Pneumococcal extracellular vesicles mediate horizontal gene transfer via the transformation machinery
Bacterial cells secrete extracellular vesicles (EVs), the function of which is a matter of intense investigation. Here, we show that the EVs secreted by the human pathogen (pneumococcus) are associated with bacterial DNA on their surface and can deliver this DNA to the transformation machinery of co...
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| Veröffentlicht in: | mSphere 2024-12, Vol.9 (12), p.e0072724 |
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| creator | Werner Lass, Sarah Smith, Bailey E Camphire, Shaw Eutsey, Rory A Prentice, Jojo A Yerneni, Saigopalakrishna S Arun, Ashni Bridges, Andrew A Rosch, Jason W Conway, James F Campbell, Phil Hiller, N Luisa |
| description | Bacterial cells secrete extracellular vesicles (EVs), the function of which is a matter of intense investigation. Here, we show that the EVs secreted by the human pathogen
(pneumococcus) are associated with bacterial DNA on their surface and can deliver this DNA to the transformation machinery of competent cells. These findings suggest that EVs contribute to gene transfer in Gram-positive bacteria and, in doing so, may promote the spread of drug resistance genes in the population.IMPORTANCEThis work extends our understanding of horizontal gene transfer and the roles of extracellular vesicles in pneumococcus. This bacterium serves as the model for transformation, a process by which bacteria can take up naked DNA from the environment. Here, we show that extracellular vesicles secreted by the pneumococcus have DNA on their surface and that this DNA can be imported by the transformation machinery, facilitating gene transfer. Understanding EV-mediated gene transfer may provide new avenues to manage the spread of antibiotic drug resistance. |
| doi_str_mv | 10.1128/msphere.00727-24 |
| format | Article |
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(pneumococcus) are associated with bacterial DNA on their surface and can deliver this DNA to the transformation machinery of competent cells. These findings suggest that EVs contribute to gene transfer in Gram-positive bacteria and, in doing so, may promote the spread of drug resistance genes in the population.IMPORTANCEThis work extends our understanding of horizontal gene transfer and the roles of extracellular vesicles in pneumococcus. This bacterium serves as the model for transformation, a process by which bacteria can take up naked DNA from the environment. Here, we show that extracellular vesicles secreted by the pneumococcus have DNA on their surface and that this DNA can be imported by the transformation machinery, facilitating gene transfer. Understanding EV-mediated gene transfer may provide new avenues to manage the spread of antibiotic drug resistance.</description><identifier>ISSN: 2379-5042</identifier><identifier>EISSN: 2379-5042</identifier><identifier>DOI: 10.1128/msphere.00727-24</identifier><identifier>PMID: 39503503</identifier><language>eng</language><publisher>United States: American Society for Microbiology</publisher><subject>antibiotic resistance ; Bacteriology ; competence ; DNA, Bacterial - genetics ; Drug Resistance, Bacterial - genetics ; extracellular vesicle ; Extracellular Vesicles - genetics ; Extracellular Vesicles - metabolism ; Gene Transfer, Horizontal ; horizontal gene transfer ; Humans ; Research Article ; Streptococcus pneumoniae ; Streptococcus pneumoniae - genetics ; transformation ; Transformation, Bacterial</subject><ispartof>mSphere, 2024-12, Vol.9 (12), p.e0072724</ispartof><rights>Copyright © 2024 Werner Lass et al.</rights><rights>Copyright © 2024 Werner Lass et al. 2024 Werner Lass et al.