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...
Gespeichert in:
Veröffentlicht in: | Environmental microbiology reports 2011-06, Vol.3 (3), p.340-351 |
---|---|
Hauptverfasser: | , , , , , , , , , , , , |
Format: | Artikel |
Sprache: | eng |
Schlagworte: | |
Online-Zugang: | Volltext |
Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
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 |
format | Article |
fullrecord | <record><control><sourceid>proquest_hal_p</sourceid><recordid>TN_cdi_hal_primary_oai_HAL_hal_02291148v1</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>3092267120</sourcerecordid><originalsourceid>FETCH-LOGICAL-c5850-4e3169cc34eb3de03b3bb3d717f9a4f7ebbc01ad8da6491a51c32937d8c8c6a53</originalsourceid><addsrcrecordid>eNqNkUtv1DAUhSMEoqXwF5AlNrDI4EcSOwsWpSrTSgNIBcTSunFuNB6cZLCTMvn3dZp2hFjhzT26_s714yQJYXTF4nq_WzGZq5RzXq44jV1KuaCrw5Pk9Ljx9C99krwIYUdpkZWUP09OuJAF44qeJv23AfbbyfWmN2YMBEaPsdxaPzrsDBLoatLiAFXvbGgJeCS1hxYGa8C5iUDToBmwJtVENmCGx0EuahuI7YjZIgYk0eLt4WXyrAEX8NVDPUt-fLr8fnGVbr6ury_ON6nJVU7TDAUrSmNEhpWokYpKVFFIJpsSskZiVRnKoFY1xDcxyJkRvBSyVkaZAnJxlrxb5m7B6b23LfhJ92D11flGzz0av4WxTN2yyL5d2L3vf48YBt3aYNA56LAfg2ZZJoRitJQRffMPuutH38WXaEFLzgvJOI2UWijj-xA8NscbMKrnAPVOz9noORs9B6jvA9SHaH39cMBYtVgfjY-JReDDAvyxDqf_HqwvP19nUUV_uvhtGPBw9IP_pQspZK5_flnrdck_3kh5o9fiDrDruLY</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>3092267120</pqid></control><display><type>article</type><title>Staphylococcus aureus virulence and metabolism are dramatically affected by Lactococcus lactis in cheese matrix</title><source>Wiley Online Library Journals Frontfile Complete</source><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</creator><creatorcontrib>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</creatorcontrib><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.</description><identifier>ISSN: 1758-2229</identifier><identifier>EISSN: 1758-2229</identifier><identifier>DOI: 10.1111/j.1758-2229.2010.00230.x</identifier><identifier>PMID: 23761280</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Publishing Ltd</publisher><subject>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</subject><ispartof>Environmental microbiology reports, 2011-06, Vol.3 (3), p.340-351</ispartof><rights>2011 Society for Applied Microbiology and Blackwell Publishing Ltd</rights><rights>2011 Society for Applied Microbiology and Blackwell Publishing Ltd.</rights><rights>Copyright John Wiley & Sons, Inc. 2011</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5850-4e3169cc34eb3de03b3bb3d717f9a4f7ebbc01ad8da6491a51c32937d8c8c6a53</citedby><cites>FETCH-LOGICAL-c5850-4e3169cc34eb3de03b3bb3d717f9a4f7ebbc01ad8da6491a51c32937d8c8c6a53</cites><orcidid>0000-0002-6836-2855 ; 0000-0003-2038-098X ; 0000-0002-0355-1065 ; 0000-0001-7950-7258 ; 0000-0003-0772-7459</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fj.1758-2229.2010.00230.x$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fj.1758-2229.2010.00230.x$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,776,780,881,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23761280$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://normandie-univ.hal.science/hal-02291148$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Cretenet, Marina</creatorcontrib><creatorcontrib>Nouaille, Sébastien</creatorcontrib><creatorcontrib>Thouin, Jennifer</creatorcontrib><creatorcontrib>Rault, Lucie</creatorcontrib><creatorcontrib>Stenz, Ludwig</creatorcontrib><creatorcontrib>François, Patrice</creatorcontrib><creatorcontrib>Hennekinne, Jacques-Antoine</creatorcontrib><creatorcontrib>Piot, Michel</creatorcontrib><creatorcontrib>Maillard, Marie Bernadette</creatorcontrib><creatorcontrib>Fauquant, Jacques</creatorcontrib><creatorcontrib>Loubière, Pascal</creatorcontrib><creatorcontrib>Le Loir, Yves</creatorcontrib><creatorcontrib>Even, Sergine</creatorcontrib><title>Staphylococcus aureus virulence and metabolism are dramatically affected by Lactococcus lactis in cheese matrix</title><title>Environmental microbiology reports</title><addtitle>Environ Microbiol Rep</addtitle><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.