The transcriptional changes of LrgA discriminates the responsiveness of Staphylococcus aureus towards blue light from that of photodynamic inactivation
Antimicrobial blue light (aBL) is utilized as a new approach to inhibit the growth of Staphylococcus aureus (S. aureus). Mediated by the endogenous chromophore, aBL possesses the similar photokilling property with aPDI (antimicrobial photodynamic inactivation), however, their mechanistic discrepanci...
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| Veröffentlicht in: | Journal of photochemistry and photobiology. B, Biology Biology, 2024-09, Vol.258, p.112967, Article 112967 |
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| container_title | Journal of photochemistry and photobiology. B, Biology |
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| creator | Yang, Ruili Xu, Yi Xu, Jinchun Li, Yali Wan, Xiaoxiao Kong, Rui Ding, Chao Tao, Han Wang, Hui-Li |
| description | Antimicrobial blue light (aBL) is utilized as a new approach to inhibit the growth of Staphylococcus aureus (S. aureus). Mediated by the endogenous chromophore, aBL possesses the similar photokilling property with aPDI (antimicrobial photodynamic inactivation), however, their mechanistic discrepancies in triggering the death of staphylococcal cells are not yet understood. Here, we describe the use of a 460-nm-LED to curb the viability of S. aureus. According to the results, the bacterial survival was sharply decreased when blue light was applied, reaching a maximum of 4.11 ± 0.04 log10 units. Moreover, the membrane integrity was damaged by aBL, causing the leakage of intracellular DNA. Transcriptomic analysis indicates the divergent gene expression upon either aBL or aPDI, with pathways such as transport, DNA repair, expression regulation and porphyrin massively affected by aBL. Among the commonly regulated genes, LrgA was underpinned on account of its involvement with biofilm formation and protein transport. By comparing the wildtype with the LrgA-overexpressing (LrgA+) strain, the survival rate, membrane penetration, surface structure and biofilm formation were, to a varying degree, improved for LrgA+, which may suggest that LrgA plays essential roles in modulating the responsiveness of S. aureus. Besides, LrgA may function through regulating the expression of autolysis-related systems. Finally, LrgA overexpression did not attenuate but aggravate the impairment induced by aPDI, showcasing a distinct responsive strategy from aBL. Taken together, this study unveils a unique molecular alteration for the aBL-mediated inactivation, providing the basis of utilizing blue light to reduce the harm brought by S. aureus.
•LrgA discriminates aBL from aPDI in responsiveness of S. aureus•The 460-nm light can effectively decrease the survival of S. aureus by 1–4 logs•aBL exerts inhibitory effect through regulating the expression of LrgA•LrgA-AtlA plays key roles in modulating the aBL-mediated effect on biofilm |
| doi_str_mv | 10.1016/j.jphotobiol.2024.112967 |
| format | Article |
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•LrgA discriminates aBL from aPDI in responsiveness of S. aureus•The 460-nm light can effectively decrease the survival of S. aureus by 1–4 logs•aBL exerts inhibitory effect through regulating the expression of LrgA•LrgA-AtlA plays key roles in modulating the aBL-mediated effect on biofilm</description><identifier>ISSN: 1011-1344</identifier><identifier>ISSN: 1873-2682</identifier><identifier>EISSN: 1873-2682</identifier><identifier>DOI: 10.1016/j.jphotobiol.2024.112967</identifier><identifier>PMID: 38996773</identifier><language>eng</language><publisher>Switzerland: Elsevier B.V</publisher><subject>Antimicrobial blue light ; Antimicrobial photodynamic inactivation ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Biofilm ; Biofilms - drug effects ; Biofilms - radiation effects ; Blue Light ; Gene Expression Regulation, Bacterial - drug effects ; Gene Expression Regulation, Bacterial - radiation effects ; LrgA ; Microbial Viability - drug effects ; Microbial Viability - radiation effects ; Porphyrins - chemistry ; Porphyrins - pharmacology ; Staphylococcus aureus ; Staphylococcus aureus - drug effects ; Staphylococcus aureus - genetics ; Staphylococcus aureus - physiology ; Staphylococcus aureus - radiation effects ; Transcription, Genetic - drug effects ; Transcription, Genetic - radiation effects</subject><ispartof>Journal of photochemistry and photobiology. B, Biology, 2024-09, Vol.258, p.112967, Article 112967</ispartof><rights>2024 Elsevier B.V.</rights><rights>Copyright © 2024 Elsevier B.V. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c249t-ade6dc840fb9ef98f2aa5981b07e60723c0c1dc566b8a322f8e699b6cce5363d3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.jphotobiol.2024.112967$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38996773$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yang, Ruili</creatorcontrib><creatorcontrib>Xu, Yi</creatorcontrib><creatorcontrib>Xu, Jinchun</creatorcontrib><creatorcontrib>Li, Yali</creatorcontrib><creatorcontrib>Wan, Xiaoxiao</creatorcontrib><creatorcontrib>Kong, Rui</creatorcontrib><creatorcontrib>Ding, Chao</creatorcontrib><creatorcontrib>Tao, Han</creatorcontrib><creatorcontrib>Wang, Hui-Li</creatorcontrib><title>The transcriptional changes of LrgA discriminates the responsiveness of Staphylococcus aureus towards blue light from that of photodynamic inactivation</title><title>Journal of photochemistry and photobiology. B, Biology</title><addtitle>J Photochem Photobiol B</addtitle><description>Antimicrobial blue light (aBL) is utilized as a new approach to inhibit the growth of Staphylococcus aureus (S. aureus). Mediated by the endogenous chromophore, aBL possesses the similar photokilling property with aPDI (antimicrobial photodynamic inactivation), however, their mechanistic discrepancies in triggering the death of staphylococcal cells are not yet understood. Here, we describe the use of a 460-nm-LED to curb the viability of S. aureus. According to the results, the bacterial survival was sharply decreased when blue light was applied, reaching a maximum of 4.11 ± 0.04 log10 units. Moreover, the membrane integrity was damaged by aBL, causing the leakage of intracellular DNA. Transcriptomic analysis indicates the divergent gene expression upon either aBL or aPDI, with pathways such as transport, DNA repair, expression regulation and porphyrin massively affected by aBL. Among the commonly regulated genes, LrgA was underpinned on account of its involvement with biofilm formation and protein transport. By comparing the wildtype with the LrgA-overexpressing (LrgA+) strain, the survival rate, membrane penetration, surface structure and biofilm formation were, to a varying degree, improved for LrgA+, which may suggest that LrgA plays essential roles in modulating the responsiveness of S. aureus. Besides, LrgA may function through regulating the expression of autolysis-related systems. Finally, LrgA overexpression did not attenuate but aggravate the impairment induced by aPDI, showcasing a distinct responsive strategy from aBL. Taken together, this study unveils a unique molecular alteration for the aBL-mediated inactivation, providing the basis of utilizing blue light to reduce the harm brought by S. aureus.