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-a384t-1eb1fa11ab886464abcb09670d0a9df60123112d5bf0b567b9d10d1423b696013</cites><orcidid>0000-0002-4613-734X ; 0000-0002-8132-751X ; 0000-0003-4309-250X ; 0000-0001-6572-1368 ; 0000-0002-1798-1760 ; 0000-0001-8004-2152 ; 0000-0002-6581-4748</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://journals.asm.org/doi/pdf/10.1128/msphere.00727-24$$EPDF$$P50$$Gasm2$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://journals.asm.org/doi/full/10.1128/msphere.00727-24$$EHTML$$P50$$Gasm2$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2100,3179,27915,27916,52742,52743,52744,53782,53784</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39503503$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Tringe, Susannah Green</contributor><creatorcontrib>Werner Lass, Sarah</creatorcontrib><creatorcontrib>Smith, Bailey E</creatorcontrib><creatorcontrib>Camphire, Shaw</creatorcontrib><creatorcontrib>Eutsey, Rory A</creatorcontrib><creatorcontrib>Prentice, Jojo A</creatorcontrib><creatorcontrib>Yerneni, Saigopalakrishna S</creatorcontrib><creatorcontrib>Arun, Ashni</creatorcontrib><creatorcontrib>Bridges, Andrew A</creatorcontrib><creatorcontrib>Rosch, Jason W</creatorcontrib><creatorcontrib>Conway, James F</creatorcontrib><creatorcontrib>Campbell, Phil</creatorcontrib><creatorcontrib>Hiller, N Luisa</creatorcontrib><title>Pneumococcal extracellular vesicles mediate horizontal gene transfer via the transformation machinery</title><title>mSphere</title><addtitle>mSphere</addtitle><addtitle>mSphere</addtitle><description>Bacterial cells secrete extracellular vesicles (EVs), the function of which is a matter of intense investigation. Here, we show that the EVs secreted by the human pathogen
(pneumococcus) are associated with bacterial DNA on their surface and can deliver this DNA to the transformation machinery of competent cells. These findings suggest that EVs contribute to gene transfer in Gram-positive bacteria and, in doing so, may promote the spread of drug resistance genes in the population.IMPORTANCEThis work extends our understanding of horizontal gene transfer and the roles of extracellular vesicles in pneumococcus. This bacterium serves as the model for transformation, a process by which bacteria can take up naked DNA from the environment. Here, we show that extracellular vesicles secreted by the pneumococcus have DNA on their surface and that this DNA can be imported by the transformation machinery, facilitating gene transfer. Understanding EV-mediated gene transfer may provide new avenues to manage the spread of antibiotic drug resistance.</description><subject>antibiotic resistance</subject><subject>Bacteriology</subject><subject>competence</subject><subject>DNA, Bacterial - genetics</subject><subject>Drug Resistance, Bacterial - genetics</subject><subject>extracellular vesicle</subject><subject>Extracellular Vesicles - genetics</subject><subject>Extracellular Vesicles - metabolism</subject><subject>Gene Transfer, Horizontal</subject><subject>horizontal gene transfer</subject><subject>Humans</subject><subject>Research Article</subject><subject>Streptococcus pneumoniae</subject><subject>Streptococcus pneumoniae - genetics</subject><subject>transformation</subject><subject>Transformation, Bacterial</subject><issn>2379-5042</issn><issn>2379-5042</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>DOA</sourceid><recordid>eNp9Uk1v1DAQtRCIVqV3TihHLmn9FSc-IVQBrVQJDnC2xvFk41ViL3ZSUX493u62ai9IlmzNvHkz740Jec_oBWO8u5zzbsSEF5S2vK25fEVOuWh13VDJXz97n5DznLeUUqa4Uq16S06Ebqgo55Tgj4DrHPvY9zBV-GdJ0OM0rROk6g6z7yfM1YzOw4LVGJP_G8NSkBsMWBVwyAMWpIdqGR8DMc2w-BiqGfrRB0z378ibAaaM58f7jPz6-uXn1XV9-_3bzdXn2xpEJ5eaoWUDMAa265RUEmxvqVYtdRS0GxRlXBTprrEDtY1qrXaMOia5sEqXrDgjNwdeF2FrdsnPkO5NBG8eAjFtDKRlL8pQVKKV0LBGOTnophO8ERy1BaDMOle4Ph24dqstBvQYirrpBenLTPCj2cQ7w5gqs-n9NB-PDCn-XjEvZvZ57y4EjGs2gnGpNGetKlB6gPYp5pxweOrDqNlv2xy3bR62bbgsJfWhBPLMzTauKRRr_4f_8FzPU4PHvyD-AQ1nuGo</recordid><startdate>20241219</startdate><enddate>20241219</enddate><creator>Werner Lass, Sarah</creator><creator>Smith, Bailey E</creator><creator>Camphire, Shaw</creator><creator>Eutsey, Rory A</creator><creator>Prentice, Jojo A</creator><creator>Yerneni, Saigopalakrishna S</creator><creator>Arun, Ashni</creator><creator>Bridges, Andrew A</creator><creator>Rosch, Jason