Genetic Responses and Aflatoxin Inhibition during Co-Culture of Aflatoxigenic and Non-Aflatoxigenic <em>Aspergillus flavus</em>

Aflatoxin is a carcinogenic mycotoxin produced by <i>Aspergillus flavus</i>. Non-aflatoxigenic (Non-tox) <i>A. flavus</i> isolates are deployed in corn fields as biocontrol because they substantially reduce aflatoxin contamination via direct replacement and additionally via d...

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Main Authors: Rebecca R. Sweany, Brian M. Mack, Geromy G. Moore, Matthew K. Gilbert, Jeffrey W. Cary, Matthew D. Lebar, Kanniah Rajasekaran, Kenneth E. Damann
Format: Article
Language:English
Published: MDPI AG 2021-11-01
Series:Toxins
Subjects:
Online Access:https://www.mdpi.com/2072-6651/13/11/794
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author Rebecca R. Sweany
Brian M. Mack
Geromy G. Moore
Matthew K. Gilbert
Jeffrey W. Cary
Matthew D. Lebar
Kanniah Rajasekaran
Kenneth E. Damann
author_facet Rebecca R. Sweany
Brian M. Mack
Geromy G. Moore
Matthew K. Gilbert
Jeffrey W. Cary
Matthew D. Lebar
Kanniah Rajasekaran
Kenneth E. Damann
author_sort Rebecca R. Sweany
collection DOAJ
description Aflatoxin is a carcinogenic mycotoxin produced by <i>Aspergillus flavus</i>. Non-aflatoxigenic (Non-tox) <i>A. flavus</i> isolates are deployed in corn fields as biocontrol because they substantially reduce aflatoxin contamination via direct replacement and additionally via direct contact or touch with toxigenic (Tox) isolates and secretion of inhibitory/degradative chemicals. To understand touch inhibition, HPLC analysis and RNA sequencing examined aflatoxin production and gene expression of Non-tox isolate 17 and Tox isolate 53 mono-cultures and during their interaction in co-culture. Aflatoxin production was reduced by 99.7% in 72 h co-cultures. Fewer than expected unique reads were assigned to Tox 53 during co-culture, indicating its growth and/or gene expression was inhibited in response to Non-tox 17. Predicted secreted proteins and genes involved in oxidation/reduction were enriched in Non-tox 17 and co-cultures compared to Tox 53. Five secondary metabolite (SM) gene clusters and kojic acid synthesis genes were upregulated in Non-tox 17 compared to Tox 53 and a few were further upregulated in co-cultures in response to touch. These results suggest Non-tox strains can inhibit growth and aflatoxin gene cluster expression in Tox strains through touch. Additionally, upregulation of other SM genes and redox genes during the biocontrol interaction demonstrates a potential role of inhibitory SMs and antioxidants as additional biocontrol mechanisms and deserves further exploration to improve biocontrol formulations.
