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Genetic Diversity and Azole Resistance Among Natural Aspergillus fumigatus Populations in Yunnan, China

Abstract

The emergence and spread of azole resistance alleles in clinical and environmental isolates of Aspergillus fumigatus is a global human health concern and endangers the “One Health” approach in our fight against antifungal resistance (AFR) in this pathogen. A major challenge to combat AFR in A. fumigatus is the massive aerial dispersal ability of its asexual spores. Our recent fine-scale survey of greenhouse populations of A. fumigatus near Kunming, Yunnan, China, suggested that the use of azole fungicides for plant protection was likely a major driver of the high-frequency azole-resistant A. fumigatus (ARAF) in greenhouses. Here, we investigated the potential spread of those ARAF and the structure of geographic populations of A. fumigatus by analyzing 452 isolates from 19 geographic locations across Yunnan. We found lower frequencies of ARAF in these outdoor populations than those in greenhouses near Kunming, but there were abundant new alleles and new genotypes, including those associated with azole resistance, consistent with multiple independent origins of ARAF across Yunnan. Interestingly, among the four ecological niches, the sediments of a large lake near Kunming were found to have the highest frequency of ARAF (~ 43%). While most genetic variations were observed within the 19 local populations, statistically significant genetic differentiations were found between many subpopulations within Yunnan. Furthermore, similar to greenhouse populations, these outdoor populations of A. fumigatus in Yunnan were significantly different from those in other parts of the world. Our results call for increased attention to local and regional studies of this fungal pathogen to help develop targeted control strategies against ARAF.

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Acknowledgments

We thank Karen Nelson and Michael Schloter for the invitation. Additionally, we thank Shaojuan Wang, Meizi Mo, and Meiling Fang for their help in sample collections.

Funding

This research is jointly supported by funding from the National Natural Science Foundation of China (31760010 to Y.Z.), the Science and Technology for Youth Talent Growth Project of the Guizhou Provincial Education Department (KY2018412 to D.Z.), the Top Young Talents Program of the 10 Thousand Talents Plan in Yunnan Province (to Y.Z.), and the Global Science Initiative Award of McMaster University (to J.X.).

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Conceptualization, J.X. and Y.Z.; methodology, D.Z., R.W., X.L., B.P., and G.Y.; software, D.Z., R.W. and X.L.; validation, Y.Z. and J.X.; formal analysis, D.Z., R.W. and B.P.; investigation, D.Z., R.W., X.L., B.P., and G.Y.; writing, original draft preparation, D.Z. and Y.Z.; writing, review and editing, J.X. and Y.Z.; visualization, J.X. and Y.Z.; supervision, Y.Z. K.Z. and J.X.; project administration, Y.Z. K.Z. and J.X.; funding acquisition, Y.Z. K.Z. and J.X. All authors have read and agreed to the published version of the manuscript.

Corresponding authors

Correspondence to Ying Zhang or Jianping Xu.

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Mantel test of the relationship between Nei’s genetic distance (NeiP) and geographical distance (GGD). (PNG 347 kb)

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Zhou, D., Wang, R., Li, X. et al. Genetic Diversity and Azole Resistance Among Natural Aspergillus fumigatus Populations in Yunnan, China. Microb Ecol (2021). https://doi.org/10.1007/s00248-021-01804-w

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Keywords

  • Azole resistance
  • Fungicide
  • Genetic enrichment
  • Unique allele
  • Independent origin