Bacillus cereus sensu lato is a common contaminant of improperly stored food and human milk, capable of causing severe emetic and diarrheal diseases, particularly in infants and immunocompromised individuals. In this in vitro study, the effects of various temperatures and carbohydrate substrates on the growth of B. cereus (pacificus) strain ATCC 10987 and its expression of enterotoxin genes were explored. Bacterial growth at several temperatures and with six different carbohydrate substrates was evaluated. In cultures grown with various substrates at 37 °C, selected metabolites were analyzed using capillary electrophoresis and RNA-seq transcriptomic profiling was performed. At the same temperature, glucose, fructose, sucrose, and xylitol-enriched environments were preferable for the bacterial growth to lactose and galactose-enriched media. Lactate production markedly increased in bacterial cultures grown with glucose, fructose, or sucrose, accompanied by a drop in pH and increased substrate consumption. The lowest expression of non-hemolytic enterotoxin genes (nhe) was observed in glucose and lactose-enriched media, while downregulation of enterotoxin FM gene (entFM) expression was found in bacteria cultured with lactose. Other known enterotoxin genes, such as hemolysin BL (hbl) and cytotoxin K (cytK), were not expressed by this bacterial strain under any of the tested conditions. In conclusion, a lactose-rich environment slowed the growth of B. cereus (pacificus) ATCC 10987 and was associated with a downward trend in the expression of the enterotoxin genes nhe and entFM. These findings indicate that the presence of lactose, a dominant carbohydrate of human milk, may influence the pathogenic potential of B. cereus s. l.

Department of Biochemistry Faculty of Science Masaryk University Kotlarska 2 Brno Czech Republic

Institute of Analytical Chemistry of the Czech Academy of Sciences v v i Veveri 97 Brno Czech Republic

Institute of Microbiology St Anne's University Hospital in Brno Pekarska 53 Brno Czech Republic

RECETOX Faculty of Science Masaryk University Kotlarska 2 Brno Czech Republic

Zobrazit více v PubMed

Griffiths, M. W. & Schraft, H. Bacillus cereus food poisoning. In

Marrollo, R. Bacillus cereus food-borne disease. In

Andersen Borge, G. I., Skeie, M., Sørhaug, T., Langsrud, T. & Granum, P. E. Growth and toxin profiles of PubMed DOI

Liao, S. L. & Tsai, M. H. Bacillus cereus bacteremia in a preterm infant caused by consumption of contaminated breastmilk. PubMed DOI

Rasko, D. A. et al. The genome sequence of Bacillus cereus ATCC 10987 reveals metabolic adaptations and a large plasmid related to Bacillus anthracis pXO1. PubMed DOI PMC

Rodrigo, D., Rosell, C. M. & Martinez, A. Risk of Bacillus cereus in relation to rice and derivatives. PubMed DOI PMC

Stenfors Arnesen, L. P., Fagerlund, A. & Granum, P. E. From soil to gut: PubMed DOI

Pivrncova, E., Bohm, J., Barton, V., Klanova, J. & Linhartova, P. B. Viable bacterial communities in freshly pumped human milk and their changes during cold storage conditions. 10.21203/rs.3.rs-4629897/v1 (2024). PubMed PMC

Cormontagne, D. et al. Bacillus cereus induces severe infections in preterm neonates: implication at the hospital and human milk bank level. PubMed DOI PMC

Hilliard, N. J., Schelonka, R. L. & Waites, K. B. Bacillus cereus bacteremia in a preterm neonate. PubMed DOI PMC

Zhang, W., Ma, C., Hu, L., Wang, L. & Xu, F. Late-onset sepsis in newborns caused by Bacillus cereus: a case report and literature review. PubMed DOI PMC

Jessberger, N., Dietrich, R., Granum, P. E. & Märtlbauer, E. The Bacillus cereus food infection as multifactorial process. PubMed DOI PMC

Tokieda, K., Morikawa, Y., Maeyama, K., Mori, K. & Ikeda, K. Clinical manifestations of PubMed DOI

Schoeni, J. L. & Lee Wong, A. C. Bacillus cereus food poisoning and its toxins. PubMed DOI

Senesi, S. & Ghelardi, E. Production secretion and biological activity of Bacillus cereus enterotoxins. PubMed PMC

Berthold-Pluta, A., Pluta, A. & Garbowska, M. The effect of selected factors on the survival of Bacillus cereus in the human Gastrointestinal tract. PubMed DOI

Bursová, Š. et al. Evaluation of Bacillus cereus growth in cooked rice. DOI

Fermanian, C., Fremy, J. M. & Claisse, M. Effect of temperature on the vegetative growth of type and field strains of Bacillus cereus. DOI

