Surface colonization by Flavobacterium johnsoniae promotes its survival in a model microbial community
ABSTRACT Flavobacterium johnsoniae is a ubiquitous soil and rhizosphere bacterium, but despite its abundance, the factors contributing to its success in communities are poorly understood. Using a model microbial community, The Hitchhikers of the Rhizosphere (THOR), we determined the effects of colon...
| Главные авторы: | , , , , , , , |
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| Формат: | Статья |
| Язык: | English |
| Опубликовано: |
American Society for Microbiology
2024-03-01
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| Серии: | mBio |
| Предметы: | |
| Online-ссылка: | https://journals.asm.org/doi/10.1128/mbio.03428-23 |
| _version_ | 1827150311054114816 |
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| author | Shruthi Magesh Amanda I. Hurley Julia F. Nepper Marc G. Chevrette Jonathan H. Schrope Chao Li David J. Beebe Jo Handelsman |
| author_facet | Shruthi Magesh Amanda I. Hurley Julia F. Nepper Marc G. Chevrette Jonathan H. Schrope Chao Li David J. Beebe Jo Handelsman |
| author_sort | Shruthi Magesh |
| collection | DOAJ |
| description | ABSTRACT Flavobacterium johnsoniae is a ubiquitous soil and rhizosphere bacterium, but despite its abundance, the factors contributing to its success in communities are poorly understood. Using a model microbial community, The Hitchhikers of the Rhizosphere (THOR), we determined the effects of colonization on the fitness of F. johnsoniae in the community. Insertion sequencing, a massively parallel transposon mutant screen, on sterile sand identified 25 genes likely to be important for surface colonization. We constructed in-frame deletions of candidate genes predicted to be involved in cell membrane biogenesis, motility, signal transduction, and transport of amino acids and lipids. All mutants poorly colonized sand, glass, and polystyrene and produced less biofilm than the wild type, indicating the importance of the targeted genes in surface colonization. Eight of the nine colonization-defective mutants were also unable to form motile biofilms or zorbs, thereby suggesting that the affected genes play a role in group movement and linking stationary and motile biofilm formation genetically. Furthermore, we showed that the deletion of colonization genes in F. johnsoniae affected its behavior and survival in THOR on surfaces, suggesting that the same traits are required for success in a multispecies microbial community. Our results provide insight into the mechanisms of surface colonization by F. johnsoniae and form the basis for further understanding its ecology in the rhizosphere.IMPORTANCEMicrobial communities direct key environmental processes through multispecies interactions. Understanding these interactions is vital for manipulating microbiomes to promote health in human, environmental, and agricultural systems. However, microbiome complexity can hinder our understanding of the underlying mechanisms in microbial community interactions. As a first step toward unraveling these interactions, we explored the role of surface colonization in microbial community interactions using The Hitchhikers Of the Rhizosphere (THOR), a genetically tractable model community of three bacterial species, Flavobacterium johnsoniae, Pseudomonas koreensis, and Bacillus cereus. We identified F. johnsoniae genes important for surface colonization in solitary conditions and in the THOR community. Understanding the mechanisms that promote the success of bacteria in microbial communities brings us closer to targeted manipulations to achieve outcomes that benefit agriculture, the environment, and human health. |
| first_indexed | 2024-04-25T00:10:18Z |
| format | Article |
| id | doaj.art-828b12bdf3434465b71d106bf9f35264 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2025-03-20T21:32:03Z |