</description><subject>Acidification</subject><subject>Bacteriology</subject><subject>Biochemistry, Molecular Biology</subject><subject>Carbohydrates</subject><subject>Cell division</subject><subject>Cheese</subject><subject>Chemical and Process Engineering</subject><subject>Cold</subject><subject>Dairy products</subject><subject>Dehydrogenases</subject><subject>Dominant species</subject><subject>Engineering Sciences</subject><subject>Enterotoxins</subject><subject>Food contamination</subject><subject>Food engineering</subject><subject>Food poisoning</subject><subject>Food safety</subject><subject>Gene expression</subject><subject>Genomics</subject><subject>Kinases</subject><subject>Lactococcus lactis</subject><subject>Life Sciences</subject><subject>Metabolism</subject><subject>Microbiology and Parasitology</subject><subject>Milk</subject><subject>Physiology</subject><subject>Proteins</subject><subject>Proteomics</subject><subject>Redox potential</subject><subject>Risk assessment</subject><subject>Risk management</subject><subject>Staphylococcus aureus</subject><subject>Transcriptomics</subject><subject>Virulence</subject><issn>1758-2229</issn><issn>1758-2229</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><recordid>eNqNkUtv1DAUhSMEoqXwF5AlNrDI4EcSOwsWpSrTSgNIBcTSunFuNB6cZLCTMvn3dZp2hFjhzT26_s714yQJYXTF4nq_WzGZq5RzXq44jV1KuaCrw5Pk9Ljx9C99krwIYUdpkZWUP09OuJAF44qeJv23AfbbyfWmN2YMBEaPsdxaPzrsDBLoatLiAFXvbGgJeCS1hxYGa8C5iUDToBmwJtVENmCGx0EuahuI7YjZIgYk0eLt4WXyrAEX8NVDPUt-fLr8fnGVbr6ury_ON6nJVU7TDAUrSmNEhpWokYpKVFFIJpsSskZiVRnKoFY1xDcxyJkRvBSyVkaZAnJxlrxb5m7B6b23LfhJ92D11flGzz0av4WxTN2yyL5d2L3vf48YBt3aYNA56LAfg2ZZJoRitJQRffMPuutH38WXaEFLzgvJOI2UWijj-xA8NscbMKrnAPVOz9noORs9B6jvA9SHaH39cMBYtVgfjY-JReDDAvyxDqf_HqwvP19nUUV_uvhtGPBw9IP_pQspZK5_flnrdck_3kh5o9fiDrDruLY</recordid><startdate>201106</startdate><enddate>201106</enddate><creator>Cretenet, Marina</creator><creator>Nouaille, Sébastien</creator><creator>Thouin, Jennifer</creator><creator>Rault, Lucie</creator><creator>Stenz, Ludwig</creator><creator>François, Patrice</creator><creator>Hennekinne, Jacques-Antoine</creator><creator>Piot, Michel</creator><creator>Maillard, Marie Bernadette</creator><creator>Fauquant, Jacques</creator><creator>Loubière, Pascal</creator><creator>Le Loir, Yves</creator><creator>Even, Sergine</creator><general>Blackwell Publishing Ltd</general><general>John Wiley & Sons, Inc</general><general>Wiley</general><scope>BSCLL</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><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></search><sort><creationdate>201106</creationdate><title>Staphylococcus aureus virulence and metabolism are dramatically affected by Lactococcus lactis in cheese matrix</title><author>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</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5850-4e3169cc34eb3de03b3bb3d717f9a4f7ebbc01ad8da6491a51c32937d8c8c6a53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Acidification</topic><topic>Bacteriology</topic><topic>Biochemistry, Molecular Biology</topic><topic>Carbohydrates</topic><topic>Cell division</topic><topic>Cheese</topic><topic>Chemical