Lactoferrin-based food supplements trigger toxin production of enteropathogenic Bacillus cereus

Frontiers in Microbiology · 3 authors, 2 centres

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The central finding was that lactoferrin exposure increased the production of the enterotoxin NheB in the majority of strains.

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Researchers tested 31 strains, including reference strains, and found that exposure to physiological concentrations of lactoferrin led to increased secretion of the enterotoxin component NheB in 23 strains. The enhancement was observed with products containing pure bovine lactoferrin. Transcriptomic analysis of a responsive strain revealed that lactoferrin exposure induced a broad transcriptional response distinct from iron deficiency, including upregulation of genes for sporulation and nutrient uptake, but downregulation of the PlcR-PapR quorum-sensing system. The findings suggest that despite lactoferrin's known antimicrobial properties, it may inadvertently promote enterotoxin production in certain pathogenic bacteria, with implications for food safety.

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other

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food science

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ORIGINAL PAPER

PMC10646309

Lactoferrin-based food supplements trigger toxin production of enteropathogenic Bacillus cereus

Frontiers in Microbiology

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ABSTRACT

Abstract Lactoferrin is an iron-binding glycoprotein exhibiting antibacterial, antiviral, antifungal, antiparasitic, antiinflammatory, antianaemic and anticarcinogenic properties. While its inhibitory effects against bacterial pathogens are well investigated, little is known about its influence on the production and/or mode of action of bacterial toxins. Thus, the present study aimed to determine the impact of food supplements based on bovine lactoferrin on Bacillus cereus enterotoxin production. First, strain-specific growth inhibition of three representative isolates was observed in minimal medium with 1 or 10 mg/mL of a lactoferrin-based food supplement, designated as product no. 1. Growth inhibition did not result from iron deficiency. In contrast to that, all three strains showed increased amounts of enterotoxin component NheB in the supernatant, which corresponded with cytotoxicity. Moreover, lactoferrin product no. 1 enhanced NheB production of further 20 out of 28 B. cereus and Bacillus thuringiensis strains. These findings again suggested a strain-specific response toward lactoferrin. Product-specific differences also became apparent comparing the influence of further six products on highly responsive strain INRA C3. Highest toxin titres were detected after exposure to products no. 7, 1 and 2, containing no ingredients except pure bovine lactoferrin. INRA C3 was also used to determine the transcriptional response toward lactoferrin exposure via RNA sequencing. As control, iron-free medium was also included, which resulted in down-regulation of eight genes, mainly involved in amino acid metabolism, and in up-regulation of 52 genes, mainly involved in iron transport, uptake and utilization. In contrast to that, 153 genes were down-regulated in the presence of lactoferrin, including genes involved in flagellar assembly, motility, chemotaxis and sporulation as well as genes encoding regulatory proteins, transporters, heat and cold shock proteins and virulence factors. Furthermore, 125 genes were up-regulated in the presence of lactoferrin, comprising genes involved in sporulation and germination, nutrient uptake, iron transport and utilization, and resistance. In summary, lactoferrin exposure of B. cereus strain-specifically triggers an extensive transcriptional response that considerably exceeds the response toward iron deficiency and, despite down-regulation of various genes belonging to the PlcR-regulon, ultimately leads to an increased level of secreted enterotoxin by a mechanism, which has yet to be elucidated. Keywords: food additive, lactoferrin, Bacillus cereus , non-hemolytic enterotoxin, transcriptome, quorum sensing

CITATION EXPORT

Clara-Sophie Jugert, Andrea Didier, Nadja Jessberger. Lactoferrin-based food supplements trigger toxin production of enteropathogenic Bacillus cereus. Frontiers in Microbiology. (2023). https://doi.org/10.3389/fmicb.2023.1284473

AUTHORS

3 · 2 CENTRES

Clara-Sophie Jugert, Andrea Didier, Nadja Jessberger

1Department of Veterinary Sciences, Faculty of Veterinary Medicine, Ludwig-Maximilians-Universität München, Oberschleißheim, Germany
2Institute for Food Quality and Food Safety, University of Veterinary Medicine Hannover, Hannover, Germany