Epidemiological Studies of Pan-Azole Resistant <i>Aspergillus fumigatus</i> Populations Sampled during Tulip Cultivation Show Clonal Expansion with Acquisition of Multi-Fungicide Resistance as Potential Driver

Pan-azole resistant isolates are found in clinical and environmental <i>Aspergillus fumigatus</i> (<i>Af</i>) populations. Azole resistance can evolve in both settings, with <i>Af</i> directly targeted by antifungals in patients and, in the environment, <i>A...

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Main Authors: Bart A. Fraaije, Sarah L. Atkins, Ricardo F. Santos, Steven J. Hanley, Jonathan S. West, John A. Lucas
Format: Article
Language:English
Published: MDPI AG 2021-11-01
Series:Microorganisms
Subjects:
Online Access:https://www.mdpi.com/2076-2607/9/11/2379
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author Bart A. Fraaije
Sarah L. Atkins
Ricardo F. Santos
Steven J. Hanley
Jonathan S. West
John A. Lucas
author_facet Bart A. Fraaije
Sarah L. Atkins
Ricardo F. Santos
Steven J. Hanley
Jonathan S. West
John A. Lucas
author_sort Bart A. Fraaije
collection DOAJ
description Pan-azole resistant isolates are found in clinical and environmental <i>Aspergillus fumigatus</i> (<i>Af</i>) populations. Azole resistance can evolve in both settings, with <i>Af</i> directly targeted by antifungals in patients and, in the environment, <i>Af</i> unintendedly exposed to fungicides used for material preservation and plant disease control. Resistance to non-azole fungicides, including methyl benzimidazole carbamates (MBCs), quinone outside inhibitors (QoIs) and succinate dehydrogenase inhibitors (SDHIs), has recently been reported. These fungicide groups are not used in medicine but can play an important role in the further spread of pan-azole resistant genotypes. We investigated the multi-fungicide resistance status and the genetic diversity of <i>Af</i> populations sampled from tulip field soils, tulip peel waste and flower compost heaps using fungicide sensitivity testing and a range of genotyping tools, including STR<i>Af</i> typing and sequencing of fungicide resistant alleles. Two major clones were present in the tulip bulb population. Comparisons with clinical isolates and literature data revealed that several common clonal lineages of TR<sub>34</sub>/L98H and TR<sub>46</sub>/Y121F/T289A strains that have expanded successfully in the environment have also acquired resistance to MBC, QoI and/or SDHI fungicides. Strains carrying multiple fungicide resistant alleles have a competitive advantage in environments where residues of multiple fungicides belonging to different modes of action are present.
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spelling doaj.art-0b406c6f2e1a46ef8d33ff64c4ee22522023-11-23T00:30:35ZengMDPI AGMicroorganisms2076-26072021-11-01911237910.3390/microorganisms9112379Epidemiological Studies of Pan-Azole Resistant <i>Aspergillus fumigatus</i> Populations Sampled during Tulip Cultivation Show Clonal Expansion with Acquisition of Multi-Fungicide Resistance as Potential DriverBart A. Fraaije0Sarah L. Atkins1Ricardo F. Santos2Steven J. Hanley3Jonathan S. West4John A. Lucas5NIAB, Cambridge CB3 0LE, UKNIAB, Cambridge CB3 0LE, UKLuiz de Queiroz College of Agriculture, University of São Paulo, Piracicaba 13418-900, SP, BrazilRothamsted Research, Harpenden AL5 2Q, UKRothamsted Research, Harpenden AL5 2Q, UKRothamsted Research, Harpenden AL5 2Q, UKPan-azole resistant isolates are found in clinical and environmental <i>Aspergillus fumigatus</i> (<i>Af</i>) populations. Azole resistance can evolve in both settings, with <i>Af</i> directly targeted by antifungals in patients and, in the environment, <i>Af</i> unintendedly exposed to fungicides used for material preservation and plant disease control. Resistance to non-azole fungicides, including methyl benzimidazole carbamates (MBCs), quinone outside inhibitors (QoIs) and succinate dehydrogenase inhibitors (SDHIs), has recently been reported. These fungicide groups are not used in medicine but can play an important role in the further spread of pan-azole resistant genotypes. We investigated the multi-fungicide resistance status and the genetic diversity of <i>Af</i> populations sampled from tulip field soils, tulip peel waste and flower compost heaps using fungicide sensitivity testing and a range of genotyping tools, including STR<i>Af</i> typing and sequencing of fungicide resistant alleles. Two major clones were present in the tulip bulb population. Comparisons with clinical isolates and literature data revealed that several common clonal lineages of TR<sub>34</sub>/L98H and TR<sub>46</sub>/Y121F/T289A strains that have expanded successfully in the environment have also acquired resistance to MBC, QoI and/or SDHI fungicides. Strains carrying multiple fungicide resistant alleles have a competitive advantage in environments where residues of multiple fungicides belonging to different modes of action are present.https://www.mdpi.com/2076-2607/9/11/2379fungicide resistanceazole fungicidesfungicide target proteinsCYP51Aaspergillosis<i>Aspergillus fumigatus</i>
spellingShingle Bart A. Fraaije
Sarah L. Atkins
Ricardo F. Santos
Steven J. Hanley
Jonathan S. West
John A. Lucas
Epidemiological Studies of Pan-Azole Resistant <i>Aspergillus fumigatus</i> Populations Sampled during Tulip Cultivation Show Clonal Expansion with Acquisition of Multi-Fungicide Resistance as Potential Driver
Microorganisms
fungicide resistance
azole fungicides
fungicide target proteins
CYP51A
aspergillosis
<i>Aspergillus fumigatus</i>
title Epidemiological Studies of Pan-Azole Resistant <i>Aspergillus fumigatus</i> Populations Sampled during Tulip Cultivation Show Clonal Expansion with Acquisition of Multi-Fungicide Resistance as Potential Driver
title_full Epidemiological Studies of Pan-Azole Resistant <i>Aspergillus fumigatus</i> Populations Sampled during Tulip Cultivation Show Clonal Expansion with Acquisition of Multi-Fungicide Resistance as Potential Driver
title_fullStr Epidemiological Studies of Pan-Azole Resistant <i>Aspergillus fumigatus</i> Populations Sampled during Tulip Cultivation Show Clonal Expansion with Acquisition of Multi-Fungicide Resistance as Potential Driver
title_full_unstemmed Epidemiological Studies of Pan-Azole Resistant <i>Aspergillus fumigatus</i> Populations Sampled during Tulip Cultivation Show Clonal Expansion with Acquisition of Multi-Fungicide Resistance as Potential Driver
title_short Epidemiological Studies of Pan-Azole Resistant <i>Aspergillus fumigatus</i> Populations Sampled during Tulip Cultivation Show Clonal Expansion with Acquisition of Multi-Fungicide Resistance as Potential Driver
title_sort epidemiological studies of pan azole resistant i aspergillus fumigatus i populations sampled during tulip cultivation show clonal expansion with acquisition of multi fungicide resistance as potential driver
topic fungicide resistance
azole fungicides
fungicide target proteins
CYP51A
aspergillosis
<i>Aspergillus fumigatus</i>
url https://www.mdpi.com/2076-2607/9/11/2379
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