The Frequency of Sex: Population Genomics Reveals Differences in Recombination and Population Structure of the Aflatoxin-Producing Fungus <named-content content-type="genus-species">Aspergillus flavus</named-content>

ABSTRACT The apparent rarity of sex in many fungal species has raised questions about how much sex is needed to purge deleterious mutations and how differences in frequency of sex impact fungal evolution. We sought to determine how differences in the extent of recombination between populations of As...

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Autores principales:	Milton T. Drott, Tatum R. Satterlee, Jeffrey M. Skerker, Brandon T. Pfannenstiel, N. Louise Glass, Nancy P. Keller, Michael G. Milgroom
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	Aspergillus flavus sex recombination aflatoxin population structure population genomics Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/26acb7eb45784064ab1448a0a5588ae2
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spelling	oai:doaj.org-article:26acb7eb45784064ab1448a0a5588ae22021-11-15T15:56:43ZThe Frequency of Sex: Population Genomics Reveals Differences in Recombination and Population Structure of the Aflatoxin-Producing Fungus <named-content content-type="genus-species">Aspergillus flavus</named-content>10.1128/mBio.00963-202150-7511https://doaj.org/article/26acb7eb45784064ab1448a0a5588ae22020-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00963-20https://doaj.org/toc/2150-7511ABSTRACT The apparent rarity of sex in many fungal species has raised questions about how much sex is needed to purge deleterious mutations and how differences in frequency of sex impact fungal evolution. We sought to determine how differences in the extent of recombination between populations of Aspergillus flavus impact the evolution of genes associated with the synthesis of aflatoxin, a notoriously potent carcinogen. We sequenced the genomes of, and quantified aflatoxin production in, 94 isolates of A. flavus sampled from seven states in eastern and central latitudinal transects of the United States. The overall population is subdivided into three genetically differentiated populations (A, B, and C) that differ greatly in their extent of recombination, diversity, and aflatoxin-producing ability. Estimates of the number of recombination events and linkage disequilibrium decay suggest relatively frequent sex only in population A. Population B is sympatric with population A but produces significantly less aflatoxin and is the only population where the inability of nonaflatoxigenic isolates to produce aflatoxin was explained by multiple gene deletions. Population expansion evident in population B suggests a recent introduction or range expansion. Population C is largely nonaflatoxigenic and restricted mainly to northern sampling locations through restricted migration and/or selection. Despite differences in the number and type of mutations in the aflatoxin gene cluster, codon optimization and site frequency differences in synonymous and nonsynonymous mutations suggest that low levels of recombination in some A. flavus populations are sufficient to purge deleterious mutations. IMPORTANCE Differences in the relative frequencies of sexual and asexual reproduction have profound implications for the accumulation of deleterious mutations (Muller’s ratchet), but little is known about how these differences impact the evolution of ecologically important phenotypes. Aspergillus flavus is the main producer of aflatoxin, a notoriously potent carcinogen that often contaminates food. We investigated if differences in the levels of production of aflatoxin by A. flavus could be explained by the accumulation of deleterious mutations due to a lack of recombination. Despite differences in the extent of recombination, variation in aflatoxin production is better explained by the demography and history of specific populations and may suggest important differences in the ecological roles of aflatoxin among populations. Furthermore, the association of aflatoxin production and populations provides a means of predicting the risk of aflatoxin contamination by determining the frequencies of isolates from low- and high-production populations.Milton T. DrottTatum R. SatterleeJeffrey M. SkerkerBrandon T. PfannenstielN. Louise GlassNancy P. KellerMichael G. MilgroomAmerican Society for MicrobiologyarticleAspergillus flavussexrecombinationaflatoxinpopulation structurepopulation genomicsMicrobiologyQR1-502ENmBio, Vol 11, Iss 4 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	Aspergillus flavus sex recombination aflatoxin population structure population genomics Microbiology QR1-502
spellingShingle	Aspergillus flavus sex recombination aflatoxin population structure population genomics Microbiology QR1-502 Milton T. Drott Tatum R. Satterlee Jeffrey M. Skerker Brandon T. Pfannenstiel N. Louise Glass Nancy P. Keller Michael G. Milgroom The Frequency of Sex: Population Genomics Reveals Differences in Recombination and Population Structure of the Aflatoxin-Producing Fungus <named-content content-type="genus-species">Aspergillus flavus</named-content>
