Small RNA SmsR1 modulates acidogenicity and cariogenic virulence by affecting protein acetylation in Streptococcus mutans
Post-transcriptional regulation by small RNAs and post-translational modifications (PTM) such as lysine acetylation play fundamental roles in physiological circuits, offering rapid responses to environmental signals with low energy consumption. Yet, the interplay between these regulatory systems rem...
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| Veröffentlicht in: | PLoS pathogens 2024-04, Vol.20 (4), p.e1012147-e1012147 |
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| creator | Li, Jing Ma, Qizhao Huang, Jun Liu, Yaqi Zhou, Jing Yu, Shuxing Zhang, Qiong Lin, Yongwang Wang, Lingyun Zou, Jing Li, Yuqing |
| description | Post-transcriptional regulation by small RNAs and post-translational modifications (PTM) such as lysine acetylation play fundamental roles in physiological circuits, offering rapid responses to environmental signals with low energy consumption. Yet, the interplay between these regulatory systems remains underexplored. Here, we unveil the cross-talk between sRNAs and lysine acetylation in Streptococcus mutans, a primary cariogenic pathogen known for its potent acidogenic virulence. Through systematic overexpression of sRNAs in S. mutans, we identified sRNA SmsR1 as a critical player in modulating acidogenicity, a key cariogenic virulence feature in S. mutans. Furthermore, combined with the analysis of predicted target mRNA and transcriptome results, potential target genes were identified and experimentally verified. A direct interaction between SmsR1 and 5'-UTR region of pdhC gene was determined by in vitro binding assays. Importantly, we found that overexpression of SmsR1 reduced the expression of pdhC mRNA and increased the intracellular concentration of acetyl-CoA, resulting in global changes in protein acetylation levels. This was verified by acetyl-proteomics in S. mutans, along with an increase in acetylation level and decreased activity of LDH. Our study unravels a novel regulatory paradigm where sRNA bridges post-transcriptional regulation with post-translational modification, underscoring bacterial adeptness in fine-tuning responses to environmental stress. |
| doi_str_mv | 10.1371/journal.ppat.1012147 |
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Yet, the interplay between these regulatory systems remains underexplored. Here, we unveil the cross-talk between sRNAs and lysine acetylation in Streptococcus mutans, a primary cariogenic pathogen known for its potent acidogenic virulence. Through systematic overexpression of sRNAs in S. mutans, we identified sRNA SmsR1 as a critical player in modulating acidogenicity, a key cariogenic virulence feature in S. mutans. Furthermore, combined with the analysis of predicted target mRNA and transcriptome results, potential target genes were identified and experimentally verified. A direct interaction between SmsR1 and 5'-UTR region of pdhC gene was determined by in vitro binding assays. Importantly, we found that overexpression of SmsR1 reduced the expression of pdhC mRNA and increased the intracellular concentration of acetyl-CoA, resulting in global changes in protein acetylation levels. This was verified by acetyl-proteomics in S. mutans, along with an increase in acetylation level and decreased activity of LDH. Our study unravels a novel regulatory paradigm where sRNA bridges post-transcriptional regulation with post-translational modification, underscoring bacterial adeptness in fine-tuning responses to environmental stress.