Effects of Agricultural Fungicide Use on <named-content content-type="genus-species">Aspergillus fumigatus</named-content> Abundance, Antifungal Susceptibility, and Population Structure

ABSTRACT Antibiotic resistance is an increasing threat to human health. In the case of Aspergillus fumigatus, which is both an environmental saprobe and an opportunistic human fungal pathogen, resistance is suggested to arise from fungicide use in agriculture, as the azoles used for plant protection...

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Autores principales: Amelia E. Barber, Jennifer Riedel, Tongta Sae-Ong, Kang Kang, Werner Brabetz, Gianni Panagiotou, Holger B. Deising, Oliver Kurzai
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Publicado: American Society for Microbiology 2020
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spelling oai:doaj.org-article:d8072aa7903b4e8e91be158b1e48fce42021-11-15T15:55:44ZEffects of Agricultural Fungicide Use on <named-content content-type="genus-species">Aspergillus fumigatus</named-content> Abundance, Antifungal Susceptibility, and Population Structure10.1128/mBio.02213-202150-7511https://doaj.org/article/d8072aa7903b4e8e91be158b1e48fce42020-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02213-20https://doaj.org/toc/2150-7511ABSTRACT Antibiotic resistance is an increasing threat to human health. In the case of Aspergillus fumigatus, which is both an environmental saprobe and an opportunistic human fungal pathogen, resistance is suggested to arise from fungicide use in agriculture, as the azoles used for plant protection share the same molecular target as the frontline antifungals used clinically. However, limiting azole fungicide use on crop fields to preserve their activity for clinical use could threaten the global food supply via a reduction in yield. In this study, we clarify the link between azole fungicide use on crop fields and resistance in a prototypical human pathogen through systematic soil sampling on farms in Germany and surveying fields before and after fungicide application. We observed a reduction in the abundance of A. fumigatus on fields following fungicide treatment in 2017, a finding that was not observed on an organic control field with only natural plant protection agents applied. However, this finding was less pronounced during our 2018 sampling, indicating that the impact of fungicides on A. fumigatus population size is variable and influenced by additional factors. The overall resistance frequency among agricultural isolates is low, with only 1 to 3% of isolates from 2016 to 2018 displaying resistance to medical azoles. Isolates collected after the growing season and azole exposure show a subtle but consistent decrease in susceptibility to medical and agricultural azoles. Whole-genome sequencing indicates that, despite the alterations in antifungal susceptibility, fungicide application does not significantly affect the population structure and genetic diversity of A. fumigatus in fields. Given the low observed resistance rate among agricultural isolates as well the lack of genomic impact following azole application, we do not find evidence that azole use on crops is significantly driving resistance in A. fumigatus in this context. IMPORTANCE Antibiotic resistance is an increasing threat to human health. In the case of Aspergillus fumigatus, which is an environmental fungus that also causes life-threatening infections in humans, antimicrobial resistance is suggested to arise from fungicide use in agriculture, as the chemicals used for plant protection are almost identical to the antifungals used clinically. However, removing azole fungicides from crop fields threatens the global food supply via a reduction in yield. In this study, we survey crop fields before and after fungicide application. We find a low overall azole resistance rate among agricultural isolates, as well as a lack of genomic and population impact following fungicide application, leading us to conclude azole use on crops does not significantly contribute to resistance in A. fumigatus.Amelia E. BarberJennifer RiedelTongta Sae-OngKang KangWerner BrabetzGianni PanagiotouHolger B. DeisingOliver KurzaiAmerican Society for MicrobiologyarticleAspergillus fumigatusAspergillusantifungal resistanceazolefungicidepopulation genomicsMicrobiologyQR1-502ENmBio, Vol 11, Iss 6 (2020)
institution DOAJ
collection DOAJ
language EN
topic Aspergillus fumigatus
Aspergillus
antifungal resistance
azole
fungicide
population genomics
Microbiology
QR1-502
spellingShingle Aspergillus fumigatus
Aspergillus
antifungal resistance
azole
fungicide
population genomics
Microbiology
QR1-502
Amelia E. Barber
Jennifer Riedel
Tongta Sae-Ong
Kang Kang