Finlay, W. J. J., Logan, N. A. & Sutherland, A. D. Bacillus cereus produces most emetic toxin at lower temperatures. PubMed DOI

Jurakova, V. et al. Gene expression and metabolic activity of Streptococcus mutans during exposure to dietary carbohydrates glucose, sucrose, lactose, and xylitol. PubMed DOI

Ceuppens, S. et al. Regulation of toxin production by Bacillus cereus and its food safety implications. PubMed DOI

Rowan, N. J. & Anderson, J. G. Maltodextrin stimulates growth of Bacillus cereus and synthesis of diarrheal enterotoxin in infant milk formulae. PubMed DOI PMC

Prince, C. & Kovac, J. Regulation of enterotoxins associated with Bacillus cereus sensu Lato toxicoinfection. PubMed PMC

Holesh, J. E., Aslam, S. & Martin, A. Physiology, carbohydrates. In PubMed

Suez, J., Korem, T., Zilberman-Schapira, G., Segal, E. & Elinav, E. Non-caloric artificial sweeteners and the microbiome: findings and challenges. PubMed DOI PMC

Ewels, P. A. et al. The nf-core framework for community-curated bioinformatics pipelines. PubMed DOI

Grüning, B. et al. Bioconda: sustainable and comprehensive software distribution for the life sciences. PubMed DOI PMC

da Leprevost, V. BioContainers: an open-source and community-driven framework for software standardization. PubMed DOI PMC

Liao, Y., Smyth, G. K. & Shi, W. FeatureCounts: an efficient general purpose program for assigning sequence reads to genomic features. PubMed DOI

Kanehisa, M. & Goto, S. KEGG: kyoto encyclopedia of genes and genomes. PubMed DOI PMC

Geistlinger, L., Csaba, G. & Zimmer, R. Bioconductor’s enrichmentbrowser: seamless navigation through combined results of set- & network-based enrichment analysis. PubMed DOI PMC

Izco, J. M., Tormo, M. & Jiménez-Flores, R. Development of a CE method to analyze organic acids in dairy products: application to study the metabolism of Heat-Shocked spores. PubMed DOI

Zhang, Y. et al. A new mechanism of carbon metabolism and acetic acid balance regulated by CcpA. PubMed DOI PMC

Flamholz, A., Noor, E., Bar-Even, A., Liebermeister, W. & Milo, R. Glycolytic strategy as a tradeoff between energy yield and protein cost. PubMed DOI PMC

Riemann, H. & Cliver, D. O.

Carlin, F. et al. Adaptation of Bacillus cereus, an ubiquitous worldwide-distributed foodborne pathogen, to a changing environment. DOI

Warda, A. K. et al. Linking Bacillus cereus genotypes and carbohydrate utilization capacity. PubMed DOI PMC

van Netten, P., van De Moosdijk, A., van Hoensel, P., Mossel, D. A. & Perales, I. Psychrotrophic strains of Bacillus cereus producing enterotoxin. PubMed DOI

Fermanian, C., Lapeyre, C., Fremy, J. M. & Claisse, M. Diarrhoeal toxin production at low temperature by selected strains of PubMed DOI

Ouhib, O., Clavel, T. & Schmitt, P. The production of Bacillus cereus enterotoxins is influenced by carbohydrate and growth rate. PubMed DOI

Chang, J. D. et al. Metabolic profiling reveals nutrient preferences during carbon utilization in Bacillus species. PubMed DOI PMC

Kazan, D., Çamurdan, A. & Hortaçsu, A. The effect of glucose concentration on the growth rate and some intracellular components of a recombinant E. coli culture. DOI

Sutherland, A. D. & Limond, A. M. Influence of pH and sugars on the growth and production of diarrhoeagenic toxin by PubMed DOI

Lindbäck, T., Økstad, O. A., Rishovd, A. L. & Kolstø, A. B. Insertional inactivation of HblC encoding the L2 component of Bacillus cereus ATCC 14579 haemolysin BL strongly reduces enterotoxigenic activity, but not the haemolytic activity against human erythrocytes. PubMed DOI

Outurquin, G. et al. Bacillus cereus strains from donor human milk and hospital environment: uncovering a putative common origin using comparative analysis of toxin and infra-red spectroscopy profiles. PubMed DOI PMC

Wang, Y. et al. Effect of temperature, pH, and Aw on cereulide synthesis and regulator genes transcription with respect to Bacillus cereus growth and cereulide production. PubMed DOI PMC