., St-Arnaud, M., and Hijri, M. (2011). Isolation and identification of soil bacteria growing at the expense of arbuscular mycorrhizal fungi. FEMS Microbiol. Lett. 317, 43-51. doi: 10.1111/j.1574-6968.2011.02209.x
83. Lee, K., Costerton, J. W., Ravel, J., Auerbach, R. K., Wagner, D. M., Keim, P., et al. (2007). Phenotypic and functional characterization of Bacillus anthracis biofilms. Microbiology 153, 1693-1701. doi: 10.1099/mic.0.2006/003376-0
84. Lemon, K. P., Earl, A. M., Vlamakis, H. C., Aguilar, C., and Kolter, R. (2008). Biofilm development with an emphasis on Bacillus subtilis Curr. Top. Microbiol. Immunol. 322, 1-16. doi: 10.1007/978-3-540-75418-3_1
85. Lemos, M., Mergulhão, F., Melo, L., and Simões, M. (2015). The effect of shear stress on the formation and removal of Bacillus cereus biofilms. Food Bioproducts Process. 93, 242-248. doi: 10.1016/j.fbp.2014.09.005
86. Lequette, Y., Boels, G., Clarisse, M., and Faille, C. (2010). Using enzymes to remove biofilms of bacterial isolates sampled in the food-industry. Biofouling 26, 421-431. doi: 10.1080/08927011003699535
87. Lindback, T., Mols, M., Basset, C., Granum, P. E., Kuipers, O. P., and Kovacs, A. T. (2012). CodY, a pleiotropic regulator, influences multicellular behaviour and efficient production of virulence factors in Bacillus cereus. Environ. Microbiol. 14, 2233-2246. doi: 10.1111/j.1462-2920.2012.02766.x
88. Lindsay, D., Brözel, V. S., Mostert, J. F., and Von Holy, A. (2002). Differential efficacy of a chlorine dioxide-containing sanitizer against single species and binary biofilms of a dairy-associated Bacillus cereus and a Pseudomonas fluorescens isolate. J. Appl. Microbiol. 92, 352-361. doi: 10.1046/j.1365-2672.2002.01538.x
89. Marchand, S., De Block, J., De Jonghe, V., Coorevits, A., Heyndrickx, M., and Herman, L. (2012). Biofilm formation in milk production and processing environments; influence on milk quality and safety. Compr. Rev. Food Sci. Food Saf. 11, 133-147. doi: 10.1111/j.1541-4337.2011.00183.x
90. Margulis, L., Jorgensen, J. Z., Dolan, S., Kolchinsky, R., Rainey, F. A., and Lo, S. C. (1998). The Arthromitus stage of Bacillus cereus: intestinal symbionts of animals. Proc. Natl. Acad. Sci. U.S.A. 95, 1236-1241. doi: 10.1073/pnas.95.3.1236
91. Mattila, T., Manninen, M., and Kyläsiurola, A. L. (1990). Effect of cleaning-in-place disinfectants on wild bacterial strains isolated from a milking line. J. Dairy Res. 57, 33-39. doi: 10.1017/S0022029900026583
92. Meer, R. R., Baker, J., Bodyfelt, F. W., and Griffiths, M. W. (1991). Psychrotrophic Bacillus Spp. in fluid milk-products - a review. J. Food Prot. 54, 969-979.