| publishDate | 2024-03-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-828b12bdf3434465b71d106bf9f352642024-08-11T18:12:03ZengAmerican Society for MicrobiologymBio2150-75112024-03-0115310.1128/mbio.03428-23Surface colonization by Flavobacterium johnsoniae promotes its survival in a model microbial communityShruthi Magesh0Amanda I. Hurley1Julia F. Nepper2Marc G. Chevrette3Jonathan H. Schrope4Chao Li5David J. Beebe6Jo Handelsman7Department of Plant Pathology, Wisconsin Institute for Discovery, University of Wisconsin-Madison, Madison, Wisconsin, USADepartment of Plant Pathology, Wisconsin Institute for Discovery, University of Wisconsin-Madison, Madison, Wisconsin, USADepartment of Plant Pathology, Wisconsin Institute for Discovery, University of Wisconsin-Madison, Madison, Wisconsin, USADepartment of Microbiology and Cell Science, University of Florida, Gainesville, Florida, USADepartment of Biomedical Engineering, University of Wisconsin Madison, Madison, Wisconsin, USACarbone Cancer Center, University of Wisconsin Madison, Madison, Wisconsin, USADepartment of Biomedical Engineering, University of Wisconsin Madison, Madison, Wisconsin, USADepartment of Plant Pathology, Wisconsin Institute for Discovery, University of Wisconsin-Madison, Madison, Wisconsin, USAABSTRACT Flavobacterium johnsoniae is a ubiquitous soil and rhizosphere bacterium, but despite its abundance, the factors contributing to its success in communities are poorly understood. Using a model microbial community, The Hitchhikers of the Rhizosphere (THOR), we determined the effects of colonization on the fitness of F. johnsoniae in the community. Insertion sequencing, a massively parallel transposon mutant screen, on sterile sand identified 25 genes likely to be important for surface colonization. We constructed in-frame deletions of candidate genes predicted to be involved in cell membrane biogenesis, motility, signal transduction, and transport of amino acids and lipids. All mutants poorly colonized sand, glass, and polystyrene and produced less biofilm than the wild type, indicating the importance of the targeted genes in surface colonization. Eight of the nine colonization-defective mutants were also unable to form motile biofilms or zorbs, thereby suggesting that the affected genes play a role in group movement and linking stationary and motile biofilm formation genetically. Furthermore, we showed that the deletion of colonization genes in F. johnsoniae affected its behavior and survival in THOR on surfaces, suggesting that the same traits are required for success in a multispecies microbial community. Our results provide insight into the mechanisms of surface colonization by F. johnsoniae and form the basis for further understanding its ecology in the rhizosphere.IMPORTANCEMicrobial communities direct key environmental processes through multispecies interactions. Understanding these interactions is vital for manipulating microbiomes to promote health in human, environmental, and agricultural systems. However, microbiome complexity can hinder our understanding of the underlying mechanisms in microbial community interactions. As a first step toward unraveling these interactions, we explored the role of surface colonization in microbial community interactions using The Hitchhikers Of the Rhizosphere (THOR), a genetically tractable model community of three bacterial species, Flavobacterium johnsoniae, Pseudomonas koreensis, and Bacillus cereus. We identified F. johnsoniae genes important for surface colonization in solitary conditions and in the THOR community. Understanding the mechanisms that promote the success of bacteria in microbial communities brings us closer to targeted manipulations to achieve outcomes that benefit agriculture, the environment, and human health.https://journals.asm.org/doi/10.1128/mbio.03428-23Type 9 secretion systemattachmentbiofilmsTnSeqexosortasezorbs |
| spellingShingle | Shruthi Magesh Amanda I. Hurley Julia F. Nepper Marc G. Chevrette Jonathan H. Schrope Chao Li David J. Beebe Jo Handelsman Surface colonization by Flavobacterium johnsoniae promotes its survival in a model microbial community mBio Type 9 secretion system attachment biofilms TnSeq exosortase zorbs |
| title | Surface colonization by Flavobacterium johnsoniae promotes its survival in a model microbial community |
| title_full | Surface colonization by Flavobacterium johnsoniae promotes its survival in a model microbial community |
| title_fullStr | Surface colonization by Flavobacterium johnsoniae promotes its survival in a model microbial community |
| title_full_unstemmed | Surface colonization by Flavobacterium johnsoniae promotes its survival in a model microbial community |
| title_short | Surface colonization by Flavobacterium johnsoniae promotes its survival in a model microbial community |
| title_sort | surface colonization by flavobacterium johnsoniae promotes its survival in a model microbial community |
| topic | Type 9 secretion system attachment biofilms TnSeq exosortase zorbs |
| url | https://journals.asm.org/doi/10.1128/mbio.03428-23 |
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