Bacillus cereus sensu lato biofilm formation and its ecological importance

Flemming, 2019, Bacteria and archaea on Earth and their abundance in biofilms, Nat Rev Microbiol, 17, 247, 10.1038/s41579-019-0158-9 Flemming, 2010, The biofilm matrix, Nat Rev Microbiol, 8, 623, 10.1038/nrmicro2415 Sutherland, 2001, The biofilm matrix – an immobilized but dynamic microbial environment, Trends Microbiol, 9, 222, 10.1016/S0966-842X(01)02012-1 Ehling-Schulz, 2019, The Bacillus cereus group: Bacillus species with pathogenic potential, Microbiol Spectr, 7, 10.1128/microbiolspec.GPP3-0032-2018 Enosi Tuipulotu, 2021, Bacillus cereus: epidemiology, virulence factors, and host–pathogen interactions, Trends Microbiol, 29, 458, 10.1016/j.tim.2020.09.003 Helgason, 2000, Bacillus anthracis, Bacillus cereus, and Bacillus thuringiensis - one species on the basis of genetic evidence, Appl Environ Microbiol, 66, 2627, 10.1128/AEM.66.6.2627-2630.2000 Hoornstra, 2013, Potato crop as a source of rmetic Bacillus cereus and cereulide-induced mammalian cell toxicity, Appl Environ Microbiol, 79, 3534, 10.1128/AEM.00201-13 Ehling-Schulz, 2015, Food–bacteria interplay: pathometabolism of emetic Bacillus cereus, Front Microbiol, 6, 704, 10.3389/fmicb.2015.00704 Saile, 2006, Bacillus anthracis multiplication, persistence, and genetic exchange in the rhizosphere of grass plants, Appl Environ Microbiol, 72, 3168, 10.1128/AEM.72.5.3168-3174.2006 Monnerat, 2009, Translocation and insecticidal activity of Bacillus thuringiensis living inside of plants, Microb Biotechnol, 2, 512, 10.1111/j.1751-7915.2009.00116.x Ruan, 2015, Are nematodes a missing link in the confounded ecology of the entomopathogen Bacillus thuringiensis?, Trends Microbiol, 23, 341, 10.1016/j.tim.2015.02.011 Cutting, 2011, Bacillus probiotics, Food Microbiol, 28, 214, 10.1016/j.fm.2010.03.007 Zhu, 2016, Probiotic Bacillus cereus strains, a potential risk for public health in China, Front Microbiol, 7, 718, 10.3389/fmicb.2016.00718 Vidal-Quist, 2013, Bacillus thuringiensis colonises plant roots in a phylogeny-dependent manner, FEMS Microbiol Ecol, 86, 474, 10.1111/1574-6941.12175 Duport, 2016, Adaptation in Bacillus cereus: from stress to disease, Front Microbiol, 7, 1550, 10.3389/fmicb.2016.01550 Lakshmanan, 2012, Microbe-associated molecular patterns-triggered root responses mediate beneficial rhizobacterial recruitment in Arabidopsis, Plant Physiol, 160, 1642, 10.1104/pp.112.200386 Caro-Astorga, 2014, A genomic region involved in the formation of adhesin fibers in Bacillus cereus biofilms, Front Microbiol, 5, 745 Öksüz, 2012, Bacillus Cereus catheter related bloodstream infection in a patient with acute lymphblastic leukemia, Mediterr J Hematol Infect Dis, 4, 10.4084/mjhid.2012.004 Auger, 2009, Biofilm formation and cell surface properties among pathogenic and nonpathogenic strains of the Bacillus cereus group, Appl Environ Microbiol, 75, 6616, 10.1128/AEM.00155-09 Coughlan, 2016, New weapons to fight old enemies: novel strategies for the (bio)control of bacterial biofilms in the food industry, Front Microbiol, 7, 1641, 10.3389/fmicb.2016.01641 Galié, 2018, Biofilms in the food industry: health aspects and control methods, Front Microbiol, 9, 898, 10.3389/fmicb.2018.00898 Rumbaugh, 2020, Biofilm dispersion, Nat Rev Microbiol, 18, 571, 10.1038/s41579-020-0385-0 Majed, 