Antigen 43 associated with Escherichia coli membrane vesicles contributes to bacterial cell association and biofilm formation
ABSTRACT Bacterial membrane vesicles (MVs) are produced by all bacteria and contribute to numerous bacterial functions due to their ability to package and transfer bacterial cargo. In doing so, MVs have been shown to facilitate horizontal gene transfer, mediate antimicrobial activity, and promote bi...
Saved in:
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2025-03-01
|
| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.01890-24 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1850235213692534784 |
|---|---|
| author | Lauren Zavan Lilian Hor Ella L. Johnston Jason Paxman Begoña Heras Maria Kaparakis‑Liaskos |
| author_facet | Lauren Zavan Lilian Hor Ella L. Johnston Jason Paxman Begoña Heras Maria Kaparakis‑Liaskos |
| author_sort | Lauren Zavan |
| collection | DOAJ |
| description | ABSTRACT Bacterial membrane vesicles (MVs) are produced by all bacteria and contribute to numerous bacterial functions due to their ability to package and transfer bacterial cargo. In doing so, MVs have been shown to facilitate horizontal gene transfer, mediate antimicrobial activity, and promote biofilm formation. Uropathogenic Escherichia coli is a pathogenic Gram-negative organism that persists in the urinary tract of its host due to its ability to form persistent, antibiotic-resistant biofilms. The formation of these biofilms is dependent upon proteins such as Antigen 43 (Ag43), which belongs to the widespread Autotransporter group of bacterial surface proteins. In E. coli, the autotransporter Ag43 has been shown to contribute to bacterial cell aggregation and biofilm formation via self-association of Ag43 between neighboring Ag43-expressing bacteria. As MVs package bacterial proteins, we investigated whether MVs produced by E. coli contained Ag43, and the ability of Ag43-expressing MVs to facilitate cell aggregation and biofilm formation. We showed that Ag43 expressing E. coli produced MVs that contained Ag43 on their surface and had an enhanced ability to bind to E. coli bacteria. Furthermore, we demonstrated that the addition of Ag43-containing MVs to Ag43-expressing E. coli significantly enhanced biofilm formation. These findings reveal the contribution of MVs harboring autotransporters in promoting bacterial aggregation and enhancing biofilm formation, highlighting the impact of MVs and their specific composition to bacterial adaptation and pathogenesis.IMPORTANCEAutotransporter proteins are the largest family of outer membrane and secreted proteins in Gram-negative bacteria which contribute to pathogenesis by promoting aggregation, biofilm formation, persistence, and cytotoxicity. Although the roles of bacterial autotransporters are well known, the ability of bacterial membrane vesicles (MVs) naturally released from the surface of bacteria to contain autotransporters and their role in promoting virulence remains less investigated. Our findings reveal that MVs produced by E. coli contain the autotransporter protein Ag43. Furthermore, we show that Ag43-containing MVs function to enhance bacterial cell interactions and biofilm formation. By demonstrating the ability of MVs to carry functional autotransporter adhesins, this work highlights the importance of MVs in disseminating autotransporters beyond the bacterial cell membrane to ultimately promote cellular interactions and enhance biofilm development. Overall, these findings have significant implications in furthering our understanding of the numerous ways in which MVs can facilitate bacterial persistence and pathogenesis. |
| format | Article |
| id | doaj-art-ec88b565586d4043a9adf81d91767e01 |
| institution | OA Journals |
| issn | 2165-0497 |
| language | English |
| publishDate | 2025-03-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj-art-ec88b565586d4043a9adf81d91767e012025-08-20T02:02:20ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972025-03-0113310.1128/spectrum.01890-24Antigen 43 associated with Escherichia coli membrane vesicles contributes to bacterial cell association and biofilm formationLauren Zavan0Lilian Hor1Ella L. Johnston2Jason Paxman3Begoña Heras4Maria Kaparakis‑Liaskos5Department of Microbiology, Anatomy, Physiology, and Pharmacology, La Trobe University, Melbourne, Victoria, AustraliaDepartment of Microbiology, Anatomy, Physiology, and Pharmacology, La Trobe University, Melbourne, Victoria, AustraliaDepartment of Microbiology, Anatomy, Physiology, and Pharmacology, La Trobe University, Melbourne, Victoria, AustraliaDepartment of Biochemistry and Chemistry, La Trobe Institute for Molecular Sciences, La Trobe University, Melbourne, Victoria, AustraliaDepartment of Biochemistry and Chemistry, La Trobe Institute for Molecular Sciences, La Trobe University, Melbourne, Victoria, AustraliaDepartment of Microbiology, Anatomy, Physiology, and Pharmacology, La Trobe University, Melbourne, Victoria, AustraliaABSTRACT Bacterial