Stenotrophomonas maltophilia affects the gene expression profiles of the major pathogens Pseudomonas aeruginosa and Staphylococcus aureus in an in vitro multispecies biofilm model
ABSTRACT Stenotrophomonas maltophilia is an emerging lung pathogen. In its natural habitat, it lives together with Pseudomonas aeruginosa, Staphylococcus aureus, and other pathogens. Here, we provide the first evidence that S. maltophilia interferes with the metabolism and physiology of other specie...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-12-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.00859-23 |
| _version_ | 1797393668914544640 |
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| author | Ifey Alio Raphael Moll Tim Hoffmann Uwe Mamat Ulrich E. Schaible Kai Pappenfort Malik Alawi Marcel Schie Roland Thünauer Johanna Stamm Holger Rohde Wolfgang R. Streit |
| author_facet | Ifey Alio Raphael Moll Tim Hoffmann Uwe Mamat Ulrich E. Schaible Kai Pappenfort Malik Alawi Marcel Schie Roland Thünauer Johanna Stamm Holger Rohde Wolfgang R. Streit |
| author_sort | Ifey Alio |
| collection | DOAJ |
| description | ABSTRACT Stenotrophomonas maltophilia is an emerging lung pathogen. In its natural habitat, it lives together with Pseudomonas aeruginosa, Staphylococcus aureus, and other pathogens. Here, we provide the first evidence that S. maltophilia interferes with the metabolism and physiology of other species when co-cultivated in dual- and triple-species biofilms. CSLM analyses implied that S. maltophilia was in general the first to colonize the bottom layer in multispecies biofilms. Structural patterns and niche formation resulting in distinct layer formation within the biofilm were observed on a species- and strain-dependent level for S. maltophilia. Furthermore, gene expression profiles of S. aureus and P. aeruginosa were strongly affected by the presence of S. maltophilia. The S. maltophilia metabolism was mostly fermentative in multispecies biofilms with varying sets of cytochromes used for anaerobic respiration. One of the most striking observations was that S. maltophilia interfered with P. aeruginosa LasI-dependent expression of quorum sensing-regulated pathogenicity factors in multispecies biofilms. IMPORTANCE In the past, studies have focused on bacterial pathogenicity in mono-species infections, in part ignoring the clinical relevance of diseases caused by more than one pathogen (i.e., polymicrobial infections). However, it is now common knowledge that multiple bacteria species are often involved in the course of an infection. For treatment of such infections, it is absolutely important to understand the dynamics of species interactions at possible infection sites and the molecular mechanisms behind these interactions. Here, we studied the impact of Stenotrophomonas maltophilia on its commensals Pseudomonas aeruginosa and Staphylococcus aureus in multispecies biofilms. We analyzed the 3D structural architectures of dual- and triple-species biofilms, niche formation within the biofilms, and the interspecies interactions on a molecular level. RNAseq data identified key genes involved in multispecies biofilm formation and interaction as potential drug targets for the clinical combat of multispecies infection with these major pathogens. |
| first_indexed | 2024-03-09T00:06:10Z |
| format | Article |
| id | doaj.art-57400bd64a3442158687fd416368cedd |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-09T00:06:10Z |
| publishDate | 2023-12-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-57400bd64a3442158687fd416368cedd2023-12-12T13:17:18ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-12-0111610.1128/spectrum.00859-23Stenotrophomonas maltophilia affects the gene expression profiles of the major pathogens Pseudomonas aeruginosa and Staphylococcus aureus in an in vitro multispecies biofilm modelIfey Alio0Raphael Moll1Tim Hoffmann2Uwe Mamat3Ulrich E. Schaible4Kai Pappenfort5Malik Alawi6Marcel Schie7Roland Thünauer8Johanna Stamm9Holger Rohde10Wolfgang R. Streit11Department of Microbiology and Biotechnology, University Hamburg , Hamburg, GermanyDepartment of Microbiology and Biotechnology, University Hamburg , Hamburg, GermanyDepartment of Microbiology and Biotechnology, University Hamburg , Hamburg, GermanyCellular Microbiology, Priority Research Area Infections, Research Center Borstel, Leibniz Lung Center,Leibniz Research Alliance Infection , Borstel Gemany , Borstel, GermanyCellular Microbiology, Priority Research Area Infections, Research Center Borstel, Leibniz Lung Center,Leibniz Research Alliance Infection , Borstel Gemany , Borstel, GermanyInstitute of Microbiology, Friedrich Schiller University of Jena , Jena, GermanyBioinformatics Core, UKE Hamburg , Hamburg, GermanyLIV, Leibniz Institute of Experimental Virology , Hamburg, GermanyLIV, Leibniz Institute of Experimental Virology , Hamburg, GermanyInstitute for Medical Microbiology, Virology and Hygiene, UKE, Eppendorf , Hamburg, GermanyInstitute for Medical Microbiology, Virology and Hygiene, UKE, Eppendorf , Hamburg, GermanyDepartment of Microbiology and Biotechnology, University Hamburg , Hamburg, GermanyABSTRACT Stenotrophomonas maltophilia is an emerging lung pathogen. In its natural habitat, it lives together with Pseudomonas aeruginosa, Staphylococcus aureus, and other pathogens. Here, we provide the first evidence that S. maltophilia interferes with the metabolism and physiology of other species when co-cultivated in dual- and triple-species biofilms. CSLM analyses implied that S. maltophilia was in general the first to colonize the bottom layer in multispecies biofilms. Structural patterns and niche formation resulting in distinct layer formation within the biofilm were observed on a species- and strain-dependent level for S. maltophilia. Furthermore, gene expression profiles of S. aureus and P. aeruginosa were strongly affected by the presence of S. maltophilia. The S. maltophilia metabolism was mostly fermentative in multispecies biofilms with varying sets of cytochromes used for anaerobic respiration. One of the most striking observations was that S. maltophilia interfered with P. aeruginosa LasI-dependent expression of quorum sensing-regulated pathogenicity factors in multispecies biofilms. IMPORTANCE In the past, studies have focused on bacterial pathogenicity in mono-species infections, in part ignoring the clinical relevance of diseases caused by more than one pathogen (i.e., polymicrobial infections). However, it is now common knowledge that multiple bacteria species are often involved in the course of an infection. For treatment of such infections, it is absolutely important to understand the dynamics of species interactions at possible infection sites and the molecular mechanisms behind these interactions. Here, we studied the impact of Stenotrophomonas maltophilia on its commensals Pseudomonas aeruginosa and Staphylococcus aureus in multispecies biofilms. We analyzed the 3D structural architectures of dual- and triple-species biofilms, niche formation within the biofilms, and the interspecies interactions on a molecular level. RNAseq data identified key genes involved in multispecies biofilm formation and interaction as potential drug targets for the clinical combat of multispecies infection with these major pathogens.https://journals.asm.org/doi/10.1128/spectrum.00859-23mixed species biofilmstranscriptome analysispathogens |
| spellingShingle | Ifey Alio Raphael Moll Tim Hoffmann Uwe Mamat Ulrich E. Schaible Kai Pappenfort Malik Alawi Marcel Schie Roland Thünauer Johanna Stamm Holger Rohde Wolfgang R. Streit Stenotrophomonas maltophilia affects the gene expression profiles of the major pathogens Pseudomonas aeruginosa and Staphylococcus aureus in an in vitro multispecies biofilm model Microbiology Spectrum mixed species biofilms transcriptome analysis pathogens |
| title | Stenotrophomonas maltophilia affects the gene expression profiles of the major pathogens Pseudomonas aeruginosa and Staphylococcus aureus in an in vitro multispecies biofilm model |
| title_full | Stenotrophomonas maltophilia affects the gene expression profiles of the major pathogens Pseudomonas aeruginosa and Staphylococcus aureus in an in vitro multispecies biofilm model |
| title_fullStr | Stenotrophomonas maltophilia affects the gene expression profiles of the major pathogens Pseudomonas aeruginosa and Staphylococcus aureus in an in vitro multispecies biofilm model |
| title_full_unstemmed | Stenotrophomonas maltophilia affects the gene expression profiles of the major pathogens Pseudomonas aeruginosa and Staphylococcus aureus in an in vitro multispecies biofilm model |
| title_short | Stenotrophomonas maltophilia affects the gene expression profiles of the major pathogens Pseudomonas aeruginosa and Staphylococcus aureus in an in vitro multispecies biofilm model |
| title_sort | stenotrophomonas maltophilia affects the gene expression profiles of the major pathogens pseudomonas aeruginosa and staphylococcus aureus in an in vitro multispecies biofilm model |
| topic | mixed species biofilms transcriptome analysis pathogens |
| url | https://journals.asm.org/doi/10.1128/spectrum.00859-23 |
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