Dataset Information

Isolation of azole-resistant Aspergillus fumigatus from imported plant bulbs in Japan and the effect of fungicide treatment.

ABSTRACT: Increasing numbers of azole-resistant Aspergillus fumigatus (ARAf) in the environment have become a global public health issue. We surveyed tulip bulbs that were imported from the Netherlands and found that 6.3-15.8% of bulbs were contaminated by ARAf with a tandem-repeat mutation in the promoter region of the cyp51A gene. We also showed that fungicide treatment of the tulip bulbs by benomyl or prochloraz effectively reduced the rate of isolation. This is the first report demonstrating a method of eliminating human fungal pathogens from plant bulbs.

SUBMITTER: Hagiwara D

PROVIDER: S-EPMC7453303 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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Isolation of azole-resistant Aspergillus fumigatus from imported plant bulbs in Japan and the effect of fungicide treatment.

Hagiwara Daisuke D

Journal of pesticide science 20200801 3

Increasing numbers of azole-resistant Aspergillus fumigatus (ARAf) in the environment have become a global public health issue. We surveyed tulip bulbs that were imported from the Netherlands and found that 6.3-15.8% of bulbs were contaminated by ARAf with a tandem-repeat mutation in the promoter region of the cyp51A gene. We also showed that fungicide treatment of the tulip bulbs by benomyl or prochloraz effectively reduced the rate of isolation. This is the first re ...[more]

PMID: 32913417

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Project description:Aspergillus fumigatus is a ubiquitous fungus, a saprophyte of plants, and an opportunistic pathogen of humans. Azole fungicides are used in agriculture to control plant pathogens, and azoles are also used as a first line of treatment for aspergillosis. The continued exposure of A. fumigatus to azoles in the environment has likely led to azole resistance in the clinic where infections result in high levels of mortality. Pan-azole resistance in environmental isolates is most often associated with tandem-repeat (TR) mutations containing 34 or 46 nucleotides in the cyp51A gene. Because the rapid detection of resistance is important for public health, PCR-based techniques have been developed to detect TR mutations in clinical samples. We are interested in identifying agricultural environments conducive to resistance development, but environmental surveillance of resistance has focused on labor-intensive isolation of the fungus followed by screening for resistance. Our goal was to develop assays for the rapid detection of pan-azole-resistant A. fumigatus directly from air, plants, compost, and soil samples. To accomplish this, we optimized DNA extractions for air filters, soil, compost, and plant debris and standardized two nested-PCR assays targeting the TR mutations. Sensitivity and specificity of the assays were tested using A. fumigatus DNA from wild type and TR-based resistant isolates and with soil and air filters spiked with conidia of the same isolates. The nested-PCR assays were sensitive to 5 fg and specific to A. fumigatus without cross-reaction with DNA from other soil microorganisms. Environmental samples from agricultural settings in Georgia, USA were sampled and tested. The TR46 allele was recovered from 30% of samples, including air, soil and plant debris samples from compost, hibiscus and hemp. These assays allow rapid surveillance of resistant isolates directly from environmental samples improving our identification of hotspots of azole-resistant A. fumigatus.

Project description:Azole resistance in pathogenic Aspergillus fumigatus has become a global public health issue threatening the use of medical azoles. The environmentally occurring resistance mutations, TR34/L98H (TR34) and TR46/Y121F/T289A (TR46), are widespread across multiple continents and emerging in the United States. We used whole-genome single nucleotide polymorphism (SNP) analysis on 179 nationally represented clinical and environmental A. fumigatus genomes from the United States along with 18 non-U.S. genomes to evaluate the genetic diversity and foundation of the emergence of azole resistance in the United States. We demonstrated the presence of clades of A. fumigatus isolates: clade A (17%) comprised a global collection of clinical and environmental azole-resistant strains, including all strains with the TR34/L98H allele from India, The Netherlands, the United Kingdom, and the United States, and clade B (83%) consisted of isolates without this marker mainly from the United States. The TR34/L98H polymorphism was shared among azole-resistant A. fumigatus strains from India, The Netherlands, the United Kingdom, and the United States, suggesting the common origin of this resistance mechanism. Six percent of azole-resistant A. fumigatus isolates from the United States with the TR34 resistance marker had a mixture of clade A and clade B alleles, suggestive of recombination. Additionally, the presence of equal proportions of both mating types further suggests the ongoing presence of recombination. This study demonstrates the genetic background for the emergence of azole resistance in the United States, supporting a single introduction and subsequent propagation, possibly through recombination of environmentally driven resistance mutations. IMPORTANCE Aspergillus fumigatus is one of the most common causes of invasive mold infections in patients with immune deficiencies and has also been reported in patients with severe influenza and severe acute respiratory syndrome coronavirus 2 (SARs-CoV-2). Triazole drugs are the first line of therapy for this infection; however, their efficacy has been compromised by the emergence of azole resistance in A. fumigatus, which was proposed to be selected for by exposure to azole fungicides in the environment [P. E. Verweij, E. Snelders, G. H. J. Kema, E. Mellado, et al., Lancet Infect Dis 9:789-795, 2009, https://doi.org/10.1016/S1473-3099(09)70265-8]. Isolates with environmentally driven resistance mutations, TR34/L98H (TR34) and TR46/Y121F/T289A (TR46), have been reported worldwide. Here, we used genomic analysis of a large sample of resistant and susceptible A. fumigatus isolates to demonstrate a single introduction of TR34 in the United States and suggest its ability to spread into the susceptible population is through recombination between resistant and susceptible isolates.

Dataset Information

Isolation of azole-resistant Aspergillus fumigatus from imported plant bulbs in Japan and the effect of fungicide treatment.

Publications

Isolation of azole-resistant <i>Aspergillus fumigatus</i> from imported plant bulbs in Japan and the effect of fungicide treatment.

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