An environmental isolate of Pseudomonas, 20EI1, reduces Aspergillus flavus growth in an iron-dependent manner and alters secondary metabolism

IntroductionAspergillus flavus is an opportunistic pathogenic fungus that infects oilseed crops worldwide. When colonizing plants, it produces mycotoxins, including carcinogenic compounds such as aflatoxins. Mycotoxin contamination results in an important economic and health impact. The design of ne...

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Main Authors: Elizabeth M. Wyman, W. Scott Grayburn, Matthew K. Gilbert, Matthew D. Lebar, Jessica M. Lohmar, Jeffrey W. Cary, Thomas J. C. Sauters, Antonis Rokas, Ana M. Calvo
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-01-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2024.1514950/full
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author Elizabeth M. Wyman
W. Scott Grayburn
Matthew K. Gilbert
Matthew D. Lebar
Jessica M. Lohmar
Jeffrey W. Cary
Thomas J. C. Sauters
Antonis Rokas
Ana M. Calvo
author_facet Elizabeth M. Wyman
W. Scott Grayburn
Matthew K. Gilbert
Matthew D. Lebar
Jessica M. Lohmar
Jeffrey W. Cary
Thomas J. C. Sauters
Antonis Rokas
Ana M. Calvo
author_sort Elizabeth M. Wyman
collection DOAJ
description IntroductionAspergillus flavus is an opportunistic pathogenic fungus that infects oilseed crops worldwide. When colonizing plants, it produces mycotoxins, including carcinogenic compounds such as aflatoxins. Mycotoxin contamination results in an important economic and health impact. The design of new strategies to control A. flavus colonization and mycotoxin contamination is paramount.MethodsThe biocontrol potential of a promising new isolate of Pseudomonas spp., 20EI1 against A. flavus was assessed using bioassays and microscopy. To further elucidate the nature of this bacterial-fungal interaction, we also performed chemical and transcriptomics analyses.ResultsIn the present study, Pseudomonas spp., 20EI1 was able to reduce the growth of A. flavus. Furthermore, we determined that this growth inhibition is iron-dependent. In addition, Pseudomonas 20EI1 reduced or blocked the production of aflatoxin, as well as cyclopiazonic acid and kojic acid. Expression of iron-related genes was altered in the presence of the bacteria and genes involved in the production of aflatoxin were down-regulated. Iron supplementation partially reestablished their expression. Expression of other secondary metabolite (SM) genes was also reduced by the bacteria, including genes of clusters involved in cyclopiazonic acid, kojic acid and imizoquin biosynthesis, while genes of the cluster corresponding to aspergillicin, a siderophore, were upregulated. Interestingly, the global SM regulatory gene mtfA was significantly upregulated by 20EI1, which could have contributed to the observed alterations in SM.DiscussionOur results suggest that Pseudomonas 20EI1 is a promising biocontrol against A. flavus, and provide further insight into this iron-dependent bacterial-fungal interaction affecting the expression of numerous genes, among them those involved in SM.