membrane vesicles (MVs) are produced by all bacteria and contribute to numerous bacterial functions due to their ability to package and transfer bacterial cargo. In doing so, MVs have been shown to facilitate horizontal gene transfer, mediate antimicrobial activity, and promote biofilm formation. Uropathogenic Escherichia coli is a pathogenic Gram-negative organism that persists in the urinary tract of its host due to its ability to form persistent, antibiotic-resistant biofilms. The formation of these biofilms is dependent upon proteins such as Antigen 43 (Ag43), which belongs to the widespread Autotransporter group of bacterial surface proteins. In E. coli, the autotransporter Ag43 has been shown to contribute to bacterial cell aggregation and biofilm formation via self-association of Ag43 between neighboring Ag43-expressing bacteria. As MVs package bacterial proteins, we investigated whether MVs produced by E. coli contained Ag43, and the ability of Ag43-expressing MVs to facilitate cell aggregation and biofilm formation. We showed that Ag43 expressing E. coli produced MVs that contained Ag43 on their surface and had an enhanced ability to bind to E. coli bacteria. Furthermore, we demonstrated that the addition of Ag43-containing MVs to Ag43-expressing E. coli significantly enhanced biofilm formation. These findings reveal the contribution of MVs harboring autotransporters in promoting bacterial aggregation and enhancing biofilm formation, highlighting the impact of MVs and their specific composition to bacterial adaptation and pathogenesis.IMPORTANCEAutotransporter proteins are the largest family of outer membrane and secreted proteins in Gram-negative bacteria which contribute to pathogenesis by promoting aggregation, biofilm formation, persistence, and cytotoxicity. Although the roles of bacterial autotransporters are well known, the ability of bacterial membrane vesicles (MVs) naturally released from the surface of bacteria to contain autotransporters and their role in promoting virulence remains less investigated. Our findings reveal that MVs produced by E. coli contain the autotransporter protein Ag43. Furthermore, we show that Ag43-containing MVs function to enhance bacterial cell interactions and biofilm formation. By demonstrating the ability of MVs to carry functional autotransporter adhesins, this work highlights the importance of MVs in disseminating autotransporters beyond the bacterial cell membrane to ultimately promote cellular interactions and enhance biofilm development. Overall, these findings have significant implications in furthering our understanding of the numerous ways in which MVs can facilitate bacterial persistence and pathogenesis.https://journals.asm.org/doi/10.1128/spectrum.01890-24bacterial membrane vesiclesouter membrane vesiclesautotransportersbiofilmAntigen 43 |
| spellingShingle | Lauren Zavan Lilian Hor Ella L. Johnston Jason Paxman Begoña Heras Maria Kaparakis‑Liaskos Antigen 43 associated with Escherichia coli membrane vesicles contributes to bacterial cell association and biofilm formation Microbiology Spectrum bacterial membrane vesicles outer membrane vesicles autotransporters biofilm Antigen 43 |
| title | Antigen 43 associated with Escherichia coli membrane vesicles contributes to bacterial cell association and biofilm formation |
| title_full | Antigen 43 associated with Escherichia coli membrane vesicles contributes to bacterial cell association and biofilm formation |
| title_fullStr | Antigen 43 associated with Escherichia coli membrane vesicles contributes to bacterial cell association and biofilm formation |
| title_full_unstemmed | Antigen 43 associated with Escherichia coli membrane vesicles contributes to bacterial cell association and biofilm formation |
| title_short | Antigen 43 associated with Escherichia coli membrane vesicles contributes to bacterial cell association and biofilm formation |
| title_sort | antigen 43 associated with escherichia coli membrane vesicles contributes to bacterial cell association and biofilm formation |
| topic | bacterial membrane vesicles outer membrane vesicles autotransporters biofilm Antigen 43 |
| url | https://journals.asm.org/doi/10.1128/spectrum.01890-24 |
| work_keys_str_mv | AT laurenzavan antigen43associatedwithescherichiacolimembranevesiclescontributestobacterialcellassociationandbiofilmformation AT lilianhor antigen43associatedwithescherichiacolimembranevesiclescontributestobacterialcellassociationandbiofilmformation AT ellaljohnston antigen43associatedwithescherichiacolimembranevesiclescontributestobacterialcellassociationandbiofilmformation AT jasonpaxman antigen43associatedwithescherichiacolimembranevesiclescontributestobacterialcellassociationandbiofilmformation AT begonaheras antigen43associatedwithescherichiacolimembranevesiclescontributestobacterialcellassociationandbiofilmformation AT mariakaparakisliaskos antigen43associatedwithescherichiacolimembranevesiclescontributestobacterialcellassociationandbiofilmformation |