Staphylococcus aureus virulence and metabolism are dramatically affected by Lactococcus lactis in cheese matrix

Abstract

In complex environments such as cheeses, the lack of relevant information on the physiology and virulence expression of pathogenic bacteria and the impact of endogenous microbiota has hindered progress in risk assessment and control. Here, we investigated the behaviour of Staphylococcus aureus, a major foodborne pathogen, in a cheese matrix, either alone or in the presence of Lactococcus lactis, as a dominant species of cheese ecosystems. The dynamics of S. aureus was explored in situ by coupling a microbiological and, for the first time, a transcriptomic approach. Lactococcus lactis affected the carbohydrate and nitrogen metabolisms and the stress response of S. aureus by acidifying, proteolysing and decreasing the redox potential of the cheese matrix. Enterotoxin expression was positively or negatively modulated by both L. lactis and the cheese matrix itself, depending on the enterotoxin type. Among the main enterotoxins involved in staphylococcal food poisoning, sea expression was slightly favoured in the presence of L. lactis, whereas a strong repression of sec4 was observed in cheese matrix, even in the absence of L. lactis, and correlated with a reduced saeRS expression. Remarkably, the agr system was downregulated by the presence of L. lactis, in part because of the decrease in pH. This study highlights the intimate link between environment, metabolism and virulence, as illustrated by the influence of the cheese matrix context, including the presence of L. lactis, on two major virulence regulators, the agr system and saeRS.

The formation ofStaphylococcus aureusenterotoxin in food environments and advances in risk assessment

“…In fact, recently reported data have shown that there are significant differences in the behavior of bacteria in the planktonic state and in actual food matrices. [6][7][8] Knowledge about the effects of critical food-related factors on microbial responses such as virulence gene expression, lag phase duration, growth rate and extracellular virulence formation, will not only aid in the prevention of foodborne diseases, but also enable the advancement of quantitative microbial risk assessment (QMRA). A risk assessment consists of four steps: (1) hazard identification, (2) hazard characterization, (3) exposure assessment and (4) risk characterization.…”

Expression of toxic shock syndrome toxin-1 gene of Staphylococcus aureus in milk: Proof of concept

“…However, Nouaille et al (2014) established the ability of Lactococcus lactis, a lactic acid bacterium widely used in the dairy industry, to down-regulate a major staphylococcal virulence regulator, the agr system, and, as a consequence, agr-controlled toxins. The agr system relies on at least two general properties of LAB: their ability to decrease both pH (Cretenet et al, 2011) and redox potential via oxygen-independent mechanisms (Nouaille et al, 2014).…”

“…Different types of milk that had previously tested negative for S. aureus have been inoculated with an average of 2.4×10 4 CFUmL -1 of the above strain. The milk samples tested were pasteurized and UHT 1.6 % fat milk obtained from retail.…”

Production of staphylococcal enterotoxins in food

“…Cretenet i wsp. (8) prowadzili hodowle szczepu S. aureus MW2 posiadającego geny enterotoksyn sea, sec, seg, seh, sel oraz sek wraz ze szczepem Lactococcus lactis w podłożu mikrobiologicznym i modelowym serze. Stwierdzono, iż SEA była wydzielana w serze na poziomie podobnym jak w pożywce mikrobiologicznej, w serze natomiast nie stwierdzono obecności SEC.…”

“…Spośród szerokiego asortymentu produktów spożywczych, które były wiązane z przypadkami gronkowcowych zatruć pokarmowych do tej pory zbadano mleko oraz niektóre rodzaje serów i wyrobów mięsnych. Prace te przeprowadzono na niewielkiej liczbie szczepów S. aureus i dotyczyły jedynie wybranych enterotoksyn gronkowcowych (8,17,24,47,49), w większości przypadków SEA-SEE. Zgodnie z oceną wielu autorów, ryzyko wytworzenia enterotoksyn, głównie SEC, w mleku i produktach mlecznych jest bardzo niskie i w świetle tych stwierdzeń obecność S. aureus w tego rodzaju żywności nie stanowiłaby istotnego zagrożenia zdrowia konsumenta.…”