and Process Engineering</topic><topic>Cold</topic><topic>Dairy products</topic><topic>Dehydrogenases</topic><topic>Dominant species</topic><topic>Engineering Sciences</topic><topic>Enterotoxins</topic><topic>Food contamination</topic><topic>Food engineering</topic><topic>Food poisoning</topic><topic>Food safety</topic><topic>Gene expression</topic><topic>Genomics</topic><topic>Kinases</topic><topic>Lactococcus lactis</topic><topic>Life Sciences</topic><topic>Metabolism</topic><topic>Microbiology and Parasitology</topic><topic>Milk</topic><topic>Physiology</topic><topic>Proteins</topic><topic>Proteomics</topic><topic>Redox potential</topic><topic>Risk assessment</topic><topic>Risk management</topic><topic>Staphylococcus aureus</topic><topic>Transcriptomics</topic><topic>Virulence</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Cretenet, Marina</creatorcontrib><creatorcontrib>Nouaille, Sébastien</creatorcontrib><creatorcontrib>Thouin, Jennifer</creatorcontrib><creatorcontrib>Rault, Lucie</creatorcontrib><creatorcontrib>Stenz, Ludwig</creatorcontrib><creatorcontrib>François, Patrice</creatorcontrib><creatorcontrib>Hennekinne, Jacques-Antoine</creatorcontrib><creatorcontrib>Piot, Michel</creatorcontrib><creatorcontrib>Maillard, Marie Bernadette</creatorcontrib><creatorcontrib>Fauquant, Jacques</creatorcontrib><creatorcontrib>Loubière, Pascal</creatorcontrib><creatorcontrib>Le Loir, Yves</creatorcontrib><creatorcontrib>Even, Sergine</creatorcontrib><collection>Istex</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><jtitle>Environmental microbiology reports</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Cretenet, Marina</au><au>Nouaille, Sébastien</au><au>Thouin, Jennifer</au><au>Rault, Lucie</au><au>Stenz, Ludwig</au><au>François, Patrice</au><au>Hennekinne, Jacques-Antoine</au><au>Piot, Michel</au><au>Maillard, Marie Bernadette</au><au>Fauquant, Jacques</au><au>Loubière, Pascal</au><au>Le Loir, Yves</au><au>Even, Sergine</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Staphylococcus aureus virulence and metabolism are dramatically affected by Lactococcus lactis in cheese matrix</atitle><jtitle>Environmental microbiology reports</jtitle><addtitle>Environ Microbiol Rep</addtitle><date>2011-06</date><risdate>2011</risdate><volume>3</volume><issue>3</issue><spage>340</spage><epage>351</epage><pages>340-351</pages><issn>1758-2229</issn><eissn>1758-2229</eissn><abstract>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.</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> |
fulltext | fulltext |
identifier | ISSN: 1758-2229 |
ispartof | Environmental microbiology reports, 2011-06, Vol.3 (3), p.340-351 |
issn | 1758-2229 1758-2229 |
language | eng |
recordid | cdi_hal_primary_oai_HAL_hal_02291148v1 |
source | Wiley Online Library Journals Frontfile Complete |
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 |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-19T09%3A07%3A53IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_hal_p&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Staphylococcus%20aureus%20virulence%20and%20metabolism%20are%20dramatically%20affected%20by%20Lactococcus%20lactis%20in%20cheese%20matrix&rft.jtitle=Environmental%20microbiology%20reports&rft.au=Cretenet,%20Marina&rft.date=2011-06&rft.volume=3&rft.issue=3&rft.spage=340&rft.epage=351&rft.pages=340-351&rft.issn=1758-2229&rft.eissn=1758-2229&rft_id=info:doi/10.1111/j.1758-2229.2010.00230.x&rft_dat=%3Cproquest_hal_p%3E3092267120%3C/proquest_hal_p%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=3092267120&rft_id=info:pmid/23761280&rfr_iscdi=true |