93. Mettler, E., and Carpentier, B. (1997). Location, enumeration and identification of the microbial contamination after cleaning of EPDM gaskets introduced into a milk pasteurization line. Lait 77, 489-503. doi: 10.1051/lait:1997435
94. Moscoso, M., García, E., and López, R. (2006). Biofilm formation by Streptococcus pneumoniae: role of choline, extracellular DNA, and capsular polysaccharide in microbial accretion. J. Bacteriol. 188, 7785-7795. doi: 10.1128/JB.00673-06
95. Nanasaki, Y., Hagiwara, T., Watanabe, H., and Sakiyama, T. (2010). Removability of bacterial spores made adherent to solid surfaces from suspension with and without drying. Food Control 21, 1472-1477. doi: 10.1016/j.foodcont.2010.04.016
96. Ohsaki, Y., Koyano, S., Tachibana, M., Shibukawa, K., Kuroki, M., Yoshida, I., et al. (2007). Undetected Bacillus pseudo-outbreak after renovation work in a teaching hospital. J. Infect. 54, 617-622. doi: 10.1016/j.jinf.2006.10.049
97. Oscáriz, J. C., Cintas, L., Holo, H., Lasa, I., Nes, I. F., and Pisabarro, A. G. (2006). Purification and sequencing of cerein 7B, a novel bacteriocin produced by Bacillus cereus Bc7. FEMS Microbiol. Lett. 254, 108-115. doi: 10.1111/j.1574-6968.2005.00009.x
98. Parkar, S. G., Flint, S. H., and Brooks, J. D. (2004). Evaluation of the effect of cleaning regimes on biofilms of thermophilic bacilli on stainless steel. J. Appl. Microbiol. 96, 110-116. doi: 10.1046/j.1365-2672.2003.02136.x
99. Peng, J. S., Tsai, W. C., and Chou, C. C. (2002). Inactivation and removal of Bacillus cereus by sanitizer and detergent. Int. J. Food Microbiol. 77, 11-18. doi: 10.1016/S0168-1605(02)00060-0
100. Pflughoeft, K. J., Sumby, P., and Koehler, T. M. (2011). Bacillus anthracis sin locus and regulation of secreted proteases. J. Bacteriol. 193, 631-639. doi: 10.1128/JB.01083-10
101. Rajkovic, A., Uyttendaele, M., Dierick, K., Samapundo, S., Botteldoorn, N., Mahillon, J., et al. (2008). Risk Profile of the Bacillus cereus Group Implicated in Food Poisoning. Report for the Superior Health Council Belgium.
102. Rasko, D. A., Altherr, M. R., Han, C. S., and Ravel, J. (2005). Genomics of the Bacillus cereus group of organisms. FEMS Microbiol. Rev. 29, 303-329. doi: 10.1016/j.femsre.2004.12.005
103. Rasko, D. A., Rosovitz, M. J., Okstad, O. A., Fouts, D. E., Jiang, L., Cer, R. Z., et al. (2007). Complete sequence analysis of novel plasmids from emetic and periodontal Bacillus cereus isolates reveals a common evolutionary history among the B. cereus -group plasmids, including Bacillus anthracis pXO1. J. Bacteriol. 189, 52-64. doi: 10.1128/JB.01313-06
104. Ratto, M., Suihko, M. L., and Siika-Aho, M. (2005). Polysaccharide-producing bacteria isolated from paper machine slime deposits. J. Ind. Microbiol. Biotechnol. 32, 109-114. doi: 10.1007/s10295-005-0210-9
105. Reyes-Ramirez, A., and Ibarra, J. E. (2008). Plasmid patterns of Bacillus thuringiensis type strains. Appl. Environ. Microbiol. 74, 125-129. doi: 10.1128/AEM.02133-07
106. Risoen, P. A., Ronning, P., Hegna, I. K., and Kolsto, A. B. (2004). Characterization of a broad range antimicrobial substance from Bacillus cereus J. Appl. Microbiol. 96, 648-655. doi: 10.1046/j.1365-2672.2003.02139.x
107. Romero, D., Vlamakis, H., Losick, R., and Kolter, R. (2011). An accessory protein required for anchoring and assembly of amyloid fibres in B. subtilis biofilms. Mol. Microbiol. 80, 1155-1168. doi: 10.1111/j.1365-2958.2011.07653.x
108. Ruan, L., Crickmore, N., Peng, D., and Sun, M. (2015). Are nematodes a missing link in the confounded ecology of the entomopathogen Bacillus thuringiensis? Trends Microbiol. 23, 341-346. doi: 10.1016/j.tim.2015.02.011
109. Ryu, J. H., and Beuchat, L. R. (2005). Biofilm formation and sporulation by Bacillus cereus on a stainless steel surface and subsequent resistance of vegetative cells and spores to chlorine, chlorine dioxide, and a peroxyacetic acid-based sanitizer. J. Food Prot. 68, 2614-2622.
