Nigericin and Geldanamycin Are Phytotoxic Specialized Metabolites Produced by the Plant Pathogen Streptomyces sp. 11-1-2

ABSTRACT Streptomyces bacteria are a key source of microbial specialized metabolites with useful applications in medicine and agriculture. In addition, some species are important plant pathogens and cause diseases such as potato scab, which reduces the quality and market value of affected potato cro...

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Published in:Microbiology Spectrum
Main Authors: Gustavo A. Díaz-Cruz, Jingyu Liu, Kapil Tahlan, Dawn R. D. Bignell
Format: Article in Journal/Newspaper
Language:English
Published: American Society for Microbiology 2022
Subjects:
Online Access:https://doi.org/10.1128/spectrum.02314-21
https://doaj.org/article/2e7e4872be3c4817ba393af0ac2251d9
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spelling ftdoajarticles:oai:doaj.org/article:2e7e4872be3c4817ba393af0ac2251d9 2023-05-15T17:22:54+02:00 Nigericin and Geldanamycin Are Phytotoxic Specialized Metabolites Produced by the Plant Pathogen Streptomyces sp. 11-1-2 Gustavo A. Díaz-Cruz Jingyu Liu Kapil Tahlan Dawn R. D. Bignell 2022-04-01T00:00:00Z https://doi.org/10.1128/spectrum.02314-21 https://doaj.org/article/2e7e4872be3c4817ba393af0ac2251d9 EN eng American Society for Microbiology https://journals.asm.org/doi/10.1128/spectrum.02314-21 https://doaj.org/toc/2165-0497 doi:10.1128/spectrum.02314-21 2165-0497 https://doaj.org/article/2e7e4872be3c4817ba393af0ac2251d9 Microbiology Spectrum, Vol 10, Iss 2 (2022) phytotoxins molecular networking biosynthetic gene clusters specialized metabolites Streptomyces plant pathogens Microbiology QR1-502 article 2022 ftdoajarticles https://doi.org/10.1128/spectrum.02314-21 2022-12-31T01:41:46Z ABSTRACT Streptomyces bacteria are a key source of microbial specialized metabolites with useful applications in medicine and agriculture. In addition, some species are important plant pathogens and cause diseases such as potato scab, which reduces the quality and market value of affected potato crops. Most scab-associated Streptomyces spp. produce the phytotoxic metabolite thaxtomin A as the principal pathogenicity factor. However, recent reports have described scab-causing strains that do not produce thaxtomin A, but instead produce other phytotoxins that are thought to contribute to plant host infection and symptom development. Streptomyces sp. 11-1-2 is a highly pathogenic strain that was originally isolated from a scab symptomatic potato tuber in Newfoundland, Canada. The strain secretes one or more phytotoxic compounds of unknown identity, and it is hypothesized that these compounds serve as virulence factors for this organism. We analyzed the genome sequence of Streptomyces sp. 11-1-2 and found biosynthetic gene clusters for producing the known herbicidal compounds nigericin and geldanamycin. Phytotoxic culture extracts were analyzed using liquid chromatography-coupled tandem mass spectrometry and molecular networking, and this confirmed the production of both compounds by Streptomyces sp. 11-1-2 along with other, potentially related metabolites. The biosynthesis of both metabolites was found to be suppressed by the addition of N-acetylglucosamine to the culture medium, and pure nigericin and geldanamycin were able to exhibit phytotoxic effects against both radish seedlings and potato tuber tissue. Furthermore, the coadministration of the two compounds produced greater phytotoxic effects against potato tuber tissue than administration of each compound alone. IMPORTANCE Plant pathogens use a variety of mechanisms, including the production of phytotoxic specialized metabolites, to establish an infection of host tissue. Although thaxtomin A is considered the key phytotoxin involved in the development of ... Article in Journal/Newspaper Newfoundland Directory of Open Access Journals: DOAJ Articles Canada Microbiology Spectrum 10 2
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic phytotoxins
molecular networking
biosynthetic gene clusters
specialized metabolites
Streptomyces
plant pathogens
Microbiology
QR1-502
spellingShingle phytotoxins