Werner Brabetz
Gianni Panagiotou
Holger B. Deising
Oliver Kurzai
Effects of Agricultural Fungicide Use on <named-content content-type="genus-species">Aspergillus fumigatus</named-content> Abundance, Antifungal Susceptibility, and Population Structure
description ABSTRACT Antibiotic resistance is an increasing threat to human health. In the case of Aspergillus fumigatus, which is both an environmental saprobe and an opportunistic human fungal pathogen, resistance is suggested to arise from fungicide use in agriculture, as the azoles used for plant protection share the same molecular target as the frontline antifungals used clinically. However, limiting azole fungicide use on crop fields to preserve their activity for clinical use could threaten the global food supply via a reduction in yield. In this study, we clarify the link between azole fungicide use on crop fields and resistance in a prototypical human pathogen through systematic soil sampling on farms in Germany and surveying fields before and after fungicide application. We observed a reduction in the abundance of A. fumigatus on fields following fungicide treatment in 2017, a finding that was not observed on an organic control field with only natural plant protection agents applied. However, this finding was less pronounced during our 2018 sampling, indicating that the impact of fungicides on A. fumigatus population size is variable and influenced by additional factors. The overall resistance frequency among agricultural isolates is low, with only 1 to 3% of isolates from 2016 to 2018 displaying resistance to medical azoles. Isolates collected after the growing season and azole exposure show a subtle but consistent decrease in susceptibility to medical and agricultural azoles. Whole-genome sequencing indicates that, despite the alterations in antifungal susceptibility, fungicide application does not significantly affect the population structure and genetic diversity of A. fumigatus in fields. Given the low observed resistance rate among agricultural isolates as well the lack of genomic impact following azole application, we do not find evidence that azole use on crops is significantly driving resistance in A. fumigatus in this context. IMPORTANCE Antibiotic resistance is an increasing threat to human health. In the case of Aspergillus fumigatus, which is an environmental fungus that also causes life-threatening infections in humans, antimicrobial resistance is suggested to arise from fungicide use in agriculture, as the chemicals used for plant protection are almost identical to the antifungals used clinically. However, removing azole fungicides from crop fields threatens the global food supply via a reduction in yield. In this study, we survey crop fields before and after fungicide application. We find a low overall azole resistance rate among agricultural isolates, as well as a lack of genomic and population impact following fungicide application, leading us to conclude azole use on crops does not significantly contribute to resistance in A. fumigatus.
format article
author Amelia E. Barber
Jennifer Riedel
Tongta Sae-Ong
Kang Kang
Werner Brabetz
Gianni Panagiotou
Holger B. Deising
Oliver Kurzai
author_facet Amelia E. Barber
Jennifer Riedel
Tongta Sae-Ong
Kang Kang
Werner Brabetz
Gianni Panagiotou
Holger B. Deising
Oliver Kurzai
author_sort Amelia E. Barber
title Effects of Agricultural Fungicide Use on <named-content content-type="genus-species">Aspergillus fumigatus</named-content> Abundance, Antifungal Susceptibility, and Population Structure
title_short Effects of Agricultural Fungicide Use on <named-content content-type="genus-species">Aspergillus fumigatus</named-content> Abundance, Antifungal Susceptibility, and Population Structure
title_full Effects of Agricultural Fungicide Use on <named-content content-type="genus-species">Aspergillus fumigatus</named-content> Abundance, Antifungal Susceptibility, and Population Structure
title_fullStr Effects of Agricultural Fungicide Use on <named-content content-type="genus-species">Aspergillus fumigatus</named-content> Abundance, Antifungal Susceptibility, and Population Structure
title_full_unstemmed Effects of Agricultural Fungicide Use on <named-content content-type="genus-species">Aspergillus fumigatus</named-content> Abundance, Antifungal Susceptibility, and Population Structure
title_sort effects of agricultural fungicide use on <named-content content-type="genus-species">aspergillus fumigatus</named-content> abundance, antifungal susceptibility, and population structure
publisher American Society for Microbiology
publishDate 2020
url https://doaj.org/article/d8072aa7903b4e8e91be158b1e48fce4
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