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spelling doaj.art-6bd9f70dbcc845d3886823709ecc1c612023-11-23T01:49:14ZengMDPI AGToxins2072-66512021-11-01131179410.3390/toxins13110794Genetic Responses and Aflatoxin Inhibition during Co-Culture of Aflatoxigenic and Non-Aflatoxigenic <em>Aspergillus flavus</em>Rebecca R. Sweany0Brian M. Mack1Geromy G. Moore2Matthew K. Gilbert3Jeffrey W. Cary4Matthew D. Lebar5Kanniah Rajasekaran6Kenneth E. Damann7Food and Feed Safety Research Unit, Southern Regional Research Center, US Department of Agriculture, New Orleans, LA 70124, USAFood and Feed Safety Research Unit, Southern Regional Research Center, US Department of Agriculture, New Orleans, LA 70124, USAFood and Feed Safety Research Unit, Southern Regional Research Center, US Department of Agriculture, New Orleans, LA 70124, USAFood and Feed Safety Research Unit, Southern Regional Research Center, US Department of Agriculture, New Orleans, LA 70124, USAFood and Feed Safety Research Unit, Southern Regional Research Center, US Department of Agriculture, New Orleans, LA 70124, USAFood and Feed Safety Research Unit, Southern Regional Research Center, US Department of Agriculture, New Orleans, LA 70124, USAFood and Feed Safety Research Unit, Southern Regional Research Center, US Department of Agriculture, New Orleans, LA 70124, USADepartment of Plant Pathology and Crop Physiology, Louisiana State University, Baton Rouge, LA 70808, USAAflatoxin is a carcinogenic mycotoxin produced by <i>Aspergillus flavus</i>. Non-aflatoxigenic (Non-tox) <i>A. flavus</i> isolates are deployed in corn fields as biocontrol because they substantially reduce aflatoxin contamination via direct replacement and additionally via direct contact or touch with toxigenic (Tox) isolates and secretion of inhibitory/degradative chemicals. To understand touch inhibition, HPLC analysis and RNA sequencing examined aflatoxin production and gene expression of Non-tox isolate 17 and Tox isolate 53 mono-cultures and during their interaction in co-culture. Aflatoxin production was reduced by 99.7% in 72 h co-cultures. Fewer than expected unique reads were assigned to Tox 53 during co-culture, indicating its growth and/or gene expression was inhibited in response to Non-tox 17. Predicted secreted proteins and genes involved in oxidation/reduction were enriched in Non-tox 17 and co-cultures compared to Tox 53. Five secondary metabolite (SM) gene clusters and kojic acid synthesis genes were upregulated in Non-tox 17 compared to Tox 53 and a few were further upregulated in co-cultures in response to touch. These results suggest Non-tox strains can inhibit growth and aflatoxin gene cluster expression in Tox strains through touch. Additionally, upregulation of other SM genes and redox genes during the biocontrol interaction demonstrates a potential role of inhibitory SMs and antioxidants as additional biocontrol mechanisms and deserves further exploration to improve biocontrol formulations.https://www.mdpi.com/2072-6651/13/11/794aflatoxinsecondary metabolismfungal interactionsbiocontrolbiocontrol mechanismRNA-seq
spellingShingle Rebecca R. Sweany
Brian M. Mack
Geromy G. Moore
Matthew K. Gilbert
Jeffrey W. Cary
Matthew D. Lebar
Kanniah Rajasekaran
Kenneth E. Damann
Genetic Responses and Aflatoxin Inhibition during Co-Culture of Aflatoxigenic and Non-Aflatoxigenic <em>Aspergillus flavus</em>
Toxins
aflatoxin
secondary metabolism
fungal interactions
biocontrol
biocontrol mechanism
RNA-seq
title Genetic Responses and Aflatoxin Inhibition during Co-Culture of Aflatoxigenic and Non-Aflatoxigenic <em>Aspergillus flavus</em>
title_full Genetic Responses and Aflatoxin Inhibition during Co-Culture of Aflatoxigenic and Non-Aflatoxigenic <em>Aspergillus flavus</em>
title_fullStr Genetic Responses and Aflatoxin Inhibition during Co-Culture of Aflatoxigenic and Non-Aflatoxigenic <em>Aspergillus flavus</em>
title_full_unstemmed Genetic Responses and Aflatoxin Inhibition during Co-Culture of Aflatoxigenic and Non-Aflatoxigenic <em>Aspergillus flavus</em>
title_short Genetic Responses and Aflatoxin Inhibition during Co-Culture of Aflatoxigenic and Non-Aflatoxigenic <em>Aspergillus flavus</em>
title_sort genetic responses and aflatoxin inhibition during co culture of aflatoxigenic and non aflatoxigenic em aspergillus flavus em
topic aflatoxin
secondary metabolism
fungal interactions
biocontrol
biocontrol mechanism
RNA-seq
url https://www.mdpi.com/2072-6651/13/11/794
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