Aflatoxin-exposure of Vibrio gazogenes as a novel system for the generation of aflatoxin synthesis inhibitors

Aflatoxin is a mycotoxin and a secondary metabolite, and the most potent known liver carcinogen that contaminates several important crops, and represents a significant threat to public health and the economy. Available approaches reported thus far have been insufficient to eliminate this threat, and...

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Main Authors: Phani M Gummadidala, Yung-Pin eChen, Kevin R Beauchesne, Kristin P Miller, Chandrani eMitra, Nora eBanaszek, Michelle eVelez-Martinez, Peter D.R. Moeller, John L Ferry, Alan W. Decho, Anindya eChanda
Format: Article
Language:English
Published: Frontiers Media S.A. 2016-06-01
Series:Frontiers in Microbiology
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fmicb.2016.00814/full
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spelling doaj-1e720385cdc446b395c85cfb2acc9b3b2020-11-24T21:37:20ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2016-06-01710.3389/fmicb.2016.00814193373Aflatoxin-exposure of Vibrio gazogenes as a novel system for the generation of aflatoxin synthesis inhibitorsPhani M Gummadidala0Yung-Pin eChen1Kevin R Beauchesne2Kristin P Miller3Chandrani eMitra4Nora eBanaszek5Michelle eVelez-Martinez6Peter D.R. Moeller7John L Ferry8Alan W. Decho9Anindya eChanda10University of South CarolinaUniversity of South CarolinaNational Ocean ServiceUniversity of South CarolinaUniversity of South CarolinaUniversity of South CarolinaUniversity of South CarolinaNational Ocean ServiceUniversity of South CarolinaUniversity of South CarolinaUniversity of South CarolinaAflatoxin is a mycotoxin and a secondary metabolite, and the most potent known liver carcinogen that contaminates several important crops, and represents a significant threat to public health and the economy. Available approaches reported thus far have been insufficient to eliminate this threat, and therefore provide the rational to explore novel methods for preventing aflatoxin accumulation in the environment. Many terrestrial plants and microbes that share ecological niches and encounter the aflatoxin producers have the ability to synthesize compounds that inhibit aflatoxin synthesis. However, reports of natural aflatoxin inhibitors from marine ecosystem components that do not share ecological niches with the aflatoxin producers are rare. Here we show that a non-pathogenic marine bacterium, Vibrio gazogenes, when exposed to low non-toxic doses of aflatoxin B1, demonstrates a shift in its metabolic output and synthesizes a metabolite fraction that inhibits aflatoxin synthesis without affecting hyphal growth in the model aflatoxin producer, Aspergillus parasiticus. The molecular mass of the predominant metabolite in this fraction was also different from the known prodigiosins, which are the known antifungal secondary metabolites synthesized by this Vibrio. Gene expression analyses using RT-PCR demonstrate that this metabolite fraction inhibits aflatoxin synthesis by down-regulating the expression of early-, middle- and late- growth stage aflatoxin genes, the aflatoxin pathway regulator, aflR and one global regulator of secondary metabolism, LaeA. Our study establishes a novel system for generation of aflatoxin synthesis inhibitors, and emphasizes the potential of the under-explored Vibrio’s silent genome for generating new modulators of fungal secondary metabolism.http://journal.frontiersin.org/Journal/10.3389/fmicb.2016.00814/fullAflatoxinsNatural ProductsAspergillus parasiticusVibrio gazogenesAflatoxin response metabolites (ARMs)
collection DOAJ
language English
format Article
sources DOAJ
author Phani M Gummadidala
Yung-Pin eChen
Kevin R Beauchesne
Kristin P Miller
Chandrani eMitra
Nora eBanaszek
Michelle eVelez-Martinez
Peter D.R. Moeller
John L Ferry
Alan W. Decho
Anindya eChanda
spellingShingle Phani M Gummadidala
Yung-Pin eChen
Kevin R Beauchesne
Kristin P Miller
Chandrani eMitra
Nora eBanaszek
Michelle eVelez-Martinez
Peter D.R. Moeller
John L Ferry
Alan W. Decho
Anindya eChanda
Aflatoxin-exposure of Vibrio gazogenes as a novel system for the generation of aflatoxin synthesis inhibitors
Frontiers in Microbiology
Aflatoxins
Natural Products
Aspergillus parasiticus
Vibrio gazogenes
Aflatoxin response metabolites (ARMs)
author_facet Phani M Gummadidala
Yung-Pin eChen
Kevin R Beauchesne
Kristin P Miller
Chandrani eMitra
Nora eBanaszek
Michelle eVelez-Martinez
Peter D.R. Moeller
John L Ferry
Alan W. Decho
Anindya eChanda
author_sort Phani M Gummadidala
title Aflatoxin-exposure of Vibrio gazogenes as a novel system for the generation of aflatoxin synthesis inhibitors
title_short Aflatoxin-exposure of Vibrio gazogenes as a novel system for the generation of aflatoxin synthesis inhibitors
title_full Aflatoxin-exposure of Vibrio gazogenes as a novel system for the generation of aflatoxin synthesis inhibitors
title_fullStr Aflatoxin-exposure of Vibrio gazogenes as a novel system for the generation of aflatoxin synthesis inhibitors
title_full_unstemmed Aflatoxin-exposure of Vibrio gazogenes as a novel system for the generation of aflatoxin synthesis inhibitors
title_sort aflatoxin-exposure of vibrio gazogenes as a novel system for the generation of aflatoxin synthesis inhibitors
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2016-06-01
description Aflatoxin is a mycotoxin and a secondary metabolite, and the most potent known liver carcinogen that contaminates several important crops, and represents a significant threat to public health and the economy. Available approaches reported thus far have been insufficient to eliminate this threat, and therefore provide the rational to explore novel methods for preventing aflatoxin accumulation in the environment. Many terrestrial plants and microbes that share ecological niches and encounter the aflatoxin producers have the ability to synthesize compounds that inhibit aflatoxin synthesis. However, reports of natural aflatoxin inhibitors from marine ecosystem components that do not share ecological niches with the aflatoxin producers are rare. Here we show that a non-pathogenic marine bacterium, Vibrio gazogenes, when exposed to low non-toxic doses of aflatoxin B1, demonstrates a shift in its metabolic output and synthesizes a metabolite fraction that inhibits aflatoxin synthesis without affecting hyphal growth in the model aflatoxin producer, Aspergillus parasiticus. The molecular mass of the predominant metabolite in this fraction was also different from the known prodigiosins, which are the known antifungal secondary metabolites synthesized by this Vibrio. Gene expression analyses using RT-PCR demonstrate that this metabolite fraction inhibits aflatoxin synthesis by down-regulating the expression of early-, middle- and late- growth stage aflatoxin genes, the aflatoxin pathway regulator, aflR and one global regulator of secondary metabolism, LaeA. Our study establishes a novel system for generation of aflatoxin synthesis inhibitors, and emphasizes the potential of the under-explored Vibrio’s silent genome for generating new modulators of fungal secondary metabolism.
topic Aflatoxins
Natural Products
Aspergillus parasiticus
Vibrio gazogenes
Aflatoxin response metabolites (ARMs)
url http://journal.frontiersin.org/Journal/10.3389/fmicb.2016.00814/full
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