W</creator><creator>Conway, James F</creator><creator>Campbell, Phil</creator><creator>Hiller, N Luisa</creator><general>American Society for Microbiology</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><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-4613-734X</orcidid><orcidid>https://orcid.org/0000-0002-8132-751X</orcidid><orcidid>https://orcid.org/0000-0003-4309-250X</orcidid><orcidid>https://orcid.org/0000-0001-6572-1368</orcidid><orcidid>https://orcid.org/0000-0002-1798-1760</orcidid><orcidid>https://orcid.org/0000-0001-8004-2152</orcidid><orcidid>https://orcid.org/0000-0002-6581-4748</orcidid></search><sort><creationdate>20241219</creationdate><title>Pneumococcal extracellular vesicles mediate horizontal gene transfer via the transformation machinery</title><author>Werner Lass, Sarah ; Smith, Bailey E ; Camphire, Shaw ; Eutsey, Rory A ; Prentice, Jojo A ; Yerneni, Saigopalakrishna S ; Arun, Ashni ; Bridges, Andrew A ; Rosch, Jason W ; Conway, James F ; Campbell, Phil ; Hiller, N Luisa</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a384t-1eb1fa11ab886464abcb09670d0a9df60123112d5bf0b567b9d10d1423b696013</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>antibiotic resistance</topic><topic>Bacteriology</topic><topic>competence</topic><topic>DNA, Bacterial - genetics</topic><topic>Drug Resistance, Bacterial - genetics</topic><topic>extracellular vesicle</topic><topic>Extracellular Vesicles - genetics</topic><topic>Extracellular Vesicles - metabolism</topic><topic>Gene Transfer, Horizontal</topic><topic>horizontal gene transfer</topic><topic>Humans</topic><topic>Research Article</topic><topic>Streptococcus pneumoniae</topic><topic>Streptococcus pneumoniae - genetics</topic><topic>transformation</topic><topic>Transformation, Bacterial</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Werner Lass, Sarah</creatorcontrib><creatorcontrib>Smith, Bailey E</creatorcontrib><creatorcontrib>Camphire, Shaw</creatorcontrib><creatorcontrib>Eutsey, Rory A</creatorcontrib><creatorcontrib>Prentice, Jojo A</creatorcontrib><creatorcontrib>Yerneni, Saigopalakrishna S</creatorcontrib><creatorcontrib>Arun, Ashni</creatorcontrib><creatorcontrib>Bridges, Andrew A</creatorcontrib><creatorcontrib>Rosch, Jason W</creatorcontrib><creatorcontrib>Conway, James F</creatorcontrib><creatorcontrib>Campbell, Phil</creatorcontrib><creatorcontrib>Hiller, N Luisa</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><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>mSphere</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Werner Lass, Sarah</au><au>Smith, Bailey E</au><au>Camphire, Shaw</au><au>Eutsey, Rory A</au><au>Prentice, Jojo A</au><au>Yerneni, Saigopalakrishna S</au><au>Arun, Ashni</au><au>Bridges, Andrew A</au><au>Rosch, Jason W</au><au>Conway, James F</au><au>Campbell, Phil</au><au>Hiller, N Luisa</au><au>Tringe, Susannah Green</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Pneumococcal extracellular vesicles mediate horizontal gene transfer via the transformation machinery</atitle><jtitle>mSphere</jtitle><stitle>mSphere</stitle><addtitle>mSphere</addtitle><date>2024-12-19</date><risdate>2024</risdate><volume>9</volume><issue>12</issue><spage>e0072724</spage><pages>e0072724-</pages><issn>2379-5042</issn><eissn>2379-5042</eissn><abstract>Bacterial cells secrete extracellular vesicles (EVs), the function of which is a matter of intense investigation. 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| subjects | antibiotic resistance Bacteriology competence DNA, Bacterial - genetics Drug Resistance, Bacterial - genetics extracellular vesicle Extracellular Vesicles - genetics Extracellular Vesicles - metabolism Gene Transfer, Horizontal horizontal gene transfer Humans Research Article Streptococcus pneumoniae Streptococcus pneumoniae - genetics transformation Transformation, Bacterial |
| title | Pneumococcal extracellular vesicles mediate horizontal gene transfer via the transformation machinery |
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