An Integrative Approach for the Characterization of Plant-Pathogenic Streptomyces spp. Strains Based on Metabolomic, Bioactivity, and Phylogenetic Analysis

Actinomycetes are generally recognized as a diverse group of gram-positive, mycelium-forming, soil bacteria that play an important role in mineralization processes and plant health, being Streptomyces the most well-known genus from this group. Although plant pathogenicity is a rare attribute in this...

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Main Authors: Valentina Croce, Andrés López-Radcenco, María Inés Lapaz, María Julia Pianzzola, Guillermo Moyna, María Inés Siri
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-03-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2021.643792/full
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spelling doaj-b28d957726bd4c1faa728895341a63692021-03-22T04:54:57ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-03-011210.3389/fmicb.2021.643792643792An Integrative Approach for the Characterization of Plant-Pathogenic Streptomyces spp. Strains Based on Metabolomic, Bioactivity, and Phylogenetic AnalysisValentina Croce0Valentina Croce1Andrés López-Radcenco2Andrés López-Radcenco3María Inés Lapaz4María Julia Pianzzola5Guillermo Moyna6María Inés Siri7Laboratorio de Microbiología Molecular, Departamento de Biociencias, Facultad de Química, Universidad de la República, Montevideo, UruguayPrograma de Posgrado de la Facultad de Química, Facultad de Química, Universidad de la República, Montevideo, UruguayPrograma de Posgrado de la Facultad de Química, Facultad de Química, Universidad de la República, Montevideo, UruguayLaboratorio de Fisicoquímica Orgánica, Departamento de Química del Litoral, CENUR Litoral Norte, Universidad de la República, Paysandú, UruguayLaboratorio de Microbiología Molecular, Departamento de Biociencias, Facultad de Química, Universidad de la República, Montevideo, UruguayLaboratorio de Microbiología Molecular, Departamento de Biociencias, Facultad de Química, Universidad de la República, Montevideo, UruguayLaboratorio de Fisicoquímica Orgánica, Departamento de Química del Litoral, CENUR Litoral Norte, Universidad de la República, Paysandú, UruguayLaboratorio de Microbiología Molecular, Departamento de Biociencias, Facultad de Química, Universidad de la República, Montevideo, UruguayActinomycetes are generally recognized as a diverse group of gram-positive, mycelium-forming, soil bacteria that play an important role in mineralization processes and plant health, being Streptomyces the most well-known genus from this group. Although plant pathogenicity is a rare attribute in this genus, some species have significant impact worldwide due to their ability to cause important crop diseases such as potato common scab (CS). In this work, an integrative approach was applied to investigate the pathogenic potential of Streptomyces spp. isolates obtained from a local collection of actinomycetes isolated from potato fields. Secretion of phytotoxic compounds was verified in most pathogenic strains from our collection (27 out of 29), and we followed metabolomic analysis to investigate those phytotoxins. We first evaluated the production of the known phytotoxins thaxtomin A (TXT) and desmethylmensacarcin (DMSN) in phytotoxic Streptomyces spp. by HPLC analysis, resulting in 17 TXT and 6 DMSN producers. In addition, NMR-based metabolomic models were able to classify strains according to their phytotoxicity, and metabolomic data was also used to infer chemotaxonomy within pathogenic species. A correlation between phylogeny and the production of distinct phytotoxins was found, supporting the idea that there are “species specific” metabolites produced by this genus. The recently discovered polyketide DMSN was associated unequivocally with S. niveiscabiei strains and was not produced by other species in the growth conditions employed. Two S. niveiscabiei and two S. puniciscabiei phytotoxic strains that did not produce TXT nor DMSN suggest the production of other kind of metabolites involved in phytotoxicity, and allowed the prioritization of these strains for further chemical studies. Indeed, we found two S. niveiscabiei strains whose supernatants were not phytotoxic in the radish assay, suggesting other pathogenic mechanisms involved. We believe our work will be useful to help understand relations between metabolites and phylogenetic clades within actinomycetes.https://www.frontiersin.org/articles/10.3389/fmicb.2021.643792/full1H NMRmetabolomicsphylogeneticsphytotoxinsStreptomyces