•LrgA discriminates aBL from aPDI in responsiveness of S. aureus•The 460-nm light can effectively decrease the survival of S. aureus by 1–4 logs•aBL exerts inhibitory effect through regulating the expression of LrgA•LrgA-AtlA plays key roles in modulating the aBL-mediated effect on biofilm</description><subject>Antimicrobial blue light</subject><subject>Antimicrobial photodynamic inactivation</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>Biofilm</subject><subject>Biofilms - drug effects</subject><subject>Biofilms - radiation effects</subject><subject>Blue Light</subject><subject>Gene Expression Regulation, Bacterial - drug effects</subject><subject>Gene Expression Regulation, Bacterial - radiation effects</subject><subject>LrgA</subject><subject>Microbial Viability - drug effects</subject><subject>Microbial Viability - radiation effects</subject><subject>Porphyrins - chemistry</subject><subject>Porphyrins - pharmacology</subject><subject>Staphylococcus aureus</subject><subject>Staphylococcus aureus - drug effects</subject><subject>Staphylococcus aureus - genetics</subject><subject>Staphylococcus aureus - physiology</subject><subject>Staphylococcus aureus - radiation effects</subject><subject>Transcription, Genetic - drug effects</subject><subject>Transcription, Genetic - radiation effects</subject><issn>1011-1344</issn><issn>1873-2682</issn><issn>1873-2682</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFUcuO1DAQjBCIXRZ-AfnIJYMfiWMflxULSCNxYDlbjt2ZeJTYwXYGzZfwuzg7CxzpS1vtqmqXq6oQwTuCCX9_3B2XMeTQuzDtKKbNjhAqefesuiaiYzXlgj4vZ0xITVjTXFWvUjriUi3vXlZXTMiC7th19ethBJSj9slEt2QXvJ6QGbU_QEJhQPt4uEXWbbez8zqXaS6MCGkJPrkTeEiPwG9ZL-N5CiYYsyak1wil5fBTR5tQP62AJncYMxpimIuGzhvr0YU9ez07g4q-ye6kt1e8rl4Mekrw5qnfVN_vPz7cfa73Xz99ubvd14Y2MtfaArdGNHjoJQxSDFTrVgrS4w447igz2BBrWs57oRmlgwAuZc-NgZZxZtlN9e6iu8TwY4WU1VzMwjRpD2FNiuFOirYUL1BxgZoYUoowqKV8io5nRbDaYlFH9S8WtcWiLrEU6tunLWs_g_1L_JNDAXy4AKB4PTmIKhkH3oB1EUxWNrj_b_kN9oapLw</recordid><startdate>202409</startdate><enddate>202409</enddate><creator>Yang, Ruili</creator><creator>Xu, Yi</creator><creator>Xu, Jinchun</creator><creator>Li, Yali</creator><creator>Wan, Xiaoxiao</creator><creator>Kong, Rui</creator><creator>Ding, Chao</creator><creator>Tao, Han</creator><creator>Wang, Hui-Li</creator><general>Elsevier B.V</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>7X8</scope></search><sort><creationdate>202409</creationdate><title>The transcriptional changes of LrgA discriminates the responsiveness of Staphylococcus aureus towards blue light from that of photodynamic inactivation</title><author>Yang, Ruili ; Xu, Yi ; Xu, Jinchun ; Li, Yali ; Wan, Xiaoxiao ; Kong, Rui ; Ding, Chao ; Tao, Han ; Wang, Hui-Li</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c249t-ade6dc840fb9ef98f2aa5981b07e60723c0c1dc566b8a322f8e699b6cce5363d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Antimicrobial blue light</topic><topic>Antimicrobial photodynamic inactivation</topic><topic>Bacterial Proteins - genetics</topic><topic>Bacterial Proteins - metabolism</topic><topic>Biofilm</topic><topic>Biofilms - drug effects</topic><topic>Biofilms - radiation effects</topic><topic>Blue Light</topic><topic>Gene Expression Regulation, Bacterial - drug effects</topic><topic>Gene Expression Regulation, Bacterial - radiation effects</topic><topic>LrgA</topic><topic>Microbial Viability - drug effects</topic><topic>Microbial Viability - radiation effects</topic><topic>Porphyrins - chemistry</topic><topic>Porphyrins - pharmacology</topic><topic>Staphylococcus aureus</topic><topic>Staphylococcus aureus - drug effects</topic><topic>Staphylococcus aureus - genetics</topic><topic>Staphylococcus aureus - physiology</topic><topic>Staphylococcus aureus - radiation effects</topic><topic>Transcription, Genetic - drug effects</topic><topic>Transcription, Genetic - radiation effects</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yang, Ruili</creatorcontrib><creatorcontrib>Xu, Yi</creatorcontrib><creatorcontrib>Xu, Jinchun</creatorcontrib><creatorcontrib>Li, Yali</creatorcontrib><creatorcontrib>Wan, Xiaoxiao</creatorcontrib><creatorcontrib>Kong, Rui</creatorcontrib><creatorcontrib>Ding, Chao</creatorcontrib><creatorcontrib>Tao, Han</creatorcontrib><creatorcontrib>Wang, Hui-Li</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Journal