Elsevier

Food Microbiology

Volume 90, September 2020, 103493
Food Microbiology

Bacillus cereus spores and toxins – The potential role of biofilms

https://doi.org/10.1016/j.fm.2020.103493Get rights and content

Highlights

  • The review highlights genetic determinants that are involved in sporulation, toxin production and biofilm formation based on current research.

  • The review highlights evidence showing the possible correlation of spore, toxin and biofilm formation of Bacillus cereus, especially in food-related processing.

  • This review highlighting the potential relationship between toxin production and biofilm formation in Bacillus cereus.

Abstract

Bacillus cereus is a well-known foodborne pathogen capable of causing two types of gastrointestinal diseases, diarrhoea and emesis. It is of particular concern for the food industry causing food safety issues, due to the formation of spores, biofilms and diarrhoea and/or emetic toxins. This review reveals the possible link between two food safety issues – toxins and spores - and the role of biofilms. The review highlights genetic determinants that are involved in sporulation, toxin production and biofilm formation based on current research, and evidence showing the possible correlation of spore, toxin and biofilm formation of B. cereus. This is the first review highlighting the potential relationship between toxin production and biofilm formation in B. cereus.

Section snippets

Bacillus cereus: spores, toxins and biofilms

Bacillus cereus sensu lato group comprise several closely related species including Bacillus cereus sensu stricto (B. cereus s.s. referred as B. cereus below), Bacillus thuringiensis, Bacillus anthracis, Bacillus weihenstephanensis, Bacillus mycoides, Bacillus pseudomycoides and Bacillus cytotoxicus (Jensen et al., 2003; Lechner et al., 1998; Guinebretière et al., 2010). B. cereus is a recognized foodborne pathogen widely distributed environmentally in spores and/or vegetative cells, causing

Genetic links for spore, toxin and biofilm production

Table 1 and Fig. 2 below summarise the current knowledge of genetic determinants and related pathways involved in spore, toxin and biofilm formation of B. cereus and/or Bacillus subtilis (B.subtilis) based on literature review.

Intertwined regulatory pathways between biofilm formation and sporulation have been proposed for B. subtilis (Vlamakis et al., 2013). These could also be similar in B. cereus but this needs to be confirmed. A Spo0A deletion mutant of B. subtilis shows a defect in biofilm

Biofilm: a supportive reservoir for sporulation?

B. cereus biofilms are mainly comprised of vegetative cells, however during maturation and aging, B. cereus is able to form spores within the established biofilms (Ryu and Beuchat, 2005; Wijman et al., 2007; Faille et al., 2014). The biofilms on manufacturing plant surfaces could become a reservoir for spores, as has been shown previously for thermophilic spore-formers Geobacillus stearothermophilus (Burgess et al., 2014). Those spores formed in the biofilm may provide a source of contamination

Biofilm: a microbial community that favors toxin production?

The expression of toxin genes and toxin production can be influenced by environmental factors and can vary from strain to strain of B. cereus (Jeβberger et al., 2015), making studies difficult. However, there is little knowledge about toxin production within biofilms cells compared to planktonic grown cells. It is commonly accepted that B. cereus-induced diarrhoea is caused by enterotoxin produced in the intestine (Ceuppens et al., 2012), therefore, biofilm formed in the intestine should be

Spores and toxins

Spores and toxins of B. cereus combine to provide a food safety concern, however, the link between spores and toxin production is unknown. It is known that spores of B. cereus survive gastric passage to attach to the small intestine, germinate and produce enterotoxins during outgrowth causing diarrhoea, however, these toxins hardly withstand the gastrointestinal conditions (Ceuppens et al., 2012). The cytotoxicity of B. cereus group members (B. cereus, B. subtilis and B. thuringiensis) could be

Future perspectives

The sporulation of B. cereus within biofilms has been demonstrated, although further study is needed to investigate if biofilms play a role in sporulation and the direct link between biofilm formation and sporulation of B. cereus. There is little evidence of the link between toxin production and biofilm formation in B. cereus. There is also a little evidence of the role of sporulation in the toxin production of B. cereus. As a foodborne pathogen, toxin production is important and any

Declaration of competing interest

This manuscript is original, and no part of the manuscript has been published before. There are no conflicts of interest to disclose.

References (98)

  • D. Lindsay et al.

    Biofilm-spore response in Bacillus cereus and Bacillus subtilis during nutrient limitation

    J. Food Protect.

    (2006)
  • D. Lindsay et al.

    Spore formation in Bacillus subtilis biofilms

    J. Food Protect.

    (2005)
  • M.R. Parsek et al.

    Quorum sensing signals in development of Pseudomonas aeruginosa biofilms

    Methods Enzymol.

    (1999)
  • R. Patiño-Navarrete et al.

    Evolutionary processes and environmental factors underlying the genetic diversity and lifestyles of Bacillus cereus group bacteria

    Res. Microbiol.

    (2017)
  • N. Ramarao et al.

    Adhesion and cytotoxicity of Bacillus cereus and Bacillus thuringiensis to epithelial cells are FlhA and PlcR dependent, respectively

    Microb. Infect.

    (2006)
  • M.A. Riley et al.

    Bacteriocin diversity: ecological and evolutionary perspectives

    Biochimie

    (2002)
  • J.-H. Ryu et al.

