Conserved Responses in a War of Small Molecules between a Plant-Pathogenic Bacterium and Fungi
ABSTRACT Small-molecule signaling is one major mode of communication within the polymicrobial consortium of soil and rhizosphere. While microbial secondary metabolite (SM) production and responses of individual species have been studied extensively, little is known about potentially conserved roles...
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2018-07-01
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| Series: | mBio |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.00820-18 |
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| author | Joseph E. Spraker Philipp Wiemann Joshua A. Baccile Nandhitha Venkatesh Julia Schumacher Frank C. Schroeder Laura M. Sanchez Nancy P. Keller |
| author_facet | Joseph E. Spraker Philipp Wiemann Joshua A. Baccile Nandhitha Venkatesh Julia Schumacher Frank C. Schroeder Laura M. Sanchez Nancy P. Keller |
| author_sort | Joseph E. Spraker |
| collection | DOAJ |
| description | ABSTRACT Small-molecule signaling is one major mode of communication within the polymicrobial consortium of soil and rhizosphere. While microbial secondary metabolite (SM) production and responses of individual species have been studied extensively, little is known about potentially conserved roles of SM signals in multilayered symbiotic or antagonistic relationships. Here, we characterize the SM-mediated interaction between the plant-pathogenic bacterium Ralstonia solanacearum and the two plant-pathogenic fungi Fusarium fujikuroi and Botrytis cinerea. We show that cellular differentiation and SM biosynthesis in F. fujikuroi are induced by the bacterially produced lipopeptide ralsolamycin (synonym ralstonin A). In particular, fungal bikaverin production is induced and preferentially accumulates in fungal survival spores (chlamydospores) only when exposed to supernatants of ralsolamycin-producing strains of R. solanacearum. Although inactivation of bikaverin biosynthesis moderately increases chlamydospore invasion by R. solanacearum, we show that other metabolites such as beauvericin are also induced by ralsolamycin and contribute to suppression of R. solanacearum growth in vitro. Based on our findings that bikaverin antagonizes R. solanacearum and that ralsolamycin induces bikaverin biosynthesis in F. fujikuroi, we asked whether other bikaverin-producing fungi show similar responses to ralsolamycin. Examining a strain of B. cinerea that horizontally acquired the bikaverin gene cluster from Fusarium, we found that ralsolamycin induced bikaverin biosynthesis in this fungus. Our results suggest that conservation of microbial SM responses across distantly related fungi may arise from horizontal transfer of protective gene clusters that are activated by conserved regulatory cues, e.g., a bacterial lipopeptide, providing consistent fitness advantages in dynamic polymicrobial networks. IMPORTANCE Bacteria and fungi are ubiquitous neighbors in many environments, including the rhizosphere. Many of these organisms are notorious as economically devastating plant pathogens, but little is known about how they communicate chemically with each other. Here, we uncover a conserved antagonistic communication between the widespread bacterial wilt pathogen Ralstonia solanacearum and plant-pathogenic fungi from disparate genera, Fusarium and Botrytis. Exposure of Fusarium fujikuroi to the bacterial lipopeptide ralsolamycin resulted in production of the antibacterial metabolite bikaverin specifically in fungal tissues invaded by Ralstonia. Remarkably, ralsolamycin induction of bikaverin was conserved in a Botrytis cinerea isolate carrying a horizontally transferred bikaverin gene cluster. These results indicate that horizontally transferred gene clusters may carry regulatory prompts that contribute to conserved fitness functions in polymicrobial environments. |
| first_indexed | 2024-12-19T05:02:33Z |
| format | Article |
| id | doaj.art-20e55a049a074e70b27b084596b968f9 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-19T05:02:33Z |
| publishDate | 2018-07-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-20e55a049a074e70b27b084596b968f92022-12-21T20:35:02ZengAmerican Society for MicrobiologymBio2150-75112018-07-019310.1128/mBio.00820-18Conserved Responses in a War of Small Molecules between a Plant-Pathogenic Bacterium and FungiJoseph E. Spraker0Philipp Wiemann1Joshua A. Baccile2Nandhitha Venkatesh3Julia Schumacher4Frank C. Schroeder5Laura M. Sanchez6Nancy P. Keller7Department of Plant Pathology, University of Wisconsin—Madison, Madison, Wisconsin, USADepartment of Medical Microbiology and Immunology, University of Wisconsin—Madison, Madison, Wisconsin, USABoyce Thompson Institute and Department of Chemistry and Chemical Biology, Cornell University, Ithaca, New