Bacillus cereus Biofilms-Same, Only Different

Abstract

Bacillus cereus displays a high diversity of lifestyles and ecological niches and include beneficial as well as pathogenic strains. These strains are widespread in the environment, are found on inert as well as on living surfaces and contaminate persistently the production lines of the food industry. Biofilms are suspected to play a key role in this ubiquitous distribution and in this persistency. Indeed, B. cereus produces a variety of biofilms which differ in their architecture and mechanism of formation, possibly reflecting an adaptation to various environments. Depending on the strain, B. cereus has the ability to grow as immersed or floating biofilms, and to secrete within the biofilm a vast array of metabolites, surfactants, bacteriocins, enzymes, and toxins, all compounds susceptible to act on the biofilm itself and/or on its environment. Within the biofilm, B. cereus exists in different physiological states and is able to generate highly resistant and adhesive spores, which themselves will increase the resistance of the bacterium to antimicrobials or to cleaning procedures. Current researches show that, despite similarities with the regulation processes and effector molecules involved in the initiation and maturation of the extensively studied Bacillus subtilis biofilm, important differences exists between the two species. The present review summarizes the up to date knowledge on biofilms produced by B. cereus and by two closely related pathogens, Bacillus thuringiensis and Bacillus anthracis. Economic issues caused by B. cereus biofilms and management strategies implemented to control these biofilms are included in this review, which also discuss the ecological and functional roles of biofilms in the lifecycle of these bacterial species and explore future developments in this important research area.

Keywords: Bacillus; anthracis; biofilm; cereus; ecology; food; regulation; thuringiensis.

Figure 1

Number of articles published between 1975 and 2015 on B. cereus biofilms. Articles published on B. cereus, B. thuringiensis, or B. anthracis biofilms, in percent of the total number of articles published on the same species.

Figure 2

Schematic representation of the regulatory network controlling biofilm formation in B. cereus. Circles symbolize proteins, triangles symbolize open reading frames (ORFs). Arrows indicate activation and blunt lines indicate repression. Dotted arrows represent transcription. The protein component of the matrix is encoded by the sipW-tasA operon and by calY which promoters are activated by σ54 and repressed by SinR. SinR is antagonized by SinI. The transcription of sinI is activated by the master regulator of sporulation Spo0A. Furthermore, Spo0A downregulates the regulator AbrB, resulting in biofilm formation. Several quorum sensing systems are involved in biofilm formation. The regulator PlcR activates the transcription of nprR. NprR promotes kurstakin production, which itself promotes biofilm formation. The autoinducer AI-2 plays an inhibitory effect on biofilm formation.

Figure 3

Suggested model for biofilm role in the life cycle of B. cereus and B. thuringiensis in the environment. Biofilms (in red) growing in the topsoil contaminate the roots and leaves of plants. Earthworm (in pink) feeding on soil organic matter, nematodes (in yellow) feeding on plant roots, caterpillar (in purple) feeding on plant leaves, or isopodes (in brown) feeding on plant debris, ingest bacteria, which can then grow as biofilms in their gut. The invertebrates move further in the environment and, upon death, contaminate back the topsoil, giving birth to a new cycle.

Figure 4

Observation by scanning electron microscopy of a mixed biofilm formed by two strains: B. cereus 98/4 and Comamonas testosteroni CCL24 (Faille et al., 2014).

Figure 5

Microscopic images of a B. cereus biofilm grown for 48 h in TSB 1/10. Observation by epifluorescence after staining with the Live/Dead stain (magnification × 400). Endospores produced within the biofilm are stained in green, cells are stained in orange-green.