Role of respiratory NADH oxidation in the regulation of Staphylococcus aureus virulence
The success of Staphylococcus aureus as a pathogen is due to its capability of fine‐tuning its cellular physiology to meet the challenges presented by diverse environments, which allows it to colonize multiple niches within a single vertebrate host. Elucidating the roles of energy‐yielding metabolic...
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| creator | Schurig‐Briccio, Lici A Parraga Solorzano, Paola K Lencina, Andrea M Radin, Jana N Chen, Grischa Y Sauer, John‐Demian Kehl‐Fie, Thomas E Gennis, Robert B |
| description | The success of
Staphylococcus aureus
as a pathogen is due to its capability of fine‐tuning its cellular physiology to meet the challenges presented by diverse environments, which allows it to colonize multiple niches within a single vertebrate host. Elucidating the roles of energy‐yielding metabolic pathways could uncover attractive therapeutic strategies and targets. In this work, we seek to determine the effects of disabling NADH‐dependent aerobic respiration on the physiology of
S. aureus
. Differing from many pathogens,
S. aureus
has two type‐2 respiratory NADH dehydrogenases (NDH‐2s) but lacks the respiratory ion‐pumping NDHs. Here, we show that the NDH‐2s, individually or together, are not essential either for respiration or growth. Nevertheless, their absence eliminates biofilm formation, production of α‐toxin, and reduces the ability to colonize specific organs in a mouse model of systemic infection. Moreover, we demonstrate that the reason behind these phenotypes is the alteration of the fatty acid metabolism. Importantly, the SaeRS two‐component system, which responds to fatty acids regulation, is responsible for the link between NADH‐dependent respiration and virulence in
S. aureus
.
Synopsis
NADH‐dependent respiration regulates fatty acid metabolism in
Staphylococcus aureus
. Changes in the concentration of free fatty acids are sensed by the SaeRS two‐component system, which controls virulence.
NdhC is vital for α‐toxin production, whereas NdhC and NdhF are critical for biofilm formation and systemic infection.
NdhC‐deficient strains accumulate free fatty acids in the stationary phase.
SaeRS responds to changes in fatty acid metabolism, thereby affecting α‐toxin production and biofilm formation.
Graphical Abstract
NADH‐dependent respiration regulates fatty acid metabolism in
Staphylococcus aureus
. Changes in the concentration of free fatty acids are sensed by the SaeRS two‐component system, which controls virulence. |
| doi_str_mv | 10.15252/embr.201845832 |
| format | Article |
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Staphylococcus aureus
as a pathogen is due to its capability of fine‐tuning its cellular physiology to meet the challenges presented by diverse environments, which allows it to colonize multiple niches within a single vertebrate host. Elucidating the roles of energy‐yielding metabolic pathways could uncover attractive therapeutic strategies and targets. In this work, we seek to determine the effects of disabling NADH‐dependent aerobic respiration on the physiology of
S. aureus
. Differing from many pathogens,
S. aureus
has two type‐2 respiratory NADH dehydrogenases (NDH‐2s) but lacks the respiratory ion‐pumping NDHs. Here, we show that the NDH‐2s, individually or together, are not essential either for respiration or growth. Nevertheless, their absence eliminates biofilm formation, production of α‐toxin, and reduces the ability to colonize specific organs in a mouse model of systemic infection. Moreover, we demonstrate that the reason behind these phenotypes is the alteration of the fatty acid metabolism. Importantly, the SaeRS two‐component system, which responds to fatty acids regulation, is responsible for the link between NADH‐dependent respiration and virulence in
S. aureus
.
Synopsis
NADH‐dependent respiration regulates fatty acid metabolism in
Staphylococcus aureus
. Changes in the concentration of free fatty acids are sensed by the SaeRS two‐component system, which controls virulence.
NdhC is vital for α‐toxin production, whereas NdhC and NdhF are critical for biofilm formation and systemic infection.
NdhC‐deficient strains accumulate free fatty acids in the stationary phase.
SaeRS responds to changes in fatty acid metabolism, thereby affecting α‐toxin production and biofilm formation.