of photochemistry and photobiology. B, Biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yang, Ruili</au><au>Xu, Yi</au><au>Xu, Jinchun</au><au>Li, Yali</au><au>Wan, Xiaoxiao</au><au>Kong, Rui</au><au>Ding, Chao</au><au>Tao, Han</au><au>Wang, Hui-Li</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The transcriptional changes of LrgA discriminates the responsiveness of Staphylococcus aureus towards blue light from that of photodynamic inactivation</atitle><jtitle>Journal of photochemistry and photobiology. B, Biology</jtitle><addtitle>J Photochem Photobiol B</addtitle><date>2024-09</date><risdate>2024</risdate><volume>258</volume><spage>112967</spage><pages>112967-</pages><artnum>112967</artnum><issn>1011-1344</issn><issn>1873-2682</issn><eissn>1873-2682</eissn><abstract>Antimicrobial blue light (aBL) is utilized as a new approach to inhibit the growth of Staphylococcus aureus (S. aureus). Mediated by the endogenous chromophore, aBL possesses the similar photokilling property with aPDI (antimicrobial photodynamic inactivation), however, their mechanistic discrepancies in triggering the death of staphylococcal cells are not yet understood. Here, we describe the use of a 460-nm-LED to curb the viability of S. aureus. According to the results, the bacterial survival was sharply decreased when blue light was applied, reaching a maximum of 4.11 ± 0.04 log10 units. Moreover, the membrane integrity was damaged by aBL, causing the leakage of intracellular DNA. Transcriptomic analysis indicates the divergent gene expression upon either aBL or aPDI, with pathways such as transport, DNA repair, expression regulation and porphyrin massively affected by aBL. Among the commonly regulated genes, LrgA was underpinned on account of its involvement with biofilm formation and protein transport. By comparing the wildtype with the LrgA-overexpressing (LrgA+) strain, the survival rate, membrane penetration, surface structure and biofilm formation were, to a varying degree, improved for LrgA+, which may suggest that LrgA plays essential roles in modulating the responsiveness of S. aureus. Besides, LrgA may function through regulating the expression of autolysis-related systems. Finally, LrgA overexpression did not attenuate but aggravate the impairment induced by aPDI, showcasing a distinct responsive strategy from aBL. Taken together, this study unveils a unique molecular alteration for the aBL-mediated inactivation, providing the basis of utilizing blue light to reduce the harm brought by S. aureus.
•LrgA discriminates aBL from aPDI in responsiveness of S. aureus•The 460-nm light can effectively decrease the survival of S. aureus by 1–4 logs•aBL exerts inhibitory effect through regulating the expression of LrgA•LrgA-AtlA plays key roles in modulating the aBL-mediated effect on biofilm</abstract><cop>Switzerland</cop><pub>Elsevier B.V</pub><pmid>38996773</pmid><doi>10.1016/j.jphotobiol.2024.112967</doi></addata></record> |
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| subjects | Antimicrobial blue light Antimicrobial photodynamic inactivation Bacterial Proteins - genetics Bacterial Proteins - metabolism Biofilm Biofilms - drug effects Biofilms - radiation effects Blue Light Gene Expression Regulation, Bacterial - drug effects Gene Expression Regulation, Bacterial - radiation effects LrgA Microbial Viability - drug effects Microbial Viability - radiation effects Porphyrins - chemistry Porphyrins - pharmacology Staphylococcus aureus Staphylococcus aureus - drug effects Staphylococcus aureus - genetics Staphylococcus aureus - physiology Staphylococcus aureus - radiation effects Transcription, Genetic - drug effects Transcription, Genetic - radiation effects |
| title | The transcriptional changes of LrgA discriminates the responsiveness of Staphylococcus aureus towards blue light from that of photodynamic inactivation |
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