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

  • Fungal Microbiology
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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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References

  1. Samson R, Visagie C, Houbraken J, Hong S-B, Hubka V, Klaassen C, Perrone G, Seifert K, Susca A, Tanney J, Varga J, Kocsubé S, Szigeti G, Yaguchi T, Frisvad J (2014) Phylogeny, identification and nomenclature of the genus Aspergillus. Studi Mycol 78:141–173. https://doi.org/10.1016/j.simyco.2014.07.004

    Article  CAS  Google Scholar 

  2. Pérez-Cantero A, López Fernández L, Guarro-Artigas J, Capilla J (2019) Azole resistance mechanisms in Aspergillus: update and recent advances. Int J Antimicrob Agent 55:105807. https://doi.org/10.1016/j.ijantimicag.2019.09.011

    Article  CAS  Google Scholar 

  3. Ashu E, Hagen F, Chowdhary A, Meis J, Xu J (2017) Global population genetic analysis of Aspergillus fumigatus. mSphere 2:e00019–e00017. https://doi.org/10.1128/mSphere.00019-17

    Article  PubMed  PubMed Central  Google Scholar 

  4. Kosmidis C, Denning D (2015) Republished: the clinical spectrum of pulmonary aspergillosis. Postgraduate Med J 91:403–410. https://doi.org/10.1136/thoraxjnl-2014-206291

    Article  Google Scholar 

  5. Sewell T, Zhu J, Rhodes J, Meis J, Fisher M, Jombart T (2019) Nonrandom distribution of azole resistance across the global population of Aspergillus fumigatus. mBio 10:e00392–e00319. https://doi.org/10.1128/mBio.00392-19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Garcia-Rubio R, Cuenca-Estrella M, Mellado E (2017) Triazole resistance in Aspergillus species: an emerging problem. Drugs 77:599–613. https://doi.org/10.1007/s40265-017-0714-4

    Article  CAS  PubMed  Google Scholar 

  7. Chen Y, Dong F, Zhao J, Fan H, Qin C, Li R, Verweij P, Zheng Y-Q, Han L (2020) High azole resistance in Aspergillus fumigatus isolates from strawberry fields, China, 2018. Emerg Infect Dis 26:81–89. https://doi.org/10.3201/eid2601.190885

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Verweij PE, Chowdhary A, Melchers WJG, Meis JF (2016) Azole resistance in Aspergillus fumigatus: can we retain the clinical use of mold-active antifungal azoles? Clin Infect Dis 62:362–368. https://doi.org/10.1093/cid/civ885

    Article  CAS  PubMed  Google Scholar 

  9. Denning D, Radford SA, Oakley K, Hall L, Johnson E, Warnock D (1997) Correlation between in-vitro susceptibility testing to itraconazole and in-vivo outcome of Aspergillus fumigatus Infection. J Antimicrob Chemother 40:401–414. https://doi.org/10.1093/jac/40.3.401

    Article  CAS  PubMed  Google Scholar 

  10. Mullins J, Harvey R, Seaton A (1976) Sources and incidence of airborne Aspergillus fumigatus (Fres). Clin Aller 6:209–217. https://doi.org/10.1111/j.1365-2222.1976.tb01899.x

    Article  CAS  Google Scholar 

  11. Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, McCraw SL, Gurr SJ (2012) Emerging fungal threats to animal, plant and ecosystem health. Nature 484:186–194. https://doi.org/10.1038/nature10947

    Article  CAS  PubMed  Google Scholar 

  12. Snelders E, Camps SM, Karawajczyk A, Schaftenaar G, Kema GH, van der Lee HA, Klaassen CH, Melchers WJ, Verweij PE (2012) Triazole fungicides can induce cross-resistance to medical triazoles in Aspergillus fumigatus. PLoS ONE 7:e31801. https://doi.org/10.1371/journal.pone.0031801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Snelders E, Huis RA, Rijs AJ, Kema GH, Melchers WJ, Verweij PE (2009) Possible environmental origin of resistance of Aspergillus fumigatus to medical triazoles. Appl Environ Microb 75:4053–4057. https://doi.org/10.1128/aem.00231-09