collection DOAJ
language English
format Article
sources DOAJ
author Valentina Croce
Valentina Croce
Andrés López-Radcenco
Andrés López-Radcenco
María Inés Lapaz
María Julia Pianzzola
Guillermo Moyna
María Inés Siri
spellingShingle Valentina Croce
Valentina Croce
Andrés López-Radcenco
Andrés López-Radcenco
María Inés Lapaz
María Julia Pianzzola
Guillermo Moyna
María Inés Siri
An Integrative Approach for the Characterization of Plant-Pathogenic Streptomyces spp. Strains Based on Metabolomic, Bioactivity, and Phylogenetic Analysis
Frontiers in Microbiology
1H NMR
metabolomics
phylogenetics
phytotoxins
Streptomyces
author_facet Valentina Croce
Valentina Croce
Andrés López-Radcenco
Andrés López-Radcenco
María Inés Lapaz
María Julia Pianzzola
Guillermo Moyna
María Inés Siri
author_sort Valentina Croce
title An Integrative Approach for the Characterization of Plant-Pathogenic Streptomyces spp. Strains Based on Metabolomic, Bioactivity, and Phylogenetic Analysis
title_short An Integrative Approach for the Characterization of Plant-Pathogenic Streptomyces spp. Strains Based on Metabolomic, Bioactivity, and Phylogenetic Analysis
title_full An Integrative Approach for the Characterization of Plant-Pathogenic Streptomyces spp. Strains Based on Metabolomic, Bioactivity, and Phylogenetic Analysis
title_fullStr An Integrative Approach for the Characterization of Plant-Pathogenic Streptomyces spp. Strains Based on Metabolomic, Bioactivity, and Phylogenetic Analysis
title_full_unstemmed An Integrative Approach for the Characterization of Plant-Pathogenic Streptomyces spp. Strains Based on Metabolomic, Bioactivity, and Phylogenetic Analysis
title_sort integrative approach for the characterization of plant-pathogenic streptomyces spp. strains based on metabolomic, bioactivity, and phylogenetic analysis
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2021-03-01
description Actinomycetes are generally recognized as a diverse group of gram-positive, mycelium-forming, soil bacteria that play an important role in mineralization processes and plant health, being Streptomyces the most well-known genus from this group. Although plant pathogenicity is a rare attribute in this genus, some species have significant impact worldwide due to their ability to cause important crop diseases such as potato common scab (CS). In this work, an integrative approach was applied to investigate the pathogenic potential of Streptomyces spp. isolates obtained from a local collection of actinomycetes isolated from potato fields. Secretion of phytotoxic compounds was verified in most pathogenic strains from our collection (27 out of 29), and we followed metabolomic analysis to investigate those phytotoxins. We first evaluated the production of the known phytotoxins thaxtomin A (TXT) and desmethylmensacarcin (DMSN) in phytotoxic Streptomyces spp. by HPLC analysis, resulting in 17 TXT and 6 DMSN producers. In addition, NMR-based metabolomic models were able to classify strains according to their phytotoxicity, and metabolomic data was also used to infer chemotaxonomy within pathogenic species. A correlation between phylogeny and the production of distinct phytotoxins was found, supporting the idea that there are “species specific” metabolites produced by this genus. The recently discovered polyketide DMSN was associated unequivocally with S. niveiscabiei strains and was not produced by other species in the growth conditions employed. Two S. niveiscabiei and two S. puniciscabiei phytotoxic strains that did not produce TXT nor DMSN suggest the production of other kind of metabolites involved in phytotoxicity, and allowed the prioritization of these strains for further chemical studies. Indeed, we found two S. niveiscabiei strains whose supernatants were not phytotoxic in the radish assay, suggesting other pathogenic mechanisms involved. We believe our work will be useful to help understand relations between metabolites and phylogenetic clades within actinomycetes.
topic 1H NMR
metabolomics
phylogenetics
phytotoxins
Streptomyces
url https://www.frontiersin.org/articles/10.3389/fmicb.2021.643792/full
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