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

Summary 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 aure...

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Veröffentlicht in:Environmental microbiology reports 2011-06, Vol.3 (3), p.340-351
Hauptverfasser: Cretenet, Marina, Nouaille, Sébastien, Thouin, Jennifer, Rault, Lucie, Stenz, Ludwig, François, Patrice, Hennekinne, Jacques-Antoine, Piot, Michel, Maillard, Marie Bernadette, Fauquant, Jacques, Loubière, Pascal, Le Loir, Yves, Even, Sergine
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container_end_page 351
container_issue 3
container_start_page 340
container_title Environmental microbiology reports
container_volume 3
creator Cretenet, Marina
Nouaille, Sébastien
Thouin, Jennifer
Rault, Lucie
Stenz, Ludwig
François, Patrice
Hennekinne, Jacques-Antoine
Piot, Michel
Maillard, Marie Bernadette
Fauquant, Jacques
Loubière, Pascal
Le Loir, Yves
Even, Sergine
description Summary 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.
doi_str_mv 10.1111/j.1758-2229.2010.00230.x
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Remarkably, the agr system was downregulated by the presence of L. lactis, in part because of the decrease in pH. 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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. 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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.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><pmid>23761280</pmid><doi>10.1111/j.1758-2229.2010.00230.x</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0002-6836-2855</orcidid><orcidid>https://orcid.org/0000-0003-2038-098X</orcidid><orcidid>https://orcid.org/0000-0002-0355-1065</orcidid><orcidid>https://orcid.org/0000-0001-7950-7258</orcidid><orcidid>https://orcid.org/0000-0003-0772-7459</orcidid><oa>free_for_read</oa></addata></record>
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subjects Acidification
Bacteriology
Biochemistry, Molecular Biology
Carbohydrates
Cell division
Cheese
Chemical and Process Engineering
Cold
Dairy products
Dehydrogenases
Dominant species
Engineering Sciences
Enterotoxins
Food contamination
Food engineering
Food poisoning
Food safety
Gene expression
Genomics
Kinases
Lactococcus lactis
Life Sciences
Metabolism
Microbiology and Parasitology
Milk
Physiology
Proteins
Proteomics
Redox potential
Risk assessment
Risk management
Staphylococcus aureus
Transcriptomics
Virulence
title Staphylococcus aureus virulence and metabolism are dramatically affected by Lactococcus lactis in cheese matrix
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