    Article  CAS  Google Scholar 

  14. Buil JB, Hagen F, Chowdhary A, Verweij PE, Meis JF (2018) Itraconazole, voriconazole, and posaconazole CLSI MIC distributions for wild-type and azole-resistant Aspergillus fumigatus Isolates. J Fungi 4:103. https://doi.org/10.3390/jof4030103

    Article  CAS  Google Scholar 

  15. Chowdhary A, Meis JF (2018) Emergence of azole resistant Aspergillus fumigatus and One Health: time to implement environmental stewardship. Environ Microbiol 20:1299–1301. https://doi.org/10.1111/1462-2920.14055

    Article  PubMed  Google Scholar 

  16. Zhou D, Korfanty GA, Mo M, Wang R, Li X, Li H, Li S, Wu JY, Zhang KQ, Zhang Y, Xu J (2021) Extensive genetic diversity and widespread azole resistance in greenhouse populations of Aspergillus fumigatus in Yunnan, China. mSphere 6:e00066–e00021. https://doi.org/10.1128/mSphere.00066-21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Korfanty G, Teng L, Pum N, Xu J (2019) Contemporary gene flow is a major force shaping the Aspergillus fumigatus population in Auckland, New Zealand. Mycopathologia 184:479–492. https://doi.org/10.1007/s11046-019-00361-8

    Article  CAS  PubMed  Google Scholar 

  18. Garcia-Rubio R, Escribano P, Gomez A, Guinea J, Mellado E (2018) Comparison of two highly discriminatory typing methods to analyze Aspergillus fumigatus azole resistance. Front Microbiol 9:1626–1626. https://doi.org/10.3389/fmicb.2018.01626

    Article  PubMed  PubMed Central  Google Scholar 

  19. Valk H, Meis J, Curfs-Breuker I, Muehlethaler K, Mouton J, Klaassen C (2005) Use of a novel panel of nine short tandem repeats for exact and high-resolution fingerprinting of Aspergillus fumigatus isolates. J Clin Microbiol 43:4112–4120. https://doi.org/10.1128/jcm.43.8.4112-4120.2005

    Article  PubMed  PubMed Central  Google Scholar 

  20. Hagiwara D, Watanabe A, Kamei K, Goldman GH (2016) Epidemiological and genomic landscape of azole resistance mechanisms in Aspergillus fungi. Front Microbiol 7. https://doi.org/10.3389/fmicb.2016.01382

  21. van der Torre MH, Novak-Frazer L, Rautemaa-Richardson R (2020) Detecting azole-antifungal resistance in Aspergillus fumigatus by pyrosequencing. J Fungi 6:12. https://doi.org/10.3390/jof6010012

    Article  CAS  Google Scholar 

  22. Wiederhold NP, Verweij PE (2020) Aspergillus fumigatus and pan-azole resistance: who should be concerned? Curr Opin Infect Dis 33:290–297. https://doi.org/10.1097/qco.0000000000000662

    Article  CAS  PubMed  Google Scholar 

  23. Howard SJ, Cerar D, Anderson MJ, Albarrag A, Fisher MC, Pasqualotto AC, Laverdiere M, Arendrup MC, Perlin DS, Denning DW (2009) Frequency and evolution of azole resistance in Aspergillus fumigatus associated with treatment failure. Emerg Infect Dis 15:1068–1076. https://doi.org/10.3201/eid1507.090043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Lockhart SR, Frade JP, Etienne KA, Pfaller MA, Diekema DJ, Balajee SA (2011) Azole resistance in Aspergillus fumigatus isolates from the ARTEMIS global surveillance study is primarily due to the TR/L98H mutation in the cyp51A gene. Antimicrob Agents Chemother 55:4465–4468. https://doi.org/10.1128/aac.00185-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Mellado E, Garcia-Effron G, Alcázar-Fuoli L, Melchers WJ, Verweij PE, Cuenca-Estrella M, Rodríguez-Tudela JL (2007) A new Aspergillus fumigatus resistance mechanism conferring in vitro cross-resistance to azole antifungals involves a combination of cyp51A alterations. Antimicrob Agents Chemother 51:1897–1904. https://doi.org/10.1128/aac.01092-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Ren J, Jin X, Zhang Q, Zheng Y, Lin D, Yu YL (2017) Fungicides induced triazole-resistance in Aspergillus fumigatus associated with mutations of TR46/Y121F/T289A and its appearance in agricultural fields. J Hazard Mater 326:54–60. https://doi.org/10.1016/j.jhazmat.2016.12.013

