Matrix polysaccharides and SiaD diguanylate cyclase alter community structure and competitiveness of Pseudomonas aeruginosa during dual-species biofilm development with Staphylococcus aureus
Mixed-species biofilms display a number of emergent properties, including enhanced antimicrobial tolerance and communal metabolism. These properties may depend on interspecies relationships and the structure of the biofilm. However, the contribution of specific matrix components to emergent properti...
| Main Authors: | , , , , , , , , , |
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| Format: | Journal Article |
| Language: | English |
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2019
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| Online Access: | https://hdl.handle.net/10356/87103 http://hdl.handle.net/10220/49870 |
| _version_ | 1824456403338657792 |
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| author | Chew, Su Chuen Yam, Joey Kuok Hoong Matysik, Artur Seng, Zi Jing Klebensberger, Janosch Givskov, Michael Doyle, Patrick Rice, Scott A. Yang, Liang Kjelleberg, Staffan |
| author2 | Ruby, Edward G. |
| author_facet | Ruby, Edward G. Chew, Su Chuen Yam, Joey Kuok Hoong Matysik, Artur Seng, Zi Jing Klebensberger, Janosch Givskov, Michael Doyle, Patrick Rice, Scott A. Yang, Liang Kjelleberg, Staffan |
| author_sort | Chew, Su Chuen |
| collection | NTU |
| description | Mixed-species biofilms display a number of emergent properties, including enhanced antimicrobial tolerance and communal metabolism. These properties may depend on interspecies relationships and the structure of the biofilm. However, the contribution of specific matrix components to emergent properties of mixed-species biofilms remains poorly understood. Using a dual-species biofilm community formed by the opportunistic pathogens Pseudomonas aeruginosa and Staphylococcus aureus, we found that whilst neither Pel nor Psl polysaccharides, produced by P. aeruginosa, affect relative species abundance in mature P. aeruginosa and S. aureus biofilms, Psl production is associated with increased P. aeruginosa abundance and reduced S. aureus aggregation in the early stages of biofilm formation. Our data suggest that the competitive effect of Psl is not associated with its structural role in cross-linking the matrix and adhering to P. aeruginosa cells but is instead mediated through the activation of the diguanylate cyclase SiaD. This regulatory control was also found to be independent of the siderophore pyoverdine and Pseudomonas quinolone signal, which have previously been proposed to reduce S. aureus viability by inducing lactic acid fermentation-based growth. In contrast to the effect mediated by Psl, Pel reduced the effective crosslinking of the biofilm matrix and facilitated superdiffusivity in microcolony regions. These changes in matrix cross-linking enhance biofilm surface spreading and expansion of microcolonies in the later stages of biofilm development, improving overall dual-species biofilm growth and increasing biovolume severalfold. Thus, the biofilm matrix and regulators associated with matrix production play essential roles in mixed-species biofilm interactions. |
| first_indexed | 2025-02-19T03:53:33Z |
| format | Journal Article |
| id | ntu-10356/87103 |
| institution | Nanyang Technological University |
| language | English |
| last_indexed | 2025-02-19T03:53:33Z |
| publishDate | 2019 |
| record_format | dspace |
| spelling | ntu-10356/871032020-09-21T11:36:14Z Matrix polysaccharides and SiaD diguanylate cyclase alter community structure and competitiveness of Pseudomonas aeruginosa during dual-species biofilm development with Staphylococcus aureus Chew, Su Chuen Yam, Joey Kuok Hoong Matysik, Artur Seng, Zi Jing Klebensberger, Janosch Givskov, Michael Doyle, Patrick Rice, Scott A. Yang, Liang Kjelleberg, Staffan Ruby, Edward G. School of Biological Sciences Singapore Centre for Environmental Life Sciences and Engineering Pseudomonas Aeruginosa SiaD Science::Biological sciences Mixed-species biofilms display a number of emergent properties, including enhanced antimicrobial tolerance and communal metabolism. These properties may depend on interspecies relationships and the