Graphical Abstract
NADH‐dependent respiration regulates fatty acid metabolism in
Staphylococcus aureus
. Changes in the concentration of free fatty acids are sensed by the SaeRS two‐component system, which controls virulence.</description><identifier>ISSN: 1469-221X</identifier><identifier>EISSN: 1469-3178</identifier><identifier>DOI: 10.15252/embr.201845832</identifier><identifier>PMID: 32202364</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>Aerobic respiration ; Animals ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Biofilms ; Disseminated infection ; EMBO21 ; EMBO23 ; Fatty acids ; Gene Expression Regulation, Bacterial ; Metabolic pathways ; Metabolism ; Mice ; NAD ; NADH ; NADH dehydrogenase ; NADH/NAD ; Nicotinamide adenine dinucleotide ; Organs ; Oxidation ; Pathogens ; Phenotypes ; Physiology ; Respiration ; respiratory chain ; Staphylococcal Infections ; Staphylococcus aureus ; Staphylococcus aureus - genetics ; Stationary phase ; Toxins ; two‐component system ; Vertebrates ; Virulence ; α-Toxin</subject><ispartof>EMBO reports, 2020-05, Vol.21 (5), p.e45832-n/a</ispartof><rights>The Author(s) 2020</rights><rights>2020 The Authors</rights><rights>2020 The Authors.</rights><rights>2020 EMBO</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4642-31572504480049c4a49c7763a6d8998b02aa180c42cf78443c06e2cc4deca7aa3</citedby><cites>FETCH-LOGICAL-c4642-31572504480049c4a49c7763a6d8998b02aa180c42cf78443c06e2cc4deca7aa3</cites><orcidid>0000-0001-9367-794X ; 0000-0002-5514-2298 ; 0000-0001-7933-6460 ; 0000-0002-3805-6945</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7202225/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7202225/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,1411,1427,27901,27902,41096,42165,45550,45551,46384,46808,51551,53766,53768</link.rule.ids><linktorsrc>$$Uhttps://doi.org/10.15252/embr.201845832$$EView_record_in_Springer_Nature$$FView_record_in_$$GSpringer_Nature</linktorsrc><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32202364$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Schurig‐Briccio, Lici A</creatorcontrib><creatorcontrib>Parraga Solorzano, Paola K</creatorcontrib><creatorcontrib>Lencina, Andrea M</creatorcontrib><creatorcontrib>Radin, Jana N</creatorcontrib><creatorcontrib>Chen, Grischa Y</creatorcontrib><creatorcontrib>Sauer, John‐Demian</creatorcontrib><creatorcontrib>Kehl‐Fie, Thomas E</creatorcontrib><creatorcontrib>Gennis, Robert B</creatorcontrib><title>Role of respiratory NADH oxidation in the regulation of Staphylococcus aureus virulence</title><title>EMBO reports</title><addtitle>EMBO Rep</addtitle><addtitle>EMBO Rep</addtitle><description>The success of
Staphylococcus aureus
as a pathogen is due to its capability of fine‐tuning its cellular physiology to meet the challenges presented by diverse environments, which allows it to colonize multiple niches within a single vertebrate host. Elucidating the roles of energy‐yielding metabolic pathways could uncover attractive therapeutic strategies and targets. In this work, we seek to determine the effects of disabling NADH‐dependent aerobic respiration on the physiology of
S. aureus
. Differing from many pathogens,
S. aureus
has two type‐2 respiratory NADH dehydrogenases (NDH‐2s) but lacks the respiratory ion‐pumping NDHs. Here, we show that the NDH‐2s, individually or together, are not essential either for respiration or growth. Nevertheless, their absence eliminates biofilm formation, production of α‐toxin, and reduces the ability to colonize specific organs in a mouse model of systemic infection. Moreover, we demonstrate that the reason behind these phenotypes is the alteration of the fatty acid metabolism. Importantly, the SaeRS two‐component system, which responds to fatty acids regulation, is responsible for the link between NADH‐dependent respiration and virulence in
S. aureus
.
Synopsis
NADH‐dependent respiration regulates fatty acid metabolism in
Staphylococcus aureus
. Changes in the concentration of free fatty acids are sensed by the SaeRS two‐component system, which controls virulence.
NdhC is vital for α‐toxin production, whereas NdhC and NdhF are critical for biofilm formation and systemic infection.
NdhC‐deficient strains accumulate free fatty acids in the stationary phase.
SaeRS responds to changes in fatty acid metabolism, thereby affecting α‐toxin production and biofilm formation.