2016, Bacillus cereus biofilms—same, only different, Front Microbiol, 7, 1054, 10.3389/fmicb.2016.01054 Arnaouteli, 2017, Bifunctionality of a biofilm matrix protein controlled by redox state, Proc Natl Acad Sci Unit States Am, 114, E6184, 10.1073/pnas.1707687114 Yan, 2017, Genome-wide investigation of biofilm formation in Bacillus cereus, Appl Environ Microbiol, 83, 10.1128/AEM.00561-17 Slack, 2006, A gene required for nutritional repression of the Bacillus subtilis dipeptide permease operon, Mol Microbiol, 15, 689, 10.1111/j.1365-2958.1995.tb02378.x Yan, 2016, The comER gene plays an important role in biofilm formation and sporulation in both Bacillus subtilis and Bacillus cereus, Front Microbiol, 7, 1025, 10.3389/fmicb.2016.01025 Okshevsky, 2018, A transposon mutant library of Bacillus cereus ATCC 10987 reveals novel genes required for biofilm formation and implicates motility as an important factor for pellicle-biofilm formation, Microbiol, 7 Chai, 2012, Galactose metabolism plays a crucial role in biofilm formation by Bacillus subtilis, mBio, 3, 10.1128/mBio.00184-12 Lin, 2021, Adaptation of Bacillus thuringiensis to plant colonization affects differentiation and toxicity, mSystems, 6, 10.1128/mSystems.00864-21 Caro-Astorga, 2020, Biofilm formation displays intrinsic offensive and defensive features of Bacillus cereus, NPJ Biofilms Microbiomes, 6, 3, 10.1038/s41522-019-0112-7 Houry, 2010, Involvement of motility and flagella in Bacillus cereus biofilm formation, Microbiology, 156, 1009, 10.1099/mic.0.034827-0 Hengge, 2009, Principles of c-di-GMP signalling in bacteria, Nat Rev Microbiol, 7, 263, 10.1038/nrmicro2109 Fagerlund, 2016, Cyclic diguanylate regulation of Bacillus cereus group biofilm formation, Mol Microbiol, 101, 471, 10.1111/mmi.13405 Jenal, 2017, Cyclic di-GMP: second messenger extraordinaire, Nat Rev Microbiol, 15, 271, 10.1038/nrmicro.2016.190 Fu, 2018, c-di-GMP regulates various phenotypes and insecticidal activity of Gram-Positive Bacillus thuringiensis, Front Microbiol, 9, 45, 10.3389/fmicb.2018.00045 Smith, 2020, MogR Is a ubiquitous transcriptional repressor affecting motility, biofilm formation and virulence in Bacillus thuringiensis, Front Microbiol, 11, 610650, 10.3389/fmicb.2020.610650 Houry, 2012, Bacterial swimmers that infiltrate and take over the biofilm matrix, Proc Natl Acad Sci U S A, 109, 13088, 10.1073/pnas.1200791109 Yu, 2021, Hitchhiking behavior in bacteriophages facilitates phage infection and enhances carrier bacteria colonization, Environ Sci Technol, 55, 2462, 10.1021/acs.est.0c06969 Li, 2015, Spatio-temporal interaction of bacteria mixture within biofilms, Procedia Environ Sci, 26, 11, 10.1016/j.proenv.2015.05.009 Flemming, 2016, 179 Cairns, 2014, Biofilm formation by Bacillus subtilis: new insights into regulatory strategies and assembly mechanisms, Mol Microbiol, 93, 587, 10.1111/mmi.12697 Vlamakis, 2013, Sticking together: building a biofilm the Bacillus subtilis way, Nat Rev Microbiol, 11, 157, 10.1038/nrmicro2960 Arnaouteli, 2021, Bacillus subtilis biofilm formation and social interactions, Nat Rev Microbiol, 19, 600, 10.1038/s41579-021-00540-9 Branda, 2001, Fruiting body formation by Bacillus subtilis, Proc Natl Acad Sci U S A, 98, 11621, 10.1073/pnas.191384198 Kearns, 2005, A master regulator for biofilm formation by Bacillus subtilis, Mol