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Conserved Responses in a War of Small Molecules between a Plant-Pathogenic Bacterium and Fungi

Spraker, Joseph E. and Wiemann, Philipp and Baccile, Joshua A. and Venkatesh, Nandhitha and Schumacher, Julia and Schroeder, Frank C. and Sanchez, Laura M. and Keller, Nancy P. (2018) Conserved Responses in a War of Small Molecules between a Plant-Pathogenic Bacterium and Fungi. mBio, 9 (3). Art. No. e00820-18. ISSN 2150-7511. PMCID PMC5964348. https://resolver.caltech.edu/CaltechAUTHORS:20180613-092436939

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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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1128/mBio.00820-18DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5964348/PubMed CentralArticle
ORCID:
AuthorORCID
Spraker, Joseph E.0000-0002-5429-0328
Wiemann, Philipp0000-0002-7983-2218
Baccile, Joshua A.0000-0003-4334-755X
Schroeder, Frank C.0000-0002-4420-0237
Sanchez, Laura M.0000-0001-9223-7977
Keller, Nancy P.0000-0002-4386-9473
Additional Information:© 2018 Spraker et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license. Received 25 April 2018; Accepted 27 April 2018; Published 22 May 2018. This research was funded by an NSF graduate research fellowship under grant no. DGE-1256259 as well as an NSF postdoctoral research fellowship under award no. 1612169 to J.E.S. Other agencies contributing to this work included NIH CBI training grant T32GM008500 to J.A.B., NIH R01GM112739-01 to N.P.K. and F.C.S., in part USDA Hatch Formula Fund WIS01710 to N.P.K., and K12HD055892 from the National Institute of Child Health and Human Development (NICHD) and the National Institutes of Health Office of Research on Women’s Health (ORWH) and UIC startup funds to L.M.S. We thank Bettina Tudzynski for providing F. fujikuroi IMI58289 and Δbik1 strains, Hans-Ulrich Humpf for providing an authentic bikaverin standard, Antonio Di Pietro for providing F. oxysporum f. sp. lycopersici 4287, and Atul Jain and Terry Moore for assistance with recrystallization of DHB and CHCA.
Funders:
Funding AgencyGrant Number
NSF Graduate Research FellowshipDGE-1256259
NSF1612169
NIH Predoctoral FellowshipT32GM008500
NIHR01GM112739-01
United States Department of Agriculture (USDA)WIS01710
NIHK12HD055892
Subject Keywords:Fusarium; antimicrobial activity; bacterial wilt; bikaverin; chemical communication; microbial interactions; ralsolamycin
Issue or Number:3
PubMed Central ID:PMC5964348
Record Number:CaltechAUTHORS:20180613-092436939
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20180613-092436939
Official Citation:Spraker JE, Wiemann P, Baccile JA, Venkatesh N, Schumacher J, Schroeder FC, Sanchez LM, Keller NP. 2018. Conserved responses in a war of small molecules between a plant-pathogenic bacterium and fungi. mBio 9:e00820-18. https://doi.org/10.1128/mBio.00820-18
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:87052
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:13 Jun 2018 16:43
Last Modified:09 Mar 2020 13:18

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