</description><identifier>ISSN: 1553-7374</identifier><identifier>ISSN: 1553-7366</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.1012147</identifier><identifier>PMID: 38620039</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>5' Untranslated Regions ; Acetylation ; Analysis ; Animals ; Bacteria ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Biofilms ; Biology and Life Sciences ; Care and treatment ; Complications and side effects ; Dehydrogenases ; Dental Caries - metabolism ; Dental Caries - microbiology ; Energy consumption ; Environmental stress ; Gene expression ; Gene Expression Regulation, Bacterial ; Gene regulation ; Humans ; Lysine ; Medicine and Health Sciences ; Messenger RNA ; Metabolism ; Mice ; Peptides ; Physical Sciences ; Physiology ; Post-transcription ; Post-translation ; Post-translational modification ; Protein Processing, Post-Translational ; Proteins ; Proteomics ; Research and Analysis Methods ; Ribonucleic acid ; RNA ; RNA, Bacterial - genetics ; RNA, Bacterial - metabolism ; RNA, Small Untranslated - genetics ; RNA, Small Untranslated - metabolism ; Streptococcal infections ; Streptococcus mutans ; Streptococcus mutans - genetics ; Streptococcus mutans - metabolism ; Streptococcus mutans - pathogenicity ; Transcription factors ; Transcriptomes ; Translation ; Variance analysis ; Virulence ; Virulence (Microbiology)</subject><ispartof>PLoS pathogens, 2024-04, Vol.20 (4), p.e1012147-e1012147</ispartof><rights>Copyright: © 2024 Li et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>COPYRIGHT 2024 Public Library of Science</rights><rights>2024 Li et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2024 Li et al 2024 Li et al</rights><rights>2024 Li et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c611t-c261ae50c292505f2fa382945356776365bb14b90c854c5be3ff058467044a4e3</cites><orcidid>0000-0002-3410-6300</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/PMC11045139/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11045139/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38620039$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Zhang, Gongyi</contributor><creatorcontrib>Li, Jing</creatorcontrib><creatorcontrib>Ma, Qizhao</creatorcontrib><creatorcontrib>Huang, Jun</creatorcontrib><creatorcontrib>Liu, Yaqi</creatorcontrib><creatorcontrib>Zhou, Jing</creatorcontrib><creatorcontrib>Yu, Shuxing</creatorcontrib><creatorcontrib>Zhang, Qiong</creatorcontrib><creatorcontrib>Lin, Yongwang</creatorcontrib><creatorcontrib>Wang, Lingyun</creatorcontrib><creatorcontrib>Zou, Jing</creatorcontrib><creatorcontrib>Li, Yuqing</creatorcontrib><title>Small RNA SmsR1 modulates acidogenicity and cariogenic virulence by affecting protein acetylation in Streptococcus mutans</title><title>PLoS pathogens</title><addtitle>PLoS Pathog</addtitle><description>Post-transcriptional regulation by small RNAs and post-translational modifications (PTM) such as lysine acetylation play fundamental roles in physiological circuits, offering rapid responses to environmental signals with low energy consumption. 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This was verified by acetyl-proteomics in S. mutans, along with an increase in acetylation level and decreased activity of LDH. Our study unravels a novel regulatory paradigm where sRNA bridges post-transcriptional regulation with post-translational modification, underscoring bacterial adeptness in fine-tuning responses to environmental stress.</description><subject>5' Untranslated Regions</subject><subject>Acetylation</subject><subject>Analysis</subject><subject>Animals</subject><subject>Bacteria</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>Biofilms</subject><subject>Biology and Life Sciences</subject><subject>Care and treatment</subject><subject>Complications and side effects</subject><subject>Dehydrogenases</subject><subject>Dental Caries - metabolism</subject><subject>Dental Caries - microbiology</subject><subject>Energy consumption</subject><subject>Environmental stress</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Bacterial</subject><subject>Gene regulation</subject><subject>Humans</subject><subject>Lysine</subject><subject>Medicine and Health Sciences</subject><subject>Messenger RNA</subject><subject>Metabolism</subject><subject>Mice</subject><subject>Peptides</subject><subject>Physical