    Article  CAS  PubMed  Google Scholar 

  27. van der Linden JW, Camps SM, Kampinga GA, Arends JP, Debets-Ossenkopp YJ, Haas PJ, Rijnders BJ, Kuijper EJ, van Tiel FH, Varga J, Karawajczyk A, Zoll J, Melchers WJ, Verweij PE (2013) Aspergillosis due to voriconazole highly resistant Aspergillus fumigatus and recovery of genetically related resistant isolates from domiciles. Clin Infect Dis 57:513–520. https://doi.org/10.1093/cid/cit320

    Article  CAS  PubMed  Google Scholar 

  28. Hare RK, Gertsen JB, Astvad KMT, Degn KB, Løkke A, Stegger M, Andersen PS, Kristensen L, Arendrup MC (2019) In vivo selection of a unique tandem repeat mediated azole resistance mechanism TR(120) in Aspergillus fumigatus cyp51A, Denmark. E Emerg Infect Dis 25:577–580. https://doi.org/10.3201/eid2503.180297

    Article  CAS  Google Scholar 

  29. Alvarez-Moreno C, Lavergne RA, Hagen F, Morio F, Meis JF, Le Pape P (2017) Azole-resistant Aspergillus fumigatus harboring TR(34)/L98H, TR(46)/Y121F/T289A and TR(53) mutations related to flower fields in Colombia. Sci Rep 7:45631. https://doi.org/10.1038/srep45631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Hodiamont CJ, Dolman KM, Ten Berge IJ, Melchers WJ, Verweij PE, Pajkrt D (2009) Multiple-azole-resistant Aspergillus fumigatus osteomyelitis in a patient with chronic granulomatous disease successfully treated with long-term oral posaconazole and surgery. Med Mycol 47:217–220. https://doi.org/10.1080/13693780802545600

    Article  CAS  PubMed  Google Scholar 

  31. Li Y, Zhang Y, Lu L (2019) Calcium signaling pathway is involved in non-CYP51 azole resistance in Aspergillus fumigatus. Med Mycol 57:S233–s238. https://doi.org/10.1093/mmy/myy075

    Article  CAS  PubMed  Google Scholar 

  32. Fraaije B, Atkins S, Hanley S, Macdonald A, Lucas J (2020) The multi-fungicide resistance status of Aspergillus fumigatus populations in arable soils and the wider European environment. Front Microbiol 11:599233. https://doi.org/10.3389/fmicb.2020.599233

    Article  PubMed  PubMed Central  Google Scholar 

  33. Rybak J, Ge W, Wiederhold N, Parker J, Kelly S, Rogers P, Fortwendel J (2019) Mutations in hmg1, challenging the paradigm of clinical triazole resistance in Aspergillus fumigatus. mBio 10:e00437–e00419. https://doi.org/10.1128/mBio.00437-19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Cao D, Wu R, Dong S, Wang F, Ju C, Yu S, Xu S, Fang H, Yu YL (2020) Azole resistance in environmental Aspergillus fumigatus isolates from China: a five-year survey from 2014 to 2018. Antimicrob Agent Chemother 64:e00904–e00920. https://doi.org/10.1128/AAC.00904-20

    Article  CAS  Google Scholar 

  35. Feng B, Yang Z (2018) Studies on diversity of higher fungi in Yunnan, southwestern China: a review. Plant Divers 40:165–171. https://doi.org/10.1016/j.pld.2018.07.001

    Article  PubMed  PubMed Central  Google Scholar 

  36. Zhang Y, Yang G, Fang M, Deng C, Xu J (2020) Comparative analyses of mitochondrial genomes provide evolutionary insights into nematode-trapping fungi. Front Microbiol 11:617. https://doi.org/10.3389/fmicb.2020.00617

    Article  PubMed  PubMed Central  Google Scholar 

  37. White T, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DA, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Deigo, pp 315–322

