The Bacillus cereus Group: Bacillus Species with Pathogenic Potential

Abstract

The Bacillus cereus group includes several Bacillus species with closely related phylogeny. The most well-studied members of the group, B. anthracis, B. cereus, and B. thuringiensis, are known for their pathogenic potential. Here, we present the historical rationale for speciation and discuss shared and unique features of these bacteria. Aspects of cell morphology and physiology, and genome sequence similarity and gene synteny support close evolutionary relationships for these three species. For many strains, distinct differences in virulence factor synthesis provide facile means for species assignment. B. anthracis is the causative agent of anthrax. Some B. cereus strains are commonly recognized as food poisoning agents, but strains can also cause localized wound and eye infections as well as systemic disease. Certain B. thuringiensis strains are entomopathogens and have been commercialized for use as biopesticides, while some strains have been reported to cause infection in immunocompromised individuals. In this article we compare and contrast B. anthracis, B. cereus, and B. thuringiensis, including ecology, cell structure and development, virulence attributes, gene regulation and genetic exchange systems, and experimental models of disease.

FIGURE 1

The five major phylogenetic clades of the B. cereus group. Clade I is known as the B. anthracis clade but also includes emetic B. cereus and several clinical B. thuringiensis isolates. Clade II is known as the B. cereus/B. thuringiensis clade and includes most of the commercially used B thurigiensis as well as the B. cereus and B. thuringiensis type strains. Clade III is known as the B. weihenstephanensis clade and comprises most of the psychrotolerant isolates of the B. cereus group. Clade IV includes strains belonging to various B. cereus group species. These clades are based on multilocus sequence typing, amplified fragment length polymorphism, and whole-genome sequence data (–431). The thermotolerant strains belonging to the species B. cytotoxicus cluster together in a separate group.

FIGURE 2

Transmission of the B. cereus group species from the soil reservoir to humans via food and textile production. Soil and soil-associated organisms including plants, insects, nematodes, and amoebae, serve as the major reservoirs for acquisition of spores. The bacteria are transferred to humans through agricultural products including food and animal-associated textiles, entering humans and other mammals through ingestion, inhalation, and breaks in the skin. Illustration credit: Olive E. Morrison.

FIGURE 3

(A) Thin-section transmission electron micrograph of B. anthracis cell after 5 hours of sporulation (left image) and a mature spore (right image). The forespore inner membrane (FS IM) and nascent exosporium (Ex) (left image), and forespore inner membrane (FS IM), mature exosporium (Ex), coat (Ct), interspace, (Is), and cortex (Cx) (right image) are labeled. (B) B. thuringiensis sporulating cell with parasporal crystal. Cells were sporulated, prepared, and imaged as described in reference . Image credit: (A) Tyler Boone and Adam Driks. (B) Fuping Song.

FIGURE 4

Cereulide, the emetic toxin of B. cereus.

FIGURE 5

The infectious cycle of B. thuringiensis in a susceptible insect larva. Ingestion of spores and crystals is followed by the dissolution of the crystal in the alkaline environment of the midgut. Insect proteases activate Cry proteins. Spores germinate in the paralyzed insect gut. Cry toxins degrade the peritrophic membrane. Bacteria multiply and express PlcR-regulated genes. The intestinal barrier is disrupted and bacteria gain access to the hemocoel. The bacteria resist host defenses and cause a fatal septicemia. The NprR regulon is activated, and the bacteria survive in the host cadaver. Finally, spores and vegetative cells are disseminated outside of the host.