Sciences</subject><subject>Physiology</subject><subject>Post-transcription</subject><subject>Post-translation</subject><subject>Post-translational modification</subject><subject>Protein Processing, Post-Translational</subject><subject>Proteins</subject><subject>Proteomics</subject><subject>Research and Analysis Methods</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA, Bacterial - genetics</subject><subject>RNA, Bacterial - metabolism</subject><subject>RNA, Small Untranslated - genetics</subject><subject>RNA, Small Untranslated - metabolism</subject><subject>Streptococcal infections</subject><subject>Streptococcus mutans</subject><subject>Streptococcus mutans - genetics</subject><subject>Streptococcus mutans - metabolism</subject><subject>Streptococcus mutans - pathogenicity</subject><subject>Transcription factors</subject><subject>Transcriptomes</subject><subject>Translation</subject><subject>Variance analysis</subject><subject>Virulence</subject><subject>Virulence (Microbiology)</subject><issn>1553-7374</issn><issn>1553-7366</issn><issn>1553-7374</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqVkk1v1DAQhiMEomXhHyCIxAUOu9jxV3KqVhUfK1VF2oWz5TiT4Cqxg-1U7L_Hy6ZVF_WCfLA9ft53PKPJstcYrTAR-OONm7xV_WocVVxhhAtMxZPsHDNGloII-vTB-Sx7EcINQhQTzJ9nZ6TkBUKkOs_2u0H1fb69Xue7IWxxPrhm6lWEkCttGteBNdrEfa5sk2vlzTGS3xo_9WA15HV6a1vQ0dguH72LYGzSQtwnG-Nsnq676GGMTjutp5APU1Q2vMyetaoP8GreF9mPz5--X35dXn37srlcXy01xzgudcGxAoZ0URUMsbZoFSmLijLCuBCccFbXmNYV0iWjmtVA2haxknKBKFUUyCJ7e_Qdexfk3LUgCeIVLokQZSI2R6Jx6kaO3gzK76VTRv4NON9J5aPRPUjRNKAEq7BCnGJeV5zjgtdly0sE6S_J62LONtUDNBps9Ko_MT19sean7NytxBhRhkmVHN7PDt79miBEOZigoe-VBTcdPk6qEqXSD-i7f9DHy5upTqUKjG1dSqwPpnItqoIwVKTEi2z1CJVWA4PRzkJrUvxE8OFEkJgIv2OnphDkZrf9D_b6lKVHVnsXgof2vnkYycPk3xUpD5Mv58lPsjcPG38vuht18gdHO_5O</recordid><startdate>20240401</startdate><enddate>20240401</enddate><creator>Li, Jing</creator><creator>Ma, Qizhao</creator><creator>Huang, Jun</creator><creator>Liu, Yaqi</creator><creator>Zhou, Jing</creator><creator>Yu, Shuxing</creator><creator>Zhang, Qiong</creator><creator>Lin, Yongwang</creator><creator>Wang, Lingyun</creator><creator>Zou, Jing</creator><creator>Li, Yuqing</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>ISN</scope><scope>ISR</scope><scope>3V.</scope><scope>7QL</scope><scope>7U9</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-3410-6300</orcidid></search><sort><creationdate>20240401</creationdate><title>Small RNA SmsR1 modulates acidogenicity and cariogenic virulence by affecting protein acetylation in Streptococcus mutans</title><author>Li, Jing ; Ma, Qizhao ; Huang, Jun ; Liu, Yaqi ; Zhou, Jing ; Yu, Shuxing ; Zhang, Qiong ; Lin, Yongwang ; Wang, Lingyun ; Zou, Jing ; Li, Yuqing</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c611t-c261ae50c292505f2fa382945356776365bb14b90c854c5be3ff058467044a4e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>5' Untranslated Regions</topic><topic>Acetylation</topic><topic>Analysis</topic><topic>Animals</topic><topic>Bacteria</topic><topic>Bacterial Proteins - 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genetics</topic><topic>RNA, Bacterial - metabolism</topic><topic>RNA, Small Untranslated - genetics</topic><topic>RNA, Small Untranslated - metabolism</topic><topic>Streptococcal infections</topic><topic>Streptococcus mutans</topic><topic>Streptococcus mutans - genetics</topic><topic>Streptococcus mutans - metabolism</topic><topic>Streptococcus mutans - pathogenicity</topic><topic>Transcription factors</topic><topic>Transcriptomes</topic><topic>Translation</topic><topic>Variance analysis</topic><topic>Virulence</topic><topic>Virulence (Microbiology)</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Li, Jing</creatorcontrib><creatorcontrib>Ma, Qizhao</creatorcontrib><creatorcontrib>Huang, Jun</creatorcontrib><creatorcontrib>Liu, Yaqi</creatorcontrib><creatorcontrib>Zhou, Jing</creatorcontrib><creatorcontrib>Yu, Shuxing</creatorcontrib><creatorcontrib>Zhang, Qiong</creatorcontrib><creatorcontrib>Lin, Yongwang</creatorcontrib><creatorcontrib>Wang, Lingyun</creatorcontrib><creatorcontrib>Zou, Jing</creatorcontrib><creatorcontrib>Li, Yuqing</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Virology