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Indole-3-Acetic Acid Produced by Burkholderia heleia Acts as a Phenylacetic Acid Antagonist to Disrupt Tropolone Biosynthesis in Burkholderia plantarii

Burkholderia heleia PAK1-2 is a potent biocontrol agent isolated from rice rhizosphere, as it prevents bacterial rice seedling blight disease caused by Burkholderia plantarii. Here, we isolated a non-antibacterial metabolite from the culture fluid of B. heleia PAK1-2 that was able to suppress B. pla...

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Autores principales: Wang, Mengcen, Tachibana, Seiji, Murai, Yuta, Li, Li, Lau, Sharon Yu Ling, Cao, Mengchao, Zhu, Guonian, Hashimoto, Makoto, Hashidoko, Yasuyuki
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4776283/
https://www.ncbi.nlm.nih.gov/pubmed/26935539
http://dx.doi.org/10.1038/srep22596
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author Wang, Mengcen
Tachibana, Seiji
Murai, Yuta
Li, Li
Lau, Sharon Yu Ling
Cao, Mengchao
Zhu, Guonian
Hashimoto, Makoto
Hashidoko, Yasuyuki
author_facet Wang, Mengcen
Tachibana, Seiji
Murai, Yuta
Li, Li
Lau, Sharon Yu Ling
Cao, Mengchao
Zhu, Guonian
Hashimoto, Makoto
Hashidoko, Yasuyuki
author_sort Wang, Mengcen
collection PubMed
description Burkholderia heleia PAK1-2 is a potent biocontrol agent isolated from rice rhizosphere, as it prevents bacterial rice seedling blight disease caused by Burkholderia plantarii. Here, we isolated a non-antibacterial metabolite from the culture fluid of B. heleia PAK1-2 that was able to suppress B. plantarii virulence and subsequently identified as indole-3-acetic acid (IAA). IAA suppressed the production of tropolone in B. plantarii in a dose-dependent manner without any antibacterial and quorum quenching activity, suggesting that IAA inhibited steps of tropolone biosynthesis. Consistent with this, supplementing cultures of B. plantarii with either L-[ring-(2)H(5)]phenylalanine or [ring-(2)H(2~5)]phenylacetic acid revealed that phenylacetic acid (PAA), which is the dominant metabolite during the early growth stage, is a direct precursor of tropolone. Exposure of B. plantarii to IAA suppressed production of both PAA and tropolone. These data particularly showed that IAA produced by B. heleia PAK1-2 disrupts tropolone production during bioconversion of PAA to tropolone via the ring-rearrangement on the phenyl group of the precursor to attenuate the virulence of B. plantarii. B. heleia PAK1-2 is thus likely a microbial community coordinating bacterium in rhizosphere ecosystems, which never eliminates phytopathogens but only represses production of phytotoxins or bacteriocidal substances.
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spelling pubmed-47762832016-03-09 Indole-3-Acetic Acid Produced by Burkholderia heleia Acts as a Phenylacetic Acid Antagonist to Disrupt Tropolone Biosynthesis in Burkholderia plantarii Wang, Mengcen Tachibana, Seiji Murai, Yuta Li, Li Lau, Sharon Yu Ling Cao, Mengchao Zhu, Guonian Hashimoto, Makoto Hashidoko, Yasuyuki Sci Rep Article Burkholderia heleia PAK1-2 is a potent biocontrol agent isolated from rice rhizosphere, as it prevents bacterial rice seedling blight disease caused by Burkholderia plantarii. Here, we isolated a non-antibacterial metabolite from the culture fluid of B. heleia PAK1-2 that was able to suppress B. plantarii virulence and subsequently identified as indole-3-acetic acid (IAA). IAA suppressed the production of tropolone in B. plantarii in a dose-dependent manner without any antibacterial and quorum quenching activity, suggesting that IAA inhibited steps of tropolone biosynthesis. Consistent with this, supplementing cultures of B. plantarii with either L-[ring-(2)H(5)]phenylalanine or [ring-(2)H(2~5)]phenylacetic acid revealed that phenylacetic acid (PAA), which is the dominant metabolite during the early growth stage, is a direct precursor of tropolone. Exposure of B. plantarii to IAA suppressed production of both PAA and tropolone. These data particularly showed that IAA produced by B. heleia PAK1-2 disrupts tropolone production during bioconversion of PAA to tropolone via the ring-rearrangement on the phenyl group of the precursor to attenuate the virulence of B. plantarii. B. heleia PAK1-2 is thus likely a microbial community coordinating bacterium in rhizosphere ecosystems, which never eliminates phytopathogens but only represses production of phytotoxins or bacteriocidal substances. Nature Publishing Group 2016-03-03 /pmc/articles/PMC4776283/ /pubmed/26935539 http://dx.doi.org/10.1038/srep22596 Text en Copyright © 2016, Macmillan Publishers Limited http://creativecommons.org/licenses/by/4.0/ This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/
spellingShingle Article
Wang, Mengcen
Tachibana, Seiji
Murai, Yuta
Li, Li
Lau, Sharon Yu Ling
Cao, Mengchao
Zhu, Guonian
Hashimoto, Makoto
Hashidoko, Yasuyuki
Indole-3-Acetic Acid Produced by Burkholderia heleia Acts as a Phenylacetic Acid Antagonist to Disrupt Tropolone Biosynthesis in Burkholderia plantarii
title Indole-3-Acetic Acid Produced by Burkholderia heleia Acts as a Phenylacetic Acid Antagonist to Disrupt Tropolone Biosynthesis in Burkholderia plantarii
title_full Indole-3-Acetic Acid Produced by Burkholderia heleia Acts as a Phenylacetic Acid Antagonist to Disrupt Tropolone Biosynthesis in Burkholderia plantarii
title_fullStr Indole-3-Acetic Acid Produced by Burkholderia heleia Acts as a Phenylacetic Acid Antagonist to Disrupt Tropolone Biosynthesis in Burkholderia plantarii
title_full_unstemmed Indole-3-Acetic Acid Produced by Burkholderia heleia Acts as a Phenylacetic Acid Antagonist to Disrupt Tropolone Biosynthesis in Burkholderia plantarii
title_short Indole-3-Acetic Acid Produced by Burkholderia heleia Acts as a Phenylacetic Acid Antagonist to Disrupt Tropolone Biosynthesis in Burkholderia plantarii
title_sort indole-3-acetic acid produced by burkholderia heleia acts as a phenylacetic acid antagonist to disrupt tropolone biosynthesis in burkholderia plantarii
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4776283/
https://www.ncbi.nlm.nih.gov/pubmed/26935539
http://dx.doi.org/10.1038/srep22596
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