110. Sagripanti, J. L., and Bonifacino, A. (1999). Bacterial spores survive treatment with commercial sterilants and disinfectants. Appl. Environ. Microbiol. 65, 4255-4260.
111. Saile, E., and Koehler, T. M. (2006). Bacillus anthracis multiplication, persistence, and genetic exchange in the rhizosphere of grass plants. Appl. Environ. Microbiol. 72, 3168-3174. doi: 10.1128/AEM.72.5.3168-3174.2006
112. Salustiano, V. C., Andrade, N. J., Soares, N. F. F., Lima, J. C., Bernardes, P. C., Luiz, L. M. P., et al. (2009). Contamination of milk with Bacillus cereus by post-pasteurization surface exposure as evaluated by automated ribotyping. Food Control 20, 439-442. doi: 10.1016/j.foodcont.2008.07.004
113. Samarzija, D., Zamberlin, S., and Pogacic, T. (2012). Psychrotrophic bacteria and their negative effects on milk and dairy products quality. Mljekarstvo 62, 77-95.
114. Schuch, R., and Fischetti, V. A. (2009). The secret life of the anthrax agent Bacillus anthracis: bacteriophage-mediated ecological adaptations. PLoS ONE 4:e6532. doi: 10.1371/journal.pone.0006532
115. Schulte, R. D., Makus, C., Hasert, B., Michiels, N. K., and Schulenburg, H. (2010). Multiple reciprocal adaptations and rapid genetic change upon experimental coevolution of an animal host and its microbial parasite. Proc. Natl. Acad. Sci. U.S.A. 107, 7359-7364. doi: 10.1073/pnas.1003113107
116. Scott, S. A., Brooks, J. D., Rakonjac, J., Walker, K. M. R., and Flint, S. H. (2007). The formation of thermophilic spores during the manufacture of whole milk powder. Int. J. Dairy Technol. 60, 109-117. doi: 10.1111/j.1471-0307.2007.00309.x
117. Sharma, M., and Anand, S. K. (2002a). Bacterial biofilm on food contact surfaces: a review. J Food Sci. Techol. 39, 573-593. doi: 10.2478/v10222-011-0018-4
118. Sharma, M., and Anand, S. K. (2002b). Biofilms evaluation as an essential component of HACCP for food/dairy processing industry - a case. Food Control 13, 469-477. doi: 10.1016/S0956-7135(01)00068-8
119. Sharma, M., and Anand, S. K. (2002c). Characterization of constitutive microflora of biofilms in dairy processing lines. Food Microbiol. 19, 627-636. doi: 10.1006/fmic.2002.0472
120. Sidhu, M. S., Sorum, H., and Holck, A. (2002). Resistance to quaternary ammonium compounds in food-related bacteria. Microb. Drug Resist. 8, 393-399. doi: 10.1089/10766290260469679
121. Silo-Suh, L. A., Lethbridge, B. J., Raffel, S. J., He, H., Clardy, J., and Handelsman, J. (1994). Biological activities of two fungistatic antibiotics produced by Bacillus cereus UW85. Appl. Environ. Microbiol. 60, 2023-2030.
