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Formation of a biofilm matrix network shapes polymicrobial interactions

The ISME Journal volume 17, pages 467–477 (2023)Cite this article

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Abstract

Staphylococcus aureus colonizes the same ecological niche as many commensals. However, little is known about how such commensals modulate staphylococcal fitness and persistence. Here we report a new mechanism that mediates dynamic interactions between a commensal streptococcus and S. aureus. Commensal Streptococcus parasanguinis significantly increased the staphylococcal biofilm formation in vitro and enhanced its colonization in vivo. A streptococcal biofilm-associated protein BapA1, not fimbriae-associated protein Fap1, is essential for dual-species biofilm formation. On the other side, three staphylococcal virulence determinants responsible for the BapA1-dependent dual-species biofilm formation were identified by screening a staphylococcal transposon mutant library. The corresponding staphylococcal mutants lacked binding to recombinant BapA1 (rBapA1) due to lower amounts of eDNA in their culture supernatants and were defective in biofilm formation with streptococcus. The rBapA1 selectively colocalized with eDNA within the dual-species biofilm and bound to eDNA in vitro, highlighting the contributions of the biofilm matrix formed between streptococcal BapA1 and staphylococcal eDNA to dual-species biofilm formation. These findings have revealed an additional new mechanism through which an interspecies biofilm matrix network mediates polymicrobial interactions.

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Fig. 1: S. parasanguinis promotes S. aureus biofilm formation, and BapA1 is required for the enhanced dual-species biofilms.
Fig. 2: Recombinant BapA1 promotes S. aureus biofilm formation.
Fig. 3: S. parasanguinis promotes the colonization of S. aureus in flies.
Fig. 4: Staphylococcal virulence factors, SarA, CodY, and Atl, are required for dual-species biofilm formation.
Fig. 5: Staphylococcal biofilm cells interact with rBapA1-C.
Fig. 6: eDNA is required for the dual-species biofilm formation.
Fig. 7: BapA1 colocalizes with eDNA within BapA1-mediated S. aureus biofilms and binds to staphylococcal DNA in vitro.

Data availability

All data are available in the main text or Supplementary materials.

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Acknowledgements

This study was supported in part by NIH/NIDCR R01 DE017954 (HW). Nebraska Transposon Mutant Library (NTML) Screening Array, NR-48501, was provided by the Network on Antimicrobial Resistance in Staphylococcus aureus (NARSA) for distribution by BEI Resources, NIAID, NIH.

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Authors and Affiliations

  1. Departments of Pediatric Dentistry and Microbiology, University of Alabama at Birmingham Schools of Dentistry and Medicine, Birmingham, Alabama, 35294, USA

    Lijun Wang, Hongxia Wang, Hua Zhang & Hui Wu

  2. Department of Laboratory Medicine, Beijing Tsinghua Changgung Hospital, School of Clinical Medicine, Tsinghua University, 102218, Beijing, China

    Lijun Wang

  3. Department of Integrative Biomedical and Diagnostic Sciences, Oregon Health and Science University School of Dentistry, Portland, OR, 97239, USA

    Hua Zhang & Hui Wu

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HW conceived and supervised the project. HW and LW designed the experiments. LW, HW, HZ performed experiments and analyzed data. LW and HW wrote the manuscript.

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Wang, L., Wang, H., Zhang, H. et al. Formation of a biofilm matrix network shapes polymicrobial interactions. ISME J 17, 467–477 (2023). https://doi.org/10.1038/s41396-023-01362-8

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