Staphylococcal Enterotoxins: Description and Importance in Food

Abstract

Staphylococcus aureus stands out as one of the most virulent pathogens in the genus Staphylococcus. This characteristic is due to its ability to produce a wide variety of staphylococcal enterotoxins (SEs) and exotoxins, which in turn can cause staphylococcal food poisoning (SFP), clinical syndromes such as skin infections, inflammation, pneumonia, and sepsis, in addition to being associated with the development of inflammation in the mammary glands of dairy cattle, which results in chronic mastitis and cell necrosis. SEs are small globular proteins that combine superantigenic and emetic activities; they are resistant to heat, low temperatures, and proteolytic enzymes and are tolerant to a wide pH range. More than 24 SE genes have been well described (SEA-SEE, SEG, SEH, SEI, SEJ, SElK, SElL, SElM, SElN, SElO, SElP, SElQ, SElR, SElS, SElT, SElU, SElV, SElW, SElX, SElY, and SElZ), being a part of different SFP outbreaks, clinical cases, and isolated animal strains. In recent years, new genes (sel26, sel27, sel28, sel31, sel32, and sel33) from SEs have been described, as well as two variants (seh-2p and ses-3p) resulting in a total of thirty-three genes from Ses, including the nine variants that are still in the process of genetic and molecular structure evaluation. SEs are encoded by genes that are located in mobile genetic elements, such as plasmids, prophages, pathogenicity islands, and the enterotoxin gene cluster (egc), and housed in the genomic island of S. aureus. Both classical SEs and SE-like toxins (SEls) share phylogenetic relationships, structure, function, and sequence homology, which are characteristics for the production of new SEs through recombination processes. Due to the epidemiological importance of SEs, their rapid assessment and detection have been crucial for food security and public health; for this reason, different methods of identification of SEs have been developed, such as liquid chromatography coupled with high-resolution mass spectrometry (LC-HRMS), molecular methods, and whole-genome sequencing; providing the diagnosis of SEs and a better understanding of the occurrence, spread, and eradication of SEs. This review provides scientific information on the enterotoxins produced by S. aureus, such as structural characteristics, genetic organization, regulatory mechanisms, superantigen activity, mechanisms of action used by SEs at the time of interaction with the immune system, methods of detection of SEs, and recent biocontrol techniques used in food.

Keywords: Staphylococcus aureus; enterotoxins; genes; staphylococcal food poisoning.

Figure 1

Structural characteristics of SEs and Sels: group I (SElX, SElY), group II (SEB, SEC, SEG, SElU, and SElW), group III (SEA, SED, SEE, SEH, SElJ, SElN, and SElP), and group V (SEI, SElK, SElL, SElM, SElQ, SElT, and SElV). Group I lacks the cystine emetic loop and contains only one low-density major histocompatibility class (MHC) II binding site; group II contains a cystine loop with a sequence of 10 to 19 amino acids, the MHC II site of the α chain, and the Vβ-TCR binding site; group III contains the nine-amino acid cystine loop of the MHC II binding sites (α and β) and the β chain-dependent Zn²⁺ MHC II binding site; group V contains MHC II (α and β) but lacks the cystine loop. Created with BioRender.com.

Figure 2

SE superantigens bind directly to the β chain of the TCR (T-cell receptor) molecule, interacting with T-cell scaffold regions and with MHC II (Signal 1) on the surface of APCs (antigen-presenting cells), resulting in the activation of polyclonal T cells (Signal 2) and overproduction of T-cell cytokines, including IL-4, IL-5 and IL-13 (Signal 3); inducing changes in cellular complexity through the apoptotic process. Created with BioRender.com.