Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
Review
. 2016 Oct 4:7:1550.
doi: 10.3389/fmicb.2016.01550. eCollection 2016.

Adaptation in Bacillus cereus: From Stress to Disease

Catherine Duport  1 , Michel Jobin  1 , Philippe Schmitt  1
Affiliations
Review

Adaptation in Bacillus cereus: From Stress to Disease

Catherine Duport et al. Front Microbiol. .

Abstract

Bacillus cereus is a food-borne pathogen that causes diarrheal disease in humans. After ingestion, B. cereus experiences in the human gastro-intestinal tract abiotic physical variables encountered in food, such as acidic pH in the stomach and changing oxygen conditions in the human intestine. B. cereus responds to environmental changing conditions (stress) by reversibly adjusting its physiology to maximize resource utilization while maintaining structural and genetic integrity by repairing and minimizing damage to cellular infrastructure. As reviewed in this article, B. cereus adapts to acidic pH and changing oxygen conditions through diverse regulatory mechanisms and then exploits its metabolic flexibility to grow and produce enterotoxins. We then focus on the intricate link between metabolism, redox homeostasis, and enterotoxins, which are recognized as important contributors of food-borne disease.

Keywords: Bacillus cereus; acidic pH; metabolism; oxygen sensing; redox homeostasis.

PubMed Disclaimer

Figures

FIGURE 1
FIGURE 1
Mechanisms involved in B. cereus acid resistance (adapted from Cotter and Hill, 2003). (i) The production of alkali by the ADI or urease system increases the internal pH of the cell. (ii) Proton pumps such as the F1F0-ATPase or that utilized by the GAD system bring about an increase in pHi. (iii) Cell density affects cell-to-cell communication. The involvement of Two Component Systems (TCS) and sigma factors can induce minor or global responses. (iv) Chaperones, proteases, and heat shock proteins (HdeAB) protect cellular proteins or degrade them if damaged. (v) DNA damaged as a consequence of a low pHi can be repaired through the excision of errors or the restarting of stalled replication forks. (vi) Modifications of membrane fatty acids composition affects the properties of the plasma membrane. (vii) Metabolism of the cells may be modified in response to environmental changes.
FIGURE 2
FIGURE 2
A simplified view of B. cereus central metabolism. This schematic shows our current understanding of how glycolysis (blue), the PPP (purple), the fermentation pathways (red), the TCA cycle (green) and aerobic respiratory chain (brown) are interconnected in growing B. cereus cells. The fermentation end products are shown in bold. The electron transport in the respiratory chain goes through dehydrogenation of NADH, as a first step. Electrons are transferred from NADH to menaquinone pool (Q), which serves as an electron carrier, and then, the pathway goes through two main branches. The first is one in which electrons go through the bc complex, cytochrome c and cytochrome oxidase caa3, in turn. The second contains only quinol oxidases (cytochromes bd or aa3). In each branch, electrons are finally accepted by oxygen molecules. The transfer of electrons is coupled to the formation of a proton gradient across the membrane which is tapped by F1F0-ATPase to generate ATP from ADP and Pi. ROS are generated as by-product from this process. Ldh, lactate dehydrogenase; Pdh, pyruvate dehydrogenase; Pfl, pyruvate formate lyase; NDH, NADH:menaquinone reductase; SDH, succinate:menaquinone oxidoreductase; GDH, glycerol-3-P:menaquinone reductase.
FIGURE 3
FIGURE 3
Redox-sensing mechanisms of transcriptional regulators in B. cereus. HoloFnr binds one [4Fe-4S]2+ cluster per monomer. This cluster is degraded upon exposition to oxygen. ApoFnr (clusterless) is active as a DNA binding protein under its reduced dimeric form. The oxidized ApoFnr form, which is stabilized by means of one or more SS bonds, is inactive. The thiol-based redox switch mediates a response to oxygen concentration or cellular oxidant (see text). Binding of ResD to DNA is not dependent on ResD phosphorylation status, which is regulated by the kinase and phosphatase activities of ResE. Rex senses the intracellular redox status through changes in the NADH/NAD+ ratio. Unlike the NAD+-bound Rex form, the NADH-bound Rex form is incapable of binding DNA. OhrR senses oxygen concentration or ROS through cysteine residues (see text). OhrR is a non-covalent dimer in its reduced form and a covalent dimer in its oxidized form. Dihydrolipoate (DHLA) and low molecular mass thiols (LMW) participate in the recovery of reduced OhrR from the oxidized form. B. cereus OhrR can bind DNA both under its reduced and oxidized form.
FIGURE 4
FIGURE 4
Adaptation to changing oxygen availability affects B. cereus pathogenicity at different levels. Oxygen acts directly on activity of Fnr and metabolism. Fnr, ResDE, Rex, and OhrR belong to a redox signaling pathway, which interconnects metabolism with expression of enterotoxins. In addition to its role in removing metabolism-generated ROS, antioxidant status modulates the oxidation status of Met residues in enterotoxins (Madeira et al., 2015). Metabolism also contributes directly to pathogenicity by supporting growth and stress resistance, and by modulating exoprotein synthesis.
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Adak S., Aulak K. S., Stuehr D. J. (2002). Direct evidence for nitric oxide production by a nitric-oxide synthase-like protein from Bacillus subtilis. J. Biol. Chem. 277 16167–16171. 10.1074/jbc.M201136200 - DOI - PubMed
    1. Agledal L., Niere M., Ziegler M. (2010). The phosphate makes a difference: cellular functions of NADP. Redox Rep. 15 2–10. 10.1179/174329210X12650506623122 - DOI - PMC - PubMed
    1. Alonso-Hernando A., Alonso-Calleja C., Capita R. (2010). Effects of exposure to poultry chemical decontaminants on the membrane fluidity of Listeria monocytogenes and Salmonella enterica strains. Int. J. Food Microbiol. 137 130–136. 10.1016/j.ijfoodmicro.2009.11.022 - DOI - PubMed
    1. Alvarez-Ordonez A., Fernandez A., Bernardo A., Lopez M. (2010a). Acid adaptation sensitizes Salmonella enterica serovar Typhimurium to osmotic and oxidative stresses. Arch. Lebensmittelhyg. 61 148–152. 10.2376/0003-925X-61-148 - DOI
    1. Alvarez-Ordonez A., Fernandez A., Bernardo A., Lopez M. (2010b). Acid tolerance in Salmonella typhimurium induced by culturing in the presence of organic acids at different growth temperatures. Food Microbiol. 27 44–49. 10.1016/j.fm.2009.07.015 - DOI - PubMed