Microbiol, 55, 739, 10.1111/j.1365-2958.2004.04440.x Fagerlund, 2014, SinR controls enterotoxin expression in Bacillus thuringiensis biofilms, PLoS One, 9, 10.1371/journal.pone.0087532 Gao, 2015, Alternative modes of biofilm formation by plant-associated Bacillus cereus, Microbiol, 4, 452 Xu, 2017, The spo0A-sinI-sinR regulatory circuit plays an essential role in biofilm formation, nematicidal activities, and plant protection in Bacillus cereus AR156, Mol Plant Microbe Interact, 30, 603, 10.1094/MPMI-02-17-0042-R Huang, 2021, SpoVG is an important regulator of sporulation and affects biofilm formation by regulating Spo0A transcription in Bacillus cereus 0–9, BMC Microbiol, 21, 172, 10.1186/s12866-021-02239-6 Zhang, 2020, The YmdB protein regulates biofilm formation dependent on the repressor SinR in Bacillus cereus 0–9, World J Microbiol Biotechnol, 36, 165, 10.1007/s11274-020-02933-z Diethmaier, 2011, A novel factor controlling bistability in Bacillus subtilis: the YmdB protein affects flagellin expression and biofilm formation, J Bacteriol, 193, 5997, 10.1128/JB.05360-11 Diethmaier, 2014, The YmdB phosphodiesterase is a global regulator of late adaptive responses in Bacillus subtilis, J Bacteriol, 196, 265, 10.1128/JB.00826-13 Zhang, 2020, GapB is involved in biofilm formation dependent on LrgAB but not the SinI/R system in Bacillus cereus 0-9, Front Microbiol, 11, 591926, 10.3389/fmicb.2020.591926 F, 1999, Regulation of nitrogen metabolism in Bacillus subtilis: vive la différence, Mol Microbiol, 32, 223, 10.1046/j.1365-2958.1999.01333.x Kovács, 2016, The global regulator CodY is required for the fitness of Bacillus cereus in various laboratory media and certain beverages, FEMS Microbiol Lett, 363, fnw126, 10.1093/femsle/fnw126 Molle, 2003, Additional targets of the Bacillus subtilis global regulator CodY identified by chromatin immunoprecipitation and genome-wide transcript analysis, J Bacteriol, 185, 1911, 10.1128/JB.185.6.1911-1922.2003 Lindbäck, 2012, CodY, a pleiotropic regulator, influences multicellular behaviour and efficient production of virulence factors in Bacillus cereus, Environ Microbiol, 14, 2233, 10.1111/j.1462-2920.2012.02766.x Hsueh, 2008, Characterization of the codY gene and its influence on biofilm formation in Bacillus cereus, Arch Microbiol, 189, 557, 10.1007/s00203-008-0348-8 Huillet, 2017, The CodY-dependent clhAB2 operon is involved in cell shape, chaining and autolysis in Bacillus cereus ATCC 14579, PLoS One, 12, 10.1371/journal.pone.0184975 Povolotsky, 2012, ‘Life-style’ control networks in Escherichia coli: signaling by the second messenger c-di-GMP, J Biotechnol, 160, 10, 10.1016/j.jbiotec.2011.12.024 Römling, 2013, Cyclic di-GMP: the first 25 years of a universal bacterial second messenger, Microbiol Mol Biol Rev, 77, 1, 10.1128/MMBR.00043-12 Chen, 2012, Evidence for cyclic di-GMP-mediated signaling in Bacillus subtilis, J Bacteriol, 194, 5080, 10.1128/JB.01092-12 Gao, 2013, Functional characterization of core components of the Bacillus subtilis cyclic-di-GMP signaling pathway, J Bacteriol, 195, 4782, 10.1128/JB.00373-13 Finke, 2019, Bacillus thuringiensis CbpA is a collagen binding cell surface protein under c-di-GMP control, Cell Surf, 5, 100032, 10.1016/j.tcsw.2019.100032 Verplaetse, 2015, Cell differentiation in a Bacillus thuringiensis population during