Graphical Abstract
NADH‐dependent respiration regulates fatty acid metabolism in
Staphylococcus aureus
. Changes in the concentration of free fatty acids are sensed by the SaeRS two‐component system, which controls virulence.</description><subject>Aerobic respiration</subject><subject>Animals</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>Biofilms</subject><subject>Disseminated infection</subject><subject>EMBO21</subject><subject>EMBO23</subject><subject>Fatty acids</subject><subject>Gene Expression Regulation, Bacterial</subject><subject>Metabolic pathways</subject><subject>Metabolism</subject><subject>Mice</subject><subject>NAD</subject><subject>NADH</subject><subject>NADH dehydrogenase</subject><subject>NADH/NAD</subject><subject>Nicotinamide adenine dinucleotide</subject><subject>Organs</subject><subject>Oxidation</subject><subject>Pathogens</subject><subject>Phenotypes</subject><subject>Physiology</subject><subject>Respiration</subject><subject>respiratory chain</subject><subject>Staphylococcal Infections</subject><subject>Staphylococcus aureus</subject><subject>Staphylococcus aureus - genetics</subject><subject>Stationary phase</subject><subject>Toxins</subject><subject>two‐component system</subject><subject>Vertebrates</subject><subject>Virulence</subject><subject>α-Toxin</subject><issn>1469-221X</issn><issn>1469-3178</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkcFPFDEUxhuiAUTP3sgkXrgstK_ttMPBBBDFBCUBjd6abvftbkl3urQz6P73Fmdd0cR46Wva3_vyvfcR8pLRQyZBwhEuxukQKNNCag5bZJeJuhlxpvST9R2Afd0hz3K-pZTKRultssMBKPBa7JIv1zFgFadVwrz0yXYxraqPJ28uqvjdT2znY1v5turmWIhZH4aXwt90djlfheiic32ubJ-wlHuf-oCtw-fk6dSGjC_WdY98fnv-6exidHn17v3ZyeXIiVpAMSoVSCqEplQ0TthyKFVzW0900-gxBWuZpk6AmyotBHe0RnBOTNBZZS3fI68H3WU_XuDEYdslG8wy-YVNKxOtN3_-tH5uZvHeqLIBAFkEDtYCKd71mDuz8NlhCLbF2GcDXJflciHrgr76C72NfWrLeIVqtARQ7EHwaKBcijknnG7MMGp-hmYeQjOb0ErH_uMZNvyvlApwPADffMDV__TM-YfT68fqdGjOpa-dYfrt-l-GfgAsJbRD</recordid><startdate>20200506</startdate><enddate>20200506</enddate><creator>Schurig‐Briccio, Lici A</creator><creator>Parraga Solorzano, Paola K</creator><creator>Lencina, Andrea M</creator><creator>Radin, Jana N</creator><creator>Chen, Grischa Y</creator><creator>Sauer, John‐Demian</creator><creator>Kehl‐Fie, Thomas E</creator><creator>Gennis, Robert B</creator><general>Nature Publishing Group UK</general><general>Springer Nature B.V</general><general>John Wiley and Sons Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7T5</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>K9.</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-9367-794X</orcidid><orcidid>https://orcid.org/0000-0002-5514-2298</orcidid><orcidid>https://orcid.org/0000-0001-7933-6460</orcidid><orcidid>https://orcid.org/0000-0002-3805-6945</orcidid></search><sort><creationdate>20200506</creationdate><title>Role of respiratory NADH oxidation in the regulation of Staphylococcus aureus virulence</title><author>Schurig‐Briccio, Lici A ; Parraga Solorzano, Paola K ; Lencina, Andrea M ; Radin, Jana N ; Chen, Grischa Y ; Sauer, John‐Demian ; Kehl‐Fie, Thomas E ; Gennis, Robert B</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4642-31572504480049c4a49c7763a6d8998b02aa180c42cf78443c06e2cc4deca7aa3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Aerobic respiration</topic><topic>Animals</topic><topic>Bacterial Proteins - genetics</topic><topic>Bacterial Proteins - metabolism</topic><topic>Biofilms</topic><topic>Disseminated infection</topic><topic>EMBO21</topic><topic>EMBO23</topic><topic>Fatty acids</topic><topic>Gene Expression Regulation, Bacterial</topic><topic>Metabolic pathways</topic><topic>Metabolism</topic><topic>Mice</topic><topic>NAD</topic><topic>NADH</topic><topic>NADH dehydrogenase</topic><topic>NADH/NAD</topic><topic>Nicotinamide adenine dinucleotide</topic><topic>Organs</topic><topic>Oxidation</topic><topic>Pathogens</topic><topic>Phenotypes</topic><topic>Physiology</topic><topic>Respiration</topic><topic>respiratory chain</topic><topic>Staphylococcal Infections</topic><topic>Staphylococcus aureus</topic><topic>Staphylococcus aureus - genetics</topic><topic>Stationary phase</topic><topic>Toxins</topic><topic>two‐component system</topic><topic>Vertebrates</topic><topic>Virulence</topic><topic>α-Toxin</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Schurig‐Briccio, Lici A</creatorcontrib><creatorcontrib>Parraga Solorzano, Paola K</creatorcontrib><creatorcontrib>Lencina, Andrea