description	ABSTRACT The apparent rarity of sex in many fungal species has raised questions about how much sex is needed to purge deleterious mutations and how differences in frequency of sex impact fungal evolution. We sought to determine how differences in the extent of recombination between populations of Aspergillus flavus impact the evolution of genes associated with the synthesis of aflatoxin, a notoriously potent carcinogen. We sequenced the genomes of, and quantified aflatoxin production in, 94 isolates of A. flavus sampled from seven states in eastern and central latitudinal transects of the United States. The overall population is subdivided into three genetically differentiated populations (A, B, and C) that differ greatly in their extent of recombination, diversity, and aflatoxin-producing ability. Estimates of the number of recombination events and linkage disequilibrium decay suggest relatively frequent sex only in population A. Population B is sympatric with population A but produces significantly less aflatoxin and is the only population where the inability of nonaflatoxigenic isolates to produce aflatoxin was explained by multiple gene deletions. Population expansion evident in population B suggests a recent introduction or range expansion. Population C is largely nonaflatoxigenic and restricted mainly to northern sampling locations through restricted migration and/or selection. Despite differences in the number and type of mutations in the aflatoxin gene cluster, codon optimization and site frequency differences in synonymous and nonsynonymous mutations suggest that low levels of recombination in some A. flavus populations are sufficient to purge deleterious mutations. IMPORTANCE Differences in the relative frequencies of sexual and asexual reproduction have profound implications for the accumulation of deleterious mutations (Muller’s ratchet), but little is known about how these differences impact the evolution of ecologically important phenotypes. Aspergillus flavus is the main producer of aflatoxin, a notoriously potent carcinogen that often contaminates food. We investigated if differences in the levels of production of aflatoxin by A. flavus could be explained by the accumulation of deleterious mutations due to a lack of recombination. Despite differences in the extent of recombination, variation in aflatoxin production is better explained by the demography and history of specific populations and may suggest important differences in the ecological roles of aflatoxin among populations. Furthermore, the association of aflatoxin production and populations provides a means of predicting the risk of aflatoxin contamination by determining the frequencies of isolates from low- and high-production populations.
format	article
author	Milton T. Drott Tatum R. Satterlee Jeffrey M. Skerker Brandon T. Pfannenstiel N. Louise Glass Nancy P. Keller Michael G. Milgroom
author_facet	Milton T. Drott Tatum R. Satterlee Jeffrey M. Skerker Brandon T. Pfannenstiel N. Louise Glass Nancy P. Keller Michael G. Milgroom
author_sort	Milton T. Drott
title	The Frequency of Sex: Population Genomics Reveals Differences in Recombination and Population Structure of the Aflatoxin-Producing Fungus <named-content content-type="genus-species">Aspergillus flavus</named-content>
title_short	The Frequency of Sex: Population Genomics Reveals Differences in Recombination and Population Structure of the Aflatoxin-Producing Fungus <named-content content-type="genus-species">Aspergillus flavus</named-content>
title_full	The Frequency of Sex: Population Genomics Reveals Differences in Recombination and Population Structure of the Aflatoxin-Producing Fungus <named-content content-type="genus-species">Aspergillus flavus</named-content>
title_fullStr	The Frequency of Sex: Population Genomics Reveals Differences in Recombination and Population Structure of the Aflatoxin-Producing Fungus <named-content content-type="genus-species">Aspergillus flavus</named-content>
title_full_unstemmed	The Frequency of Sex: Population Genomics Reveals Differences in Recombination and Population Structure of the Aflatoxin-Producing Fungus <named-content content-type="genus-species">Aspergillus flavus</named-content>
title_sort	frequency of sex: population genomics reveals differences in recombination and population structure of the aflatoxin-producing fungus <named-content content-type="genus-species">aspergillus flavus</named-content>
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/26acb7eb45784064ab1448a0a5588ae2
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The Frequency of Sex: Population Genomics Reveals Differences in Recombination and Population Structure of the Aflatoxin-Producing Fungus <named-content content-type="genus-species">Aspergillus flavus</named-content>

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