Fitness Cost of Aflatoxin Production in <named-content content-type="genus-species">Aspergillus flavus</named-content> When Competing with Soil Microbes Could Maintain Balancing Selection

ABSTRACT Selective forces that maintain the polymorphism for aflatoxigenic and nonaflatoxigenic individuals of Aspergillus flavus are largely unknown. As soils are widely considered the natural habitat of A. flavus, we hypothesized that aflatoxin production would confer a fitness advantage in the so...

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Autores principales:	Milton T. Drott, Tracy Debenport, Steven A. Higgins, Daniel H. Buckley, Michael G. Milgroom
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	aflatoxin secondary metabolism Aspergillus flavus fitness cost Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/a932a280124a4c23a9a538af2e895015
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spelling	oai:doaj.org-article:a932a280124a4c23a9a538af2e8950152021-11-15T15:55:14ZFitness Cost of Aflatoxin Production in <named-content content-type="genus-species">Aspergillus flavus</named-content> When Competing with Soil Microbes Could Maintain Balancing Selection10.1128/mBio.02782-182150-7511https://doaj.org/article/a932a280124a4c23a9a538af2e8950152019-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02782-18https://doaj.org/toc/2150-7511ABSTRACT Selective forces that maintain the polymorphism for aflatoxigenic and nonaflatoxigenic individuals of Aspergillus flavus are largely unknown. As soils are widely considered the natural habitat of A. flavus, we hypothesized that aflatoxin production would confer a fitness advantage in the soil environment. To test this hypothesis, we used A. flavus DNA quantified by quantitative PCR (qPCR) as a proxy for fitness of aflatoxigenic and nonaflatoxigenic field isolates grown in soil microcosms. Contrary to predictions, aflatoxigenic isolates had significantly lower fitness than did nonaflatoxigenic isolates in natural soils across three temperatures (25, 37, and 42°C). The addition of aflatoxin to soils (500 ng/g) had no effect on the growth of A. flavus. Amplicon sequencing showed that neither the aflatoxin-producing ability of the fungus nor the addition of aflatoxin had a significant effect on the composition of fungal or bacterial communities in soil. We argue that the fitness disadvantage of aflatoxigenic isolates is most likely explained by the metabolic cost of producing aflatoxin. Coupled with a previous report of a selective advantage of aflatoxin production in the presence of some insects, our findings give an ecological explanation for balancing selection resulting in persistent polymorphisms in aflatoxin production. IMPORTANCE Aflatoxin, produced by the fungus Aspergillus flavus, is an extremely potent hepatotoxin that causes acute toxicosis and cancer, and it incurs hundreds of millions of dollars annually in agricultural losses. Despite the importance of this toxin to humans, it has remained unclear what the fungus gains by producing aflatoxin. In fact, not all strains of A. flavus produce aflatoxin. Previous work has shown an advantage to producing aflatoxin in the presence of some insects. Our current work demonstrates the first evidence of a disadvantage to A. flavus in producing aflatoxin when competing with soil microbes. Together, these opposing evolutionary forces could explain the persistence of both aflatoxigenic and nonaflatoxigenic strains through evolutionary time.Milton T. DrottTracy DebenportSteven A. HigginsDaniel H. BuckleyMichael G. MilgroomAmerican Society for Microbiologyarticleaflatoxinsecondary metabolismAspergillus flavusfitness costMicrobiologyQR1-502ENmBio, Vol 10, Iss 1 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	aflatoxin secondary metabolism Aspergillus flavus fitness cost Microbiology QR1-502
spellingShingle	aflatoxin secondary metabolism Aspergillus flavus fitness cost Microbiology QR1-502 Milton T. Drott Tracy Debenport Steven A. Higgins Daniel H. Buckley Michael G. Milgroom Fitness Cost of Aflatoxin Production in <named-content content-type="genus-species">Aspergillus flavus</named-content> When Competing with Soil Microbes Could Maintain Balancing Selection
description	ABSTRACT Selective forces that maintain the polymorphism for aflatoxigenic and nonaflatoxigenic individuals of Aspergillus flavus are largely unknown. As soils are widely considered the natural habitat of A. flavus, we hypothesized that aflatoxin production would confer a fitness advantage in the soil environment. To test this hypothesis, we used A. flavus DNA quantified by quantitative PCR (qPCR) as a proxy for fitness of aflatoxigenic and nonaflatoxigenic field isolates grown in soil microcosms. Contrary to predictions, aflatoxigenic isolates had significantly lower fitness than did nonaflatoxigenic isolates in natural soils across three temperatures (25, 37, and 42°C). The addition of aflatoxin to soils (500 ng/g) had no effect on the growth of A. flavus. Amplicon sequencing showed that neither the aflatoxin-producing ability of the fungus nor the addition of aflatoxin had a significant effect on the composition of fungal or bacterial communities in soil. We argue that the fitness disadvantage of aflatoxigenic isolates is most likely explained by the metabolic cost of producing aflatoxin. Coupled with a previous report of a selective advantage of aflatoxin production in the presence of some insects, our findings give an ecological explanation for balancing selection resulting in persistent polymorphisms in aflatoxin production. IMPORTANCE Aflatoxin, produced by the fungus Aspergillus flavus, is an extremely potent hepatotoxin that causes acute toxicosis and cancer, and it incurs hundreds of millions of dollars annually in agricultural losses. Despite the importance of this toxin to humans, it has remained unclear what the fungus gains by producing aflatoxin. In fact, not all strains of A. flavus produce aflatoxin. Previous work has shown an advantage to producing aflatoxin in the presence of some insects. Our current work demonstrates the first evidence of a disadvantage to A. flavus in producing aflatoxin when competing with soil microbes. Together, these opposing evolutionary forces could explain the persistence of both aflatoxigenic and nonaflatoxigenic strains through evolutionary time.
format	article
author	Milton T. Drott Tracy Debenport Steven A. Higgins Daniel H. Buckley Michael G. Milgroom
author_facet	Milton T. Drott Tracy Debenport Steven A. Higgins Daniel H. Buckley Michael G. Milgroom
author_sort	Milton T. Drott
title	Fitness Cost of Aflatoxin Production in <named-content content-type="genus-species">Aspergillus flavus</named-content> When Competing with Soil Microbes Could Maintain Balancing Selection
title_short	Fitness Cost of Aflatoxin Production in <named-content content-type="genus-species">Aspergillus flavus</named-content> When Competing with Soil Microbes Could Maintain Balancing Selection
title_full	Fitness Cost of Aflatoxin Production in <named-content content-type="genus-species">Aspergillus flavus</named-content> When Competing with Soil Microbes Could Maintain Balancing Selection
title_fullStr	Fitness Cost of Aflatoxin Production in <named-content content-type="genus-species">Aspergillus flavus</named-content> When Competing with Soil Microbes Could Maintain Balancing Selection
title_full_unstemmed	Fitness Cost of Aflatoxin Production in <named-content content-type="genus-species">Aspergillus flavus</named-content> When Competing with Soil Microbes Could Maintain Balancing Selection
title_sort	fitness cost of aflatoxin production in <named-content content-type="genus-species">aspergillus flavus</named-content> when competing with soil microbes could maintain balancing selection
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/a932a280124a4c23a9a538af2e895015
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Fitness Cost of Aflatoxin Production in <named-content content-type="genus-species">Aspergillus flavus</named-content> When Competing with Soil Microbes Could Maintain Balancing Selection

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