York, USADepartment of Plant Pathology, University of Wisconsin—Madison, Madison, Wisconsin, USAInstitute for Biology and Biotechnology of Plants, Westfälische Wilhelms-Universität Münster, Münster, GermanyDepartment of Medicinal Chemistry and Pharmacognosy, College of Pharmacy, University of Illinois at Chicago, Chicago, Illinois, USADepartment of Bacteriology, University of Wisconsin—Madison, Madison, Wisconsin, USADepartment of Medical Microbiology and Immunology, University of Wisconsin—Madison, Madison, Wisconsin, USAABSTRACT Small-molecule signaling is one major mode of communication within the polymicrobial consortium of soil and rhizosphere. While microbial secondary metabolite (SM) production and responses of individual species have been studied extensively, little is known about potentially conserved roles of SM signals in multilayered symbiotic or antagonistic relationships. Here, we characterize the SM-mediated interaction between the plant-pathogenic bacterium Ralstonia solanacearum and the two plant-pathogenic fungi Fusarium fujikuroi and Botrytis cinerea. We show that cellular differentiation and SM biosynthesis in F. fujikuroi are induced by the bacterially produced lipopeptide ralsolamycin (synonym ralstonin A). In particular, fungal bikaverin production is induced and preferentially accumulates in fungal survival spores (chlamydospores) only when exposed to supernatants of ralsolamycin-producing strains of R. solanacearum. Although inactivation of bikaverin biosynthesis moderately increases chlamydospore invasion by R. solanacearum, we show that other metabolites such as beauvericin are also induced by ralsolamycin and contribute to suppression of R. solanacearum growth in vitro. Based on our findings that bikaverin antagonizes R. solanacearum and that ralsolamycin induces bikaverin biosynthesis in F. fujikuroi, we asked whether other bikaverin-producing fungi show similar responses to ralsolamycin. Examining a strain of B. cinerea that horizontally acquired the bikaverin gene cluster from Fusarium, we found that ralsolamycin induced bikaverin biosynthesis in this fungus. Our results suggest that conservation of microbial SM responses across distantly related fungi may arise from horizontal transfer of protective gene clusters that are activated by conserved regulatory cues, e.g., a bacterial lipopeptide, providing consistent fitness advantages in dynamic polymicrobial networks. IMPORTANCE Bacteria and fungi are ubiquitous neighbors in many environments, including the rhizosphere. Many of these organisms are notorious as economically devastating plant pathogens, but little is known about how they communicate chemically with each other. Here, we uncover a conserved antagonistic communication between the widespread bacterial wilt pathogen Ralstonia solanacearum and plant-pathogenic fungi from disparate genera, Fusarium and Botrytis. Exposure of Fusarium fujikuroi to the bacterial lipopeptide ralsolamycin resulted in production of the antibacterial metabolite bikaverin specifically in fungal tissues invaded by Ralstonia. Remarkably, ralsolamycin induction of bikaverin was conserved in a Botrytis cinerea isolate carrying a horizontally transferred bikaverin gene cluster. These results indicate that horizontally transferred gene clusters may carry regulatory prompts that contribute to conserved fitness functions in polymicrobial environments.https://journals.asm.org/doi/10.1128/mBio.00820-18Fusariumantimicrobial activitybacterial wiltbikaverinchemical communicationmicrobial interactions |
| spellingShingle | Joseph E. Spraker Philipp Wiemann Joshua A. Baccile Nandhitha Venkatesh Julia Schumacher Frank C. Schroeder Laura M. Sanchez Nancy P. Keller Conserved Responses in a War of Small Molecules between a Plant-Pathogenic Bacterium and Fungi mBio Fusarium antimicrobial activity bacterial wilt bikaverin chemical communication microbial interactions |
| title | Conserved Responses in a War of Small Molecules between a Plant-Pathogenic Bacterium and Fungi |
| title_full | Conserved Responses in a War of Small Molecules between a Plant-Pathogenic Bacterium and Fungi |
| title_fullStr | Conserved Responses in a War of Small Molecules between a Plant-Pathogenic Bacterium and Fungi |
| title_full_unstemmed | Conserved Responses in a War of Small Molecules between a Plant-Pathogenic Bacterium and Fungi |
| title_short | Conserved Responses in a War of Small Molecules between a Plant-Pathogenic Bacterium and Fungi |
| title_sort | conserved responses in a war of small molecules between a plant pathogenic bacterium and fungi |
| topic | Fusarium antimicrobial activity bacterial wilt bikaverin chemical communication microbial interactions |
| url | https://journals.asm.org/doi/10.1128/mBio.00820-18 |
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