122. Simoes, M., Simoes, L. C., and Vieira, M. J. (2009). Species association increases biofilm resistance to chemical and mechanical treatments. Water Res. 43, 229-237. doi: 10.1016/j.watres.2008.10.010
123. Sissons, C. H., Wong, L., and Shu, M. (1998). Factors affecting the resting pH of in vitro human microcosm dental plaque and Streptococcus mutans biofilms. Arch. Oral Biol. 43, 93-102. doi: 10.1016/S0003-9969(97)00113-1
124. Slamti, L., Lemy, C., Henry, C., Guillot, A., Huillet, E., and Lereclus, D. (2015). CodY regulates the activity of the virulence quorum sensor plcr by controlling the import of the signaling peptide papr in Bacillus thuringiensis. Front. Microbiol. 6:1501. doi: 10.3389/fmicb.2015.01501
125. Sneath, P. H. A. (1986). "13 Endospore-forming gram-positive rods and cocci," in Bergey's Manual of Systematic Bacteriology, Vol. 2., eds J. G. Holt and P. H. A. Sneath (Baltimore, MD: William & Wilkins), 1599.P
126. Sonenshein, A. L. (2005). CodY, a global regulator of stationary phase and virulence in Gram-positive bacteria. Curr. Opin. Microbiol. 8, 203-207. doi: 10.1016/j.mib.2005.01.001
127. Stenfors Arnesen, L. P., Fagerlund, A., and Granum, P. E. (2008). From soil to gut: Bacillus cereus and its food poisoning toxins. FEMS Microbiol. Rev. 32, 579-606. doi: 10.1111/j.1574-6976.2008.00112.x
128. Storgards, E., Tapani, K., Hartwall, P., Saleva, R., and Suihko, M. L. (2006). Microbial attachment and biofilm formation in brewery bottling plants. J. Am. Soc. Brewing Chem. 64, 8-15. doi: 10.1094/ASBCJ-64-0008
129. Swiecicka, I., and Mahillon, J. (2006). Diversity of commensal Bacillus cereus sensu lato isolated from the common sow bug (Porcellio scaber, Isopoda). FEMS Microbiol. Ecol. 56, 132-140. doi: 10.1111/j.1574-6941.2006.00063.x
130. Tauveron, G., Slomianny, C., Henry, C., and Faille, C. (2006). Variability among Bacillus cereus strains in spore surface properties and influence on their ability to contaminate food surface equipment. Int. J. Food Microbiol. 110, 254-262. doi: 10.1016/j.ijfoodmicro.2006.04.027
131. Te Giffel, M. C., Beumer, R. R., Van Dam, W. F., Slaghuis, B. A., and Rombouts, F. M. (1995). Sporicidal effect of disinfectants on Bacillus cereus isolated from the milk processing environment. Int. Biodeterior. Biodegradation 36, 421-430. doi: 10.1016/0964-8305(95)00104-2
132. Toljander, J. F., Artursson, V., Paul, L. R., Jansson, J. K., and Finlay, R. D. (2006). Attachment of different soil bacteria to arbuscular mycorrhizal fungal extraradical hyphae is determined by hyphal vitality and fungal species. FEMS Microbiol. Lett. 254, 34-40. doi: 10.1111/j.1574-6968.2005.00003.x
133. Tran, S. L., Guillemet, E., Gohar, M., Lereclus, D., and Ramarao, N. (2010). CwpFM (EntFM) is a Bacillus cereus potential cell wall peptidase implicated in adhesion, biofilm formation, and virulence. J. Bacteriol. 192, 2638-2642. doi: 10.1128/JB.01315-09
134. Trejo, M., Douarche, C., Bailleux, V., Poulard, C., Mariot, S., Regeard, C., et al. (2013). Elasticity and wrinkled morphology of Bacillus subtilis pellicles. Proc. Natl. Acad. Sci. U.S.A. 110, 2011-2016. doi: 10.1073/pnas.1217178110
135. Turell, M. J., and Knudson, G. B. (1987). Mechanical transmission of Bacillus anthracis by stable flies (Stomoxys calcitrans) and mosquitoes (Aedes aegypti and Aedes taeniorhynchus). Infect. Immun. 55, 1859-1861.
136. Van Meervenne, E., De Weirdt, R., Van Coillie, E., Devlieghere, F., Herman, L., and Boon, N. (2014). Biofilm models for the food industry: hot spots for plasmid transfer? Pathog. Dis. 70, 332-338. doi: 10.1111/2049-632X.12134
137. Verplaetse, E., Slamti, L., Gohar, M., and Lereclus, D. (2015). Cell differentiation in a Bacillus thuringiensis population during planktonic growth, biofilm formation, and host infection. MBio 6, e00138-e00115. doi: 10.1128/mBio.00138-15
138. Verplaetse, E., Slamti, L., Gohar, M., and Lereclus, D. (2016). Two distinct pathways lead Bacillus thuringiensis to commit to sporulation in biofilm. Res. Microbiol. doi: 10.1016/j.resmic.2016.03.006. [Epub ahead of print].
