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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Autores principales:	Joseph E. Spraker, Philipp Wiemann, Joshua A. Baccile, Nandhitha Venkatesh, Julia Schumacher, Frank C. Schroeder, Laura M. Sanchez, Nancy P. Keller
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	Fusarium antimicrobial activity bacterial wilt bikaverin chemical communication microbial interactions Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/20e55a049a074e70b27b084596b968f9
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spelling	oai:doaj.org-article:20e55a049a074e70b27b084596b968f92021-11-15T16:00:25ZConserved Responses in a War of Small Molecules between a Plant-Pathogenic Bacterium and Fungi10.1128/mBio.00820-182150-7511https://doaj.org/article/20e55a049a074e70b27b084596b968f92018-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00820-18https://doaj.org/toc/2150-7511ABSTRACT 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.Joseph E. SprakerPhilipp WiemannJoshua A. BaccileNandhitha VenkateshJulia SchumacherFrank C. SchroederLaura M. SanchezNancy P. KellerAmerican Society for MicrobiologyarticleFusariumantimicrobial activitybacterial wiltbikaverinchemical communicationmicrobial interactionsMicrobiologyQR1-502ENmBio, Vol 9, Iss 3 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	Fusarium antimicrobial activity bacterial wilt bikaverin chemical communication microbial interactions Microbiology QR1-502
spellingShingle	Fusarium antimicrobial activity bacterial wilt bikaverin chemical communication microbial interactions Microbiology QR1-502 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
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.
format	article
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
title	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_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_sort	conserved responses in a war of small molecules between a plant-pathogenic bacterium and fungi
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/20e55a049a074e70b27b084596b968f9
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Conserved Responses in a War of Small Molecules between a Plant-Pathogenic Bacterium and Fungi

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