planktonic growth, biofilm formation, and host infection, mBio, 6, e00138, 10.1128/mBio.00138-15 Slamti, 2014, Quorum sensing in Bacillus thuringiensis is required for completion of a full infectious cycle in the insect, Toxins, 6, 2239, 10.3390/toxins6082239 Gohar, 2008, The PlcR virulence regulon of Bacillus cereus, PLoS One, 3, 10.1371/journal.pone.0002793 Slamti, 2016, 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, 10.3389/fmicb.2015.01501 Slamti, 2002, A cell-cell signaling peptide activates the PlcR virulence regulon in bacteria of the Bacillus cereus group, EMBO J, 21, 4550, 10.1093/emboj/cdf450 Hsueh, 2006, Biofilm formation by Bacillus cereus is influenced by PlcR, a pleiotropic regulator, Appl Environ Microbiol, 72, 5089, 10.1128/AEM.00573-06 Gélis-Jeanvoine, 2017, Genetic and functional analyses of krs, a locus encoding kurstakin, a lipopeptide produced by Bacillus thuringiensis, Res Microbiol, 168, 356, 10.1016/j.resmic.2016.06.002 Gastélum, 2020, Rap protein paralogs of Bacillus thuringiensis: a multifunctional and redundant regulatory repertoire for the control of collective functions, J Bacteriol, 202, 747, 10.1128/JB.00747-19 Nordgaard, 2021, Deletion of Rap‐Phr systems in Bacillus subtilis influences in vitro biofilm formation and plant root colonization, Microbiol, 10, e1212 Li, 2016, Discovery of a unique extracellular polysaccharide in members of the pathogenic Bacillus that can co-form with spores, J Biol Chem, 291, 19051, 10.1074/jbc.M116.724708 Bundalovic-Torma, 2020, A systematic pipeline for classifying bacterial operons reveals the evolutionary landscape of biofilm machineries, PLoS Comput Biol, 16, 10.1371/journal.pcbi.1007721 Whitfield, 2020, Discovery and characterization of a Gram-positive Pel polysaccharide biosynthetic gene cluster, PLoS Pathog, 16, 10.1371/journal.ppat.1008281 Whitfield, 2021, The matrix revisited: opening night for the Pel polysaccharide across eubacterial Kingdoms, Microbiol Insights, 14, 10.1177/1178636120988588 Caro-Astorga, 2020, Two genomic regions encoding exopolysaccharide production systems have complementary functions in B. cereus multicellularity and host interaction, Sci Rep, 10, 1000, 10.1038/s41598-020-57970-3 Candela, 2019, CalY is a major virulence factor and a biofilm matrix protein, Mol Microbiol, 111, 1416, 10.1111/mmi.14184 Mammeri, 2019, Molecular architecture of bacterial amyloids in Bacillus biofilms, Faseb J, 33, 12146, 10.1096/fj.201900831R Veening, 2006, Effects of phosphorelay perturbations on architecture, sporulation, and spore resistance in biofilms of Bacillus subtilis, J Bacteriol, 188, 3099, 10.1128/JB.188.8.3099-3109.2006 Vlamakis, 2008, Control of cell fate by the formation of an architecturally complex bacterial community, Genes Dev, 22, 945, 10.1101/gad.1645008 Verplaetse, 2017, Two distinct pathways lead Bacillus thuringiensis to commit to sporulation in biofilm, Res Microbiol, 168, 388, 10.1016/j.resmic.2016.03.006 El-Khoury, 2021, Massive integration of planktonic cells within a developing biofilm, Microorganisms, 9, 298, 10.3390/microorganisms9020298 El-Khoury, 2016, Spatio-temporal evolution of sporulation in Bacillus thuringiensis biofilm, Front Microbiol, 7, 1222, 10.3389/fmicb.2016.01222 Huang, 2020, Bacillus cereus spores and toxins – the potential role of biofilms, Food Microbiol, 90, 103493, 