139. Vilain, S., Luo, Y., Hildreth, M. B., and Brozel, V. S. (2006). Analysis of the life cycle of the soil saprophyte Bacillus cereus in liquid soil extract and in soil. Appl. Environ. Microbiol. 72, 4970-4977. doi: 10.1128/AEM.03076-05
140. Vilain, S., Pretorius, J. M., Theron, J., and Brozel, V. S. (2009). DNA as an adhesin: Bacillus cereus requires extracellular DNA to form biofilms. Appl. Environ. Microbiol. 75, 2861-2868. doi: 10.1128/AEM.01317-08
141. Vilas-Bôas, G., Sanchis, V., Lereclus, D., Lemos, M. V., and Bourguet, D. (2002). Genetic differentiation between sympatric populations of Bacillus cereus and Bacillus thuringiensis applied and environmental Microbiology 68, 1414-1424. doi: 10.1128/AEM.68.3.1414-1424.2002
142. Vilas-Boas, L. A., Vilas-Boas, G. F., Saridakis, H. O., Lemos, M. V., Lereclus, D., and Arantes, O. M. (2000). Survival and conjugation of Bacillus thuringiensis in a soil microcosm. FEMS Microbiol. Ecol. 31, 255-259. doi: 10.1016/S0168-6496(00)00002-7
143. Visotto, L. E., Oliveira, M. G., Ribon, A. O., Mares-Guia, T. R., and Guedes, R. N. (2009). Characterization and identification of proteolytic bacteria from the gut of the velvetbean caterpillar (Lepidoptera: Noctuidae). Environ. Entomol. 38, 1078-1085. doi: 10.1603/022.038.0415
144. Vlamakis, H., Aguilar, C., Losick, R., and Kolter, R. (2008). Control of cell fate by the formation of an architecturally complex bacterial community. Genes Dev. 22, 945-953. doi: 10.1101/gad.1645008
145. Vlamakis, H., Chai, Y., Beauregard, P., Losick, R., and Kolter, R. (2013). Sticking together: building a biofilm the Bacillus subtilis way. Nat. Rev. Microbiol. 11, 157-168. doi: 10.1038/nrmicro2960
146. Vlkova, H., Babak, V., Seydlova, R., Pavlik, I., and Schlegelova, I. (2008). Biofilms and hygiene on dairy farms and in the dairy industry: sanitation chemical products and their effectiveness on biofilms - a review. Czech. J. Food Sci. 26, 309-323.
147. Whitchurch, C. B., Tolker-Nielsen, T., Ragas, P. C., and Mattick, J. S. (2002). Extracellular DNA required for bacterial biofilm formation. Science 295:1487. doi: 10.1126/science.295.5559.1487
148. Wijman, J. G., De Leeuw, P. P., Moezelaar, R., Zwietering, M. H., and Abee, T. (2007). Air-liquid interface biofilms of Bacillus cereus: formation, sporulation, and dispersion. Appl. Environ. Microbiol. 73, 1481-1488. doi: 10.1128/AEM.01781-06
149. Xu, Y. B., Chen, M., Zhang, Y., Wang, M., Wang, Y., Huang, Q. B., et al. (2014). The phosphotransferase system gene ptsI in the endophytic bacterium Bacillus cereus is required for biofilm formation, colonization, and biocontrol against wheat sharp eyespot. FEMS Microbiol. Lett. 354, 142-152. doi: 10.1111/1574-6968.12438
150. Zafra, O., Lamprecht-Grandio, M., De Figueras, C. G., and Gonzalez-Pastor, J. E. (2012). Extracellular DNA release by undomesticated Bacillus subtilis is regulated by early competence. PLoS ONE 7:e48716. doi: 10.1371/journal.pone.0048716