and AIDS Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>Access via ProQuest (Open Access)</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS pathogens</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Li, Jing</au><au>Ma, Qizhao</au><au>Huang, Jun</au><au>Liu, Yaqi</au><au>Zhou, Jing</au><au>Yu, Shuxing</au><au>Zhang, Qiong</au><au>Lin, Yongwang</au><au>Wang, Lingyun</au><au>Zou, Jing</au><au>Li, Yuqing</au><au>Zhang, Gongyi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Small RNA SmsR1 modulates acidogenicity and cariogenic virulence by affecting protein acetylation in Streptococcus mutans</atitle><jtitle>PLoS pathogens</jtitle><addtitle>PLoS Pathog</addtitle><date>2024-04-01</date><risdate>2024</risdate><volume>20</volume><issue>4</issue><spage>e1012147</spage><epage>e1012147</epage><pages>e1012147-e1012147</pages><issn>1553-7374</issn><issn>1553-7366</issn><eissn>1553-7374</eissn><abstract>Post-transcriptional regulation by small RNAs and post-translational modifications (PTM) such as lysine acetylation play fundamental roles in physiological circuits, offering rapid responses to environmental signals with low energy consumption. Yet, the interplay between these regulatory systems remains underexplored. Here, we unveil the cross-talk between sRNAs and lysine acetylation in Streptococcus mutans, a primary cariogenic pathogen known for its potent acidogenic virulence. Through systematic overexpression of sRNAs in S. mutans, we identified sRNA SmsR1 as a critical player in modulating acidogenicity, a key cariogenic virulence feature in S. mutans. Furthermore, combined with the analysis of predicted target mRNA and transcriptome results, potential target genes were identified and experimentally verified. A direct interaction between SmsR1 and 5'-UTR region of pdhC gene was determined by in vitro binding assays. Importantly, we found that overexpression of SmsR1 reduced the expression of pdhC mRNA and increased the intracellular concentration of acetyl-CoA, resulting in global changes in protein acetylation levels. This was verified by acetyl-proteomics in S. mutans, along with an increase in acetylation level and decreased activity of LDH. Our study unravels a novel regulatory paradigm where sRNA bridges post-transcriptional regulation with post-translational modification, underscoring bacterial adeptness in fine-tuning responses to environmental stress.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>38620039</pmid><doi>10.1371/journal.ppat.1012147</doi><tpages>e1012147</tpages><orcidid>https://orcid.org/0000-0002-3410-6300</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | 5' Untranslated Regions Acetylation Analysis Animals Bacteria Bacterial Proteins - genetics Bacterial Proteins - metabolism Biofilms Biology and Life Sciences Care and treatment Complications and side effects Dehydrogenases Dental Caries - metabolism Dental Caries - microbiology Energy consumption Environmental stress Gene expression Gene Expression Regulation, Bacterial Gene regulation Humans Lysine Medicine and Health Sciences Messenger RNA Metabolism Mice Peptides Physical Sciences Physiology Post-transcription Post-translation Post-translational modification Protein Processing, Post-Translational Proteins Proteomics Research and Analysis Methods Ribonucleic acid RNA RNA, Bacterial - genetics RNA, Bacterial - metabolism RNA, Small Untranslated - genetics RNA, Small Untranslated - metabolism Streptococcal infections Streptococcus mutans Streptococcus mutans - genetics Streptococcus mutans - metabolism Streptococcus mutans - pathogenicity Transcription factors Transcriptomes Translation Variance analysis Virulence Virulence (Microbiology) |
| title | Small RNA SmsR1 modulates acidogenicity and cariogenic virulence by affecting protein acetylation in Streptococcus mutans |
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