structure of the biofilm. However, the contribution of specific matrix components to emergent properties of mixed-species biofilms remains poorly understood. Using a dual-species biofilm community formed by the opportunistic pathogens Pseudomonas aeruginosa and Staphylococcus aureus, we found that whilst neither Pel nor Psl polysaccharides, produced by P. aeruginosa, affect relative species abundance in mature P. aeruginosa and S. aureus biofilms, Psl production is associated with increased P. aeruginosa abundance and reduced S. aureus aggregation in the early stages of biofilm formation. Our data suggest that the competitive effect of Psl is not associated with its structural role in cross-linking the matrix and adhering to P. aeruginosa cells but is instead mediated through the activation of the diguanylate cyclase SiaD. This regulatory control was also found to be independent of the siderophore pyoverdine and Pseudomonas quinolone signal, which have previously been proposed to reduce S. aureus viability by inducing lactic acid fermentation-based growth. In contrast to the effect mediated by Psl, Pel reduced the effective crosslinking of the biofilm matrix and facilitated superdiffusivity in microcolony regions. These changes in matrix cross-linking enhance biofilm surface spreading and expansion of microcolonies in the later stages of biofilm development, improving overall dual-species biofilm growth and increasing biovolume severalfold. Thus, the biofilm matrix and regulators associated with matrix production play essential roles in mixed-species biofilm interactions. NRF (Natl Research Foundation, S’pore) MOE (Min. of Education, S’pore) Published version 2019-09-04T07:38:22Z 2019-12-06T16:35:15Z 2019-09-04T07:38:22Z 2019-12-06T16:35:15Z 2018 Journal Article Chew, S. C., Yam, J. K. H., Matysik, A., Seng, Z. J., Klebensberger, J., Givskov, M., . . . Kjelleberg, S. (2018). Matrix polysaccharides and SiaD diguanylate cyclase alter community structure and competitiveness of Pseudomonas aeruginosa during dual-species biofilm development with Staphylococcus aureus. mBio, 9(6), e00585-18-. doi:10.1128/mBio.00585-18 https://hdl.handle.net/10356/87103 http://hdl.handle.net/10220/49870 10.1128/mBio.00585-18 en mBio © 2018 Chew et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license. 16 p. application/pdf |
| spellingShingle | Pseudomonas Aeruginosa SiaD Science::Biological sciences Chew, Su Chuen Yam, Joey Kuok Hoong Matysik, Artur Seng, Zi Jing Klebensberger, Janosch Givskov, Michael Doyle, Patrick Rice, Scott A. Yang, Liang Kjelleberg, Staffan Matrix polysaccharides and SiaD diguanylate cyclase alter community structure and competitiveness of Pseudomonas aeruginosa during dual-species biofilm development with Staphylococcus aureus |
| title | Matrix polysaccharides and SiaD diguanylate cyclase alter community structure and competitiveness of Pseudomonas aeruginosa during dual-species biofilm development with Staphylococcus aureus |
| title_full | Matrix polysaccharides and SiaD diguanylate cyclase alter community structure and competitiveness of Pseudomonas aeruginosa during dual-species biofilm development with Staphylococcus aureus |
| title_fullStr | Matrix polysaccharides and SiaD diguanylate cyclase alter community structure and competitiveness of Pseudomonas aeruginosa during dual-species biofilm development with Staphylococcus aureus |
| title_full_unstemmed | Matrix polysaccharides and SiaD diguanylate cyclase alter community structure and competitiveness of Pseudomonas aeruginosa during dual-species biofilm development with Staphylococcus aureus |
| title_short | Matrix polysaccharides and SiaD diguanylate cyclase alter community structure and competitiveness of Pseudomonas aeruginosa during dual-species biofilm development with Staphylococcus aureus |
| title_sort | matrix polysaccharides and siad diguanylate cyclase alter community structure and competitiveness of pseudomonas aeruginosa during dual species biofilm development with staphylococcus aureus |
| topic | Pseudomonas Aeruginosa SiaD Science::Biological sciences |
| url | https://hdl.handle.net/10356/87103 http://hdl.handle.net/10220/49870 |
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