10.1016/j.fm.2020.103493 Kwon, 2017, Biofilm formation of Bacillus cereus under food-processing-related conditions, Food Sci Biotechnol, 26, 1103, 10.1007/s10068-017-0129-8 Christison, 2007, Cleaning and handling implements as potential reservoirs for bacterial contamination of some ready-to-eat foods in retail delicatessen environments, J Food Protect, 70, 2878, 10.4315/0362-028X-70.12.2878 Bridier, 2010, The biofilm architecture of sixty opportunistic pathogens deciphered using a high throughput CLSM method, J Microbiol Methods, 82, 64, 10.1016/j.mimet.2010.04.006 Ehling-Schulz, 2006, Cereulide synthetase gene cluster from emetic Bacillus cereus: structure and location on a mega virulence plasmid related to Bacillus anthracis toxin plasmid pXO1, BMC Microbiol, 6, 20, 10.1186/1471-2180-6-20 Johler, 2018, Enterotoxin production of Bacillus thuringiensis isolates from biopesticides, foods, and outbreaks, Front Microbiol, 9, 1915, 10.3389/fmicb.2018.01915 Faille, 2014, Sporulation of Bacillus spp. within biofilms: a potential source of contamination in food processing environments, Food Microbiol, 40, 64, 10.1016/j.fm.2013.12.004 Elhariry, 2011, Attachment strength and biofilm forming ability of Bacillus cereus on green-leafy vegetables: cabbage and lettuce, Food Microbiol, 28, 1266, 10.1016/j.fm.2011.05.004 Garrett, 2008, Bacterial adhesion and biofilms on surfaces, Prog Nat Sci, 18, 1049, 10.1016/j.pnsc.2008.04.001 Chmielewski, 2003, Biofilm formation and control in food processing facilities, Compr Rev Food Sci Food Saf, 2, 22, 10.1111/j.1541-4337.2003.tb00012.x Peng, 2001, Surface characteristics of Bacillus cereus and its adhesion to stainless steel, Int J Food Microbiol, 65, 105, 10.1016/S0168-1605(00)00517-1 Wijman, 2007, Air-liquid interface biofilms of Bacillus cereus: formation, sporulation, and dispersion, Appl Environ Microbiol, 73, 1481, 10.1128/AEM.01781-06 Antequera‐Gómez, 2021, Sporulation is dispensable for the vegetable‐associated life cycle of the human pathogen Bacillus cereus, Microb Biotechnol, 14, 1550, 10.1111/1751-7915.13816 Bremer, 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, 10.1016/j.ijfoodmicro.2005.07.004 Kumari, 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, 10.1016/j.foodcont.2013.08.014 Lee, 2020, Inhibitory effects of combinations of chemicals on Escherichia coli, Bacillus cereus, and Staphylococcus aureus biofilms during the clean-in-place process at an experimental dairy plant, J Food Protect, 83, 1302, 10.4315/JFP-19-505 Leggett, 2016, Assessing the activity of microbicides against bacterial spores: knowledge and pitfalls, J Appl Microbiol, 120, 1174, 10.1111/jam.13061 Silva, 2018, Efficiency of different disinfectants on Bacillus cereus sensu stricto biofilms on stainless-steel surfaces in contact with milk, Front Microbiol, 9, 2934, 10.3389/fmicb.2018.02934 Choudhary, 2009, Interactions of Bacillus spp. and plants – with special reference to induced systemic resistance (ISR), Microbiol Res, 164, 493, 10.1016/j.micres.2008.08.007 Xu, 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, 10.1111/1574-6968.12438 Blake, 2021, Diversification of Bacillus subtilis during experimental evolution on Arabidopsis thaliana and the complementarity in root colonization of evolved subpopulations, Environ Microbiol, 23, 6122, 10.1111/1462-2920.15680 Nordgaard