M</creatorcontrib><creatorcontrib>Radin, Jana N</creatorcontrib><creatorcontrib>Chen, Grischa Y</creatorcontrib><creatorcontrib>Sauer, John‐Demian</creatorcontrib><creatorcontrib>Kehl‐Fie, Thomas E</creatorcontrib><creatorcontrib>Gennis, Robert B</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Immunology Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>EMBO reports</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext_linktorsrc</fulltext></delivery><addata><au>Schurig‐Briccio, Lici A</au><au>Parraga Solorzano, Paola K</au><au>Lencina, Andrea M</au><au>Radin, Jana N</au><au>Chen, Grischa Y</au><au>Sauer, John‐Demian</au><au>Kehl‐Fie, Thomas E</au><au>Gennis, Robert B</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Role of respiratory NADH oxidation in the regulation of Staphylococcus aureus virulence</atitle><jtitle>EMBO reports</jtitle><stitle>EMBO Rep</stitle><addtitle>EMBO Rep</addtitle><date>2020-05-06</date><risdate>2020</risdate><volume>21</volume><issue>5</issue><spage>e45832</spage><epage>n/a</epage><pages>e45832-n/a</pages><issn>1469-221X</issn><eissn>1469-3178</eissn><abstract>The success of
Staphylococcus aureus
as a pathogen is due to its capability of fine‐tuning its cellular physiology to meet the challenges presented by diverse environments, which allows it to colonize multiple niches within a single vertebrate host. Elucidating the roles of energy‐yielding metabolic pathways could uncover attractive therapeutic strategies and targets. In this work, we seek to determine the effects of disabling NADH‐dependent aerobic respiration on the physiology of
S. aureus
. Differing from many pathogens,
S. aureus
has two type‐2 respiratory NADH dehydrogenases (NDH‐2s) but lacks the respiratory ion‐pumping NDHs. Here, we show that the NDH‐2s, individually or together, are not essential either for respiration or growth. Nevertheless, their absence eliminates biofilm formation, production of α‐toxin, and reduces the ability to colonize specific organs in a mouse model of systemic infection. Moreover, we demonstrate that the reason behind these phenotypes is the alteration of the fatty acid metabolism. Importantly, the SaeRS two‐component system, which responds to fatty acids regulation, is responsible for the link between NADH‐dependent respiration and virulence in
S. aureus
.
Synopsis
NADH‐dependent respiration regulates fatty acid metabolism in
Staphylococcus aureus
. Changes in the concentration of free fatty acids are sensed by the SaeRS two‐component system, which controls virulence.
NdhC is vital for α‐toxin production, whereas NdhC and NdhF are critical for biofilm formation and systemic infection.
NdhC‐deficient strains accumulate free fatty acids in the stationary phase.
SaeRS responds to changes in fatty acid metabolism, thereby affecting α‐toxin production and biofilm formation.
Graphical Abstract
NADH‐dependent respiration regulates fatty acid metabolism in
Staphylococcus aureus
. Changes in the concentration of free fatty acids are sensed by the SaeRS two‐component system, which controls virulence.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>32202364</pmid><doi>10.15252/embr.201845832</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0001-9367-794X</orcidid><orcidid>https://orcid.org/0000-0002-5514-2298</orcidid><orcidid>https://orcid.org/0000-0001-7933-6460</orcidid><orcidid>https://orcid.org/0000-0002-3805-6945</orcidid><oa>free_for_read</oa></addata></record> |
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| identifier | ISSN: 1469-221X |
| ispartof | EMBO reports, 2020-05, Vol.21 (5), p.e45832-n/a |
| issn | 1469-221X 1469-3178 |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_7202225 |
| source | Springer Nature OA Free Journals |
| subjects | Aerobic respiration Animals Bacterial Proteins - genetics Bacterial Proteins - metabolism Biofilms Disseminated infection EMBO21 EMBO23 Fatty acids Gene Expression Regulation, Bacterial Metabolic pathways Metabolism Mice NAD NADH NADH dehydrogenase NADH/NAD Nicotinamide adenine dinucleotide Organs Oxidation Pathogens Phenotypes Physiology Respiration respiratory chain Staphylococcal Infections Staphylococcus aureus Staphylococcus aureus - genetics Stationary phase Toxins two‐component system Vertebrates Virulence α-Toxin |
| title | Role of respiratory NADH oxidation in the regulation of Staphylococcus aureus virulence |
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