molecular networking
biosynthetic gene clusters
specialized metabolites
Streptomyces
plant pathogens
Microbiology
QR1-502
Gustavo A. Díaz-Cruz
Jingyu Liu
Kapil Tahlan
Dawn R. D. Bignell
Nigericin and Geldanamycin Are Phytotoxic Specialized Metabolites Produced by the Plant Pathogen Streptomyces sp. 11-1-2
topic_facet phytotoxins
molecular networking
biosynthetic gene clusters
specialized metabolites
Streptomyces
plant pathogens
Microbiology
QR1-502
description ABSTRACT Streptomyces bacteria are a key source of microbial specialized metabolites with useful applications in medicine and agriculture. In addition, some species are important plant pathogens and cause diseases such as potato scab, which reduces the quality and market value of affected potato crops. Most scab-associated Streptomyces spp. produce the phytotoxic metabolite thaxtomin A as the principal pathogenicity factor. However, recent reports have described scab-causing strains that do not produce thaxtomin A, but instead produce other phytotoxins that are thought to contribute to plant host infection and symptom development. Streptomyces sp. 11-1-2 is a highly pathogenic strain that was originally isolated from a scab symptomatic potato tuber in Newfoundland, Canada. The strain secretes one or more phytotoxic compounds of unknown identity, and it is hypothesized that these compounds serve as virulence factors for this organism. We analyzed the genome sequence of Streptomyces sp. 11-1-2 and found biosynthetic gene clusters for producing the known herbicidal compounds nigericin and geldanamycin. Phytotoxic culture extracts were analyzed using liquid chromatography-coupled tandem mass spectrometry and molecular networking, and this confirmed the production of both compounds by Streptomyces sp. 11-1-2 along with other, potentially related metabolites. The biosynthesis of both metabolites was found to be suppressed by the addition of N-acetylglucosamine to the culture medium, and pure nigericin and geldanamycin were able to exhibit phytotoxic effects against both radish seedlings and potato tuber tissue. Furthermore, the coadministration of the two compounds produced greater phytotoxic effects against potato tuber tissue than administration of each compound alone. IMPORTANCE Plant pathogens use a variety of mechanisms, including the production of phytotoxic specialized metabolites, to establish an infection of host tissue. Although thaxtomin A is considered the key phytotoxin involved in the development of ...
format Article in Journal/Newspaper
author Gustavo A. Díaz-Cruz
Jingyu Liu
Kapil Tahlan
Dawn R. D. Bignell
author_facet Gustavo A. Díaz-Cruz
Jingyu Liu
Kapil Tahlan
Dawn R. D. Bignell
author_sort Gustavo A. Díaz-Cruz
title Nigericin and Geldanamycin Are Phytotoxic Specialized Metabolites Produced by the Plant Pathogen Streptomyces sp. 11-1-2
title_short Nigericin and Geldanamycin Are Phytotoxic Specialized Metabolites Produced by the Plant Pathogen Streptomyces sp. 11-1-2
title_full Nigericin and Geldanamycin Are Phytotoxic Specialized Metabolites Produced by the Plant Pathogen Streptomyces sp. 11-1-2
title_fullStr Nigericin and Geldanamycin Are Phytotoxic Specialized Metabolites Produced by the Plant Pathogen Streptomyces sp. 11-1-2
title_full_unstemmed Nigericin and Geldanamycin Are Phytotoxic Specialized Metabolites Produced by the Plant Pathogen Streptomyces sp. 11-1-2
title_sort nigericin and geldanamycin are phytotoxic specialized metabolites produced by the plant pathogen streptomyces sp. 11-1-2
publisher American Society for Microbiology
publishDate 2022
url https://doi.org/10.1128/spectrum.02314-21
https://doaj.org/article/2e7e4872be3c4817ba393af0ac2251d9
geographic Canada
geographic_facet Canada
genre Newfoundland
genre_facet Newfoundland
op_source Microbiology Spectrum, Vol 10, Iss 2 (2022)
op_relation https://journals.asm.org/doi/10.1128/spectrum.02314-21
https://doaj.org/toc/2165-0497
doi:10.1128/spectrum.02314-21
2165-0497
https://doaj.org/article/2e7e4872be3c4817ba393af0ac2251d9
op_doi https://doi.org/10.1128/spectrum.02314-21
container_title Microbiology Spectrum
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