Cross-species communication via agr controls phage susceptibility in Staphylococcus aureus
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Bacteria use quorum sensing (QS) to coordinate group behavior in response to cell density, and some bacterial viruses (phages) also respond to QS. In Staphylococcus aureus, the agr-encoded QS system relies on accumulation of auto-inducing cyclic peptides (AIPs). Other staphylococci also produce AIPs of which many inhibit S. aureus agr. We show that agr induction reduces expression of tarM, encoding a glycosyltransferase responsible for α-N-acetylglucosamine modification of the major S. aureus phage receptor, the wall teichoic acids. This allows lytic phage Stab20 and related phages to infect and kill S. aureus. However, in mixed communities, producers of inhibitory AIPs like S. haemolyticus, S. caprae, and S. pseudintermedius inhibit S. aureus agr, thereby impeding phage infection. Our results demonstrate that cross-species interactions dramatically impact phage susceptibility. These interactions likely influence microbial ecology and impact the efficacy of phages in medical and biotechnological applications such as phage therapy.
| Originalsprog | Engelsk |
|---|---|
| Artikelnummer | 113154 |
| Tidsskrift | Cell Reports |
| Vol/bind | 42 |
| Udgave nummer | 9 |
| ISSN | 2211-1247 |
| DOI | |
| Status | Udgivet - 2023 |
Bibliografisk note
Funding Information:
We thank Prof. Mikael Skurnik of the Department of Bacteriology and Immunology at University of Helsinki for providing phage Stab20, Prof. Friedrich Götz of the Interfaculty Institute for Microbiology and Infection Medicine (IMIT) at University of Tübingen for providing S. pseudintermedius strain ED99 and the mutant, and Prof. Mark Enright of Department of Life Sciences at Manchester Metropolitan University for providing phage vB_SauM_EW18, vB_SauM_EW26, vB_SauM_EW29, and vB_SauM_EW72. Also, we thank Dr. A. Robin Temming (Amsterdam UMC, the Netherlands) for the production of the WTA-specific and B12 control fragments, Prof. Christian A. Olsen (Department of Drug Design and Pharmacology, University of Copenhagen) for synthetic peptides, and Assistant Prof. Nina M. Høyland-Kroghbo (Department of Plant and Environmental Science, University of Copenhagen) for valuable input to the work. J.Y. acknowledges the China Scholarship Council for financial support. A.P. acknowledges financial support from Deutsche Forschungsgemeinschaft, (SPP 2330 and PE 805/7-1) and infrastructural funding from the Cluster of Excellence EXC 2124 “Controlling Microbes to Fight Infections” project ID 390838134. H.I. and J.B. acknowledge financial support from the Independent Research Fund, Denmark, grant number 0135-00271B. Schematic illustrations were created with BioRender (https://BioRender.com). Conceptualization, J.Y. J.Z.B. and H.I.; methodology, J.Y. J.Z.B. B.S.B. M.S.B. A.P. and H.I.; investigation, J.Y. J.Z.B. J.K. E.L. S.F.S. and T.G.; formal analysis, J.Y. J.Z.B. J.K. and H.I.; visualization, J.Y. J.Z.B. and H.I.; writing – original draft, J.Y.; writing – review & editing, J.Y. J.Z.B. and H.I.; supervision, J.Z.B. and H.I. funding acquisition, J.Z.B. and H.I. The authors declare no competing interests.
Funding Information:
We thank Prof. Mikael Skurnik of the Department of Bacteriology and Immunology at University of Helsinki for providing phage Stab20, Prof. Friedrich Götz of the Interfaculty Institute for Microbiology and Infection Medicine (IMIT) at University of Tübingen for providing S. pseudintermedius strain ED99 and the mutant, and Prof. Mark Enright of Department of Life Sciences at Manchester Metropolitan University for providing phage vB_SauM_EW18, vB_SauM_EW26, vB_SauM_EW29, and vB_SauM_EW72. Also, we thank Dr. A. Robin Temming (Amsterdam UMC, the Netherlands) for the production of the WTA-specific and B12 control fragments, Prof. Christian A. Olsen (Department of Drug Design and Pharmacology, University of Copenhagen) for synthetic peptides, and Assistant Prof. Nina M. Høyland-Kroghbo (Department of Plant and Environmental Science, University of Copenhagen) for valuable input to the work. J.Y. acknowledges the China Scholarship Council for financial support. A.P. acknowledges financial support from Deutsche Forschungsgemeinschaft , ( SPP 2330 and PE 805/7-1 ) and infrastructural funding from the Cluster of Excellence EXC 2124 “Controlling Microbes to Fight Infections” project ID 390838134. H.I. and J.B. acknowledge financial support from the Independent Research Fund , Denmark, grant number 0135-00271B . Schematic illustrations were created with BioRender ( https://BioRender.com ).
Publisher Copyright:
© 2023 The Authors
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