From the environment to the host: How non-azole agrochemical exposure affects the antifungal susceptibility and virulence of Cryptococcus gattii
Open accessAbstract
Agrochemicals such as the non-azoles, used to improve crop productivity, poses severe undesirable effects on the environment and human health. In addition, they induce cross-resistance (CR) with clinical drugs in pathogenic fungi. However, till date emphasis has been given to the role of azoles on the induction of CR. Herein, we analyzed the effect of a non-azole agrochemical, pyraclostrobin (PCT), on the antifungal susceptibility and virulence of the human and animal pathogens Cryptococcus gattii and C. neoformans. We determined the minimum inhibitory concentration (MIC) of fluconazole (FLC), itraconazole, ravuconazole, amphotericin B, and PCT on colonies: (i) that were not exposed to PCT (non-adapted-NA-cultures), (ii) were exposed at the maximum concentration of PCT (adapted-A-cultures) and (iii) the adapted colonies after cultivation 10 times in PCT-free media (10 passages-10p-cultures). Our results showed that exposure to PCT induced both temporary and permanent CR to clinical azoles in a temperature-dependent manner. With the objective to understand the mechanism of induction of CR through non-azoles, the transcriptomes of NA and 10p cells from C. gattii R265 were analyzed. The transcriptomic analysis showed that expression of the efflux-pump genes (AFR1 and MDR1) and PCT target was higher in resistant 10p cells than that in NA. Moreover, the virulence of 10p cells was reduced as compared to NA cells in mice, as observed by the differential gene expression analysis of genes related to ion-metabolism. Additionally, we observed that FLC could not increase the survival rate of mice infected with 10p cells, confirming the occurrence of permanent CR in vivo. The findings of the present study demonstrate that the non-azole agrochemical PCT can induce permanent CR to clinical antifungals through increased expression of efflux pump genes in resistant cells and that such phenomenon also manifests in vivo.
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Laboratory studies have shown that selection for resistance to environmental agrochemicals, primarily through upregulation of ERG11 and drug efflux pumps, can lead to cross-resistance to clinically deployed antifungals.
“Laboratory studies have shown that selection for resistance to environmental agrochemicals, primarily through the upregulation of the azole target gene ERG11 and drug efflux pumps, can lead to cross-resistance to clinically deployed antifungals19,20.”
From Treatment strategies for cryptococcal infection: challenges, advances and future outlook (2021) · cites this paper as [19]
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Influence of the agrochemical benomyl on Cryptococcus gattii-plant interaction in vitro and in vivo
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“…catappa , Colophospermum mopane , Eucalyptus sp., Pseudotsuga menziesii , and Tsuga heterophylla [4–9]. that agrochemicals, i.e. as pyraclostrobin [14] and tebuco-nazole [15 ] affects Cryptococcus spp. morphophysiology and fungal virulence, altering its susceptibility to clinical antifungals and…”
Self-citationFungal Infections and Climate Change: Emerging Threats, Future Directions, and Clinical Implications
Chastain, D. B., George, M. E., Cluck, D. B., & Henao‐Martínez, A. F. (2026) · Springer eBooks · doi:10.1007/978-3-032-21237-5_15
Antifungal resistance: from classical mechanisms to the expanding role of acetyltransferases
Werneck, S. M. C., Gouveia‐Eufrásio, L., de Freitas, G. J. C., de Carvalho, D. S., César, I. C., Rossato, L. L., Bastos, R. W., Peres, N. T. A., & Santos, D. A. (2026) · Journal of Biomedical Science · doi:10.1186/s12929-026-01273-8
Self-citation
- Authors
- Bastos, R. W., Freitas, G. J. C., Carneiro, H. C. S., Oliveira, L. V. N., Gouveia-Eufrasio, L., Santos, A. P. N., Moyrand, F., Maufrais, C., Janbon, G., & Santos, D. A.
- Affiliations
- Universidade Federal de Minas Gerais (BR)
- Institut Pasteur (FR)
- Corresponding author
- Santos, Daniel Assis
- ORCID
- Venue
- Science of The Total Environment
- Publisher
- Elsevier BV
- Published
- 2019-09
- Volume
- 681
- Pages
- 516-523
- ISSN
- 0048-9697 (ISSN-L)
- OpenAlex
- W2944566098
- Cited by
- 35
- References
- 44
- Citations by year
- 2026: 4 · 2025: 9 · 2024: 5 · 2023: 3 · 2022: 6 · 2021: 6 · 2020: 2
- FWCI
- 2.66
- Type
- journal article
- Language
- en
- Open access
- green
- pasteur.hal.science
- Licence
- Locations
- The Science of The Total Environment (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion, other-oa)
- Funders
- Conselho Nacional de Desenvolvimento Científico e Tecnológico (440010/2018-7, 403006/2016-3)
- Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
- Fundação de Amparo à Pesquisa do Estado de Minas Gerais (APQ-00727-16, PPM-00061-18)
- Topics
- Health Sciences › Medicine › Epidemiology › Fungal Infections and Studies
- Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Fungal Plant Pathogen Control
- Keywords
- Cryptococcus gattii, Cryptococcus neoformans, pyraclostrobin, cross-resistance, azole resistance, antifungal susceptibility, virulence, efflux pump genes, MDR1, transcriptome, fluconazole, itraconazole, ravuconazole, amphotericin B, temperature-dependent resistance, ion metabolism, mouse infection model
- MeSH terms
- Strobilurins, Animals, Antifungal Agents, Cryptococcus neoformans, Humans, Microbial Sensitivity Tests, Agrochemicals, Drug Resistance, Fungal, Mice, Cryptococcus gattii
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