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spelling doaj-art-2e72049083e741c282d305539956590b2025-01-20T07:20:14ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-01-011510.3389/fmicb.2024.15149501514950An environmental isolate of Pseudomonas, 20EI1, reduces Aspergillus flavus growth in an iron-dependent manner and alters secondary metabolismElizabeth M. Wyman0W. Scott Grayburn1Matthew K. Gilbert2Matthew D. Lebar3Jessica M. Lohmar4Jeffrey W. Cary5Thomas J. C. Sauters6Antonis Rokas7Ana M. Calvo8Department of Biological Sciences, Northern Illinois University, DeKalb, IL, United StatesDepartment of Biological Sciences, Northern Illinois University, DeKalb, IL, United StatesFood and Feed Safety Research Unit, USDA/ARS, Southern Regional Research Center, New Orleans, LA, United StatesFood and Feed Safety Research Unit, USDA/ARS, Southern Regional Research Center, New Orleans, LA, United StatesFood and Feed Safety Research Unit, USDA/ARS, Southern Regional Research Center, New Orleans, LA, United StatesFood and Feed Safety Research Unit, USDA/ARS, Southern Regional Research Center, New Orleans, LA, United StatesDepartment of Biological Sciences and Evolutionary Studies Initiative, Vanderbilt University, Nashville, TN, United StatesDepartment of Biological Sciences and Evolutionary Studies Initiative, Vanderbilt University, Nashville, TN, United StatesDepartment of Biological Sciences, Northern Illinois University, DeKalb, IL, United StatesIntroductionAspergillus flavus is an opportunistic pathogenic fungus that infects oilseed crops worldwide. When colonizing plants, it produces mycotoxins, including carcinogenic compounds such as aflatoxins. Mycotoxin contamination results in an important economic and health impact. The design of new strategies to control A. flavus colonization and mycotoxin contamination is paramount.MethodsThe biocontrol potential of a promising new isolate of Pseudomonas spp., 20EI1 against A. flavus was assessed using bioassays and microscopy. To further elucidate the nature of this bacterial-fungal interaction, we also performed chemical and transcriptomics analyses.ResultsIn the present study, Pseudomonas spp., 20EI1 was able to reduce the growth of A. flavus. Furthermore, we determined that this growth inhibition is iron-dependent. In addition, Pseudomonas 20EI1 reduced or blocked the production of aflatoxin, as well as cyclopiazonic acid and kojic acid. Expression of iron-related genes was altered in the presence of the bacteria and genes involved in the production of aflatoxin were down-regulated. Iron supplementation partially reestablished their expression. Expression of other secondary metabolite (SM) genes was also reduced by the bacteria, including genes of clusters involved in cyclopiazonic acid, kojic acid and imizoquin biosynthesis, while genes of the cluster corresponding to aspergillicin, a siderophore, were upregulated. Interestingly, the global SM regulatory gene mtfA was significantly upregulated by 20EI1, which could have contributed to the observed alterations in SM.DiscussionOur results suggest that Pseudomonas 20EI1 is a promising biocontrol against A. flavus, and provide further insight into this iron-dependent bacterial-fungal interaction affecting the expression of numerous genes, among them those involved in SM.https://www.frontiersin.org/articles/10.3389/fmicb.2024.1514950/fullAspergillus flavusPseudomonasbiocontroltranscriptomesecondary metabolismaflatoxin
spellingShingle Elizabeth M. Wyman
W. Scott Grayburn
Matthew K. Gilbert
Matthew D. Lebar
Jessica M. Lohmar
Jeffrey W. Cary
Thomas J. C. Sauters
Antonis Rokas
Ana M. Calvo
An environmental isolate of Pseudomonas, 20EI1, reduces Aspergillus flavus growth in an iron-dependent manner and alters secondary metabolism
Frontiers in Microbiology
Aspergillus flavus
Pseudomonas
biocontrol
transcriptome
secondary metabolism
aflatoxin
title An environmental isolate of Pseudomonas, 20EI1, reduces Aspergillus flavus growth in an iron-dependent manner and alters secondary metabolism
title_full An environmental isolate of Pseudomonas, 20EI1, reduces Aspergillus flavus growth in an iron-dependent manner and alters secondary metabolism
title_fullStr An environmental isolate of Pseudomonas, 20EI1, reduces Aspergillus flavus growth in an iron-dependent manner and alters secondary metabolism
title_full_unstemmed An environmental isolate of Pseudomonas, 20EI1, reduces Aspergillus flavus growth in an iron-dependent manner and alters secondary metabolism
title_short An environmental isolate of Pseudomonas, 20EI1, reduces Aspergillus flavus growth in an iron-dependent manner and alters secondary metabolism
title_sort environmental isolate of pseudomonas 20ei1 reduces aspergillus flavus growth in an iron dependent manner and alters secondary metabolism
topic Aspergillus flavus
Pseudomonas
biocontrol
transcriptome
secondary metabolism
aflatoxin
url https://www.frontiersin.org/articles/10.3389/fmicb.2024.1514950/full
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