    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 Protect.

    (2005)
  • J.l. Schoeni et al.

    Bacillus cereus food poisoning and its toxins

    J. Food Protect.

    (2005)
  • R. Shaheen et al.

    Persistence strategies of Bacillus cereus spores isolated from dairy silo tanks

    Food Microbiol.

    (2010)
  • M. Simões et al.

    A review of current and emergent biofilm control strategies

    LWT - Food Sci. Technol. (Lebensmittel-Wissenschaft -Technol.)

    (2010)
  • G. Tauveron et al.

    Variability among Bacillus cereus strains in spore surface properties and influence on their ability to contaminate food surface equipment

    Int. J. Food Microbiol.

    (2006)
  • M. Wagner et al.

    Combined use of confocal laser scanning microscopy (CLSM) and Raman microscopy (RM): investigations on EPS - Matrix

    Water Res.

    (2009)
  • H. Agaisse et al.

    PlcR is a pleiotropic regulator of extracellular virulence factor gene expression in Bacillus thuringiensis

    Mol. Microbiol.

    (1999)
  • C. Aguilar et al.

    KinD is a checkpoint protein linking spore formation to extracellular-matrix production in Bacillus subtilis biofilms

    mBio

    (2010)
  • A. Andersson et al.

    The adhesion of Bacillus cereus spores to epithelial cells might be an additional virulence mechanism

  • M.B. Miller et al.

    Quorum sensing in bacteria

    Annu. Rev. Microbiol.

    (2001)
  • D.J. Beecher et al.

    Enterotoxic activity of hemolysin BL from Bacillus cereus

    Infect. Immun.

    (1995)
  • L. Bouillaut et al.

    F1hA influences Bacillus thuringiensis PlcR-regulated gene transcription, protein production, and virulence

    Appl. Environ. Microbiol.

    (2005)
  • S.A. Burgess et al.

    The formation of spores in biofilms of Anoxybacillus flavithermus

    J. Appl. Microbiol.

    (2009)
  • S.A. Burgess et al.

    Characterization of thermophilic bacilli from a milk powder processing plant

    J. Appl. Microbiol.

    (2014)
  • S. Bragadeeswaran et al.

    Exopolysaccharide production by Bacillus cereus GU812900, a fouling marine bacterium

    Afr. J. Microbiol. Res.

    (2011)
  • N.C. Caiazza et al.

    Alpha-toxin is required for biofilm formation by Staphylococcus aureus

    J. Bacteriol.

    (2003)
  • S. Ceuppens et al.

    Diversity of Bacillus cereus group strains is reflected in their broad range of pathogenicity and diverse ecological lifestyles

    FEMS Microbiol. Ecol.

    (2013)
  • S. Ceuppens et al.

    Survival and germination of Bacillus cereus spores without outgrowth or enterotoxin production during in vitro simulation of gastrointestinal transit

    Appl. Environ. Microbiol.

    (2012)
  • S. Charlton et al.

    Characterization of the exosporium of Bacillus cereus

    J. Appl. Microbiol.

    (1999)
  • R.A.N. Chmielewski et al.

    Biofilm formation and control in food processing facilities

    Compr. Rev. Food Sci.

    (2003)
  • D. Davies

    Understanding biofilm resistance to antibacterial agents

    Nat. Rev. Drug Discov.

    (2003)
  • M.-L. Divanac’h et al.

    Tracking spore-forming bacteria in food: from natural biodiversity to selection by processes

    Int. J. Food Microbiol.

    (2012)
  • V.M. Doll et al.

    Concerted action of sphingomyelinase and non-hemolytic enterotoxin in pathogenic Bacillus cereus

    PLoS One

    (2013)
  • M. Ehling-Schulz et al.

    Bacillus cereus, the causative agent of an emetic type of food-borne illness

    Mol. Nutr. Food Res.

    (2004)
  • M. Ehling-Schulz et al.

    Emetic toxin formation of Bacillus cereus is restricted to a single evolutionary lineage of closely related strains

    Microbiology

    (2005)
  • M. Ehling-Schulz et al.

    Food–bacteria interplay: pathometabolism of emetic Bacillus cereus

    Front. Microbiol.

    (2015)
  • A. Fagerlund et al.

    SinR controls enterotoxin expression in Bacillus thuringiensis biofilms

    PLoS One

    (2014)
  • C. Fermanian et al.

    Diarrhoeal toxin production at low temperature by selected strains of Bacillus cereus

    J. Dairy Res.

    (1997)
  • H.C. Flemming et al.

    Biofilms: an emergent form of bacterial life

    Nat. Rev. Microbiol.

    (2016)
  • S. Galié et al.

    Biofilms in the food industry: health aspects and control methods

    Front. Microbiol.

    (2018)
  • T.G. García et al.

    Phosphorylation of the Bacillus subtilis replication controller YabA plays a role in regulation of sporulation and biofilm formation

    Front. Microbiol.

    (2018)
  • E. Ghelardi et al.

    Requirement of flhA for swarming differentiation, flagellin export, and secretion of virulence-associated proteins in Bacillus thuringiensis

    J. Bacteriol.

    (2002)
  • M. Gohar et al.

    The PlcR virulence regulon of Bacillus cereus

    PLoS One

    (2008)
  • Cited by (0)

    View full text