    Google Scholar 

  38. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  39. Snelders E, Karawajczyk A, Schaftenaar G, Verweij PE, Melchers WJ (2010) Azole resistance profile of amino acid changes in Aspergillus fumigatus CYP51A based on protein homology modeling. Antimicrob Agents Chemother 54:2425–2430. https://doi.org/10.1128/aac.01599-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Ashu EE, Korfanty GA, Xu JP (2017) Evidence of unique genetic diversity in Aspergillus fumigatus isolates from Cameroon. Mycoses 60:739–748. https://doi.org/10.1111/myc.12655

    Article  CAS  PubMed  Google Scholar 

  41. Ashu EE, Kim GY, Roy-Gayos P, Dong K, Forsythe A, Giglio V, Korfanty G, Yamamura D, Xu J (2018) Limited evidence of fungicide-driven triazole-resistant Aspergillus fumigatus in Hamilton, Canada. Can J Microbiol 64:119–130. https://doi.org/10.1139/cjm-2017-0410

    Article  CAS  PubMed  Google Scholar 

  42. Korfanty G, Stanley K, Lammers K, Fan Y, Xu J (2021) Variations in sexual fitness among natural strains of the opportunistic human fungal pathogen Aspergillus fumigatus. Infect Genet Evol 87:104640. https://doi.org/10.1016/j.meegid.2020.104640

    Article  CAS  PubMed  Google Scholar 

  43. O’Gorman CM, Fuller HT, Dyer PS (2009) Discovery of a sexual cycle in the opportunistic fungal pathogen Aspergillus fumigatus. Nature 457:471–474. https://doi.org/10.1038/nature07528

    Article  CAS  PubMed  Google Scholar 

  44. Camps SM, Rijs AJ, Klaassen CH, Meis JF, O ' Gorman CM, Dyer PS, Melchers WJ, Verweij PE (2012) Molecular epidemiology of Aspergillus fumigatus isolates harboring the TR34/L98H azole resistance mechanism. J Clin Microbiol 50:2674–2680. https://doi.org/10.1128/jcm.00335-12

    Article  PubMed  PubMed Central  Google Scholar 

  45. Zhang R, Ma T (2020) Analysis on pesticide use of main grain crops in Yunnan province in 2019. Yunnan Agricultural Science and Technology. 3:13–16

    Google Scholar 

  46. Zhao J, Liu Y, Ma L (2020) Pesticide market investigation and analysis of Yunnan province in 2019. Pesticide Science and Administration. 41(3):25–28

    Google Scholar 

  47. Zhang J, Snelders E, Zwaan BJ, Schoustra SE, Meis JF, van Dijk K, Hagen F, van der Beek MT, Kampinga GA, Zoll J, Melchers WJG, Verweij PE, Debets AJM (2017) A novel environmental azole resistance mutation in Aspergillus fumigatus and a possible role of sexual reproduction in its emergence. mBio 8: e00791-17. https://doi.org/10.1128/mBio.00791-17

  48. Chen Y, Lu Z, Jingjun Z, Zou Z, Gong Y, Qu F, Bao Z, Qiu G, Song M, Zhang Q, Liu L, Hu M, Han X, Shuguang T, Zhao J, Fangyan C, Zhang C, Sun Y, Verweij P, Han L (2016) Epidemiology and molecular characterizations of azole resistance in clinical and environmental Aspergillus fumigatus from China. Antimicrob Agent Chemother 60:5878–5884. https://doi.org/10.1128/aac.01005-16

    Article  CAS  Google Scholar 

  49. Barber AE, Riedel J, Sae-Ong T, Kang K, Brabetz W, Panagiotou G, Deising HB, Kurzai O (2020) Effects of agricultural fungicide use on Aspergillus fumigatus abundance, antifungal susceptibility, and population structure. mBio 11:e02213–e02220. https://doi.org/10.1128/mBio.02213-20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Ribas AD, Spolti P, Del Ponte EM, Donato KZ, Schrekker H, Fuentefria AM (2016) Is the emergence of fungal resistance to medical triazoles related to their use in the agroecosystems? A mini review. Brazil J Microbiol 47:793–799. https://doi.org/10.1016/j.bjm.2016.06.006

    Article  CAS  Google Scholar 

  51. Morio F, Aubin G, Danner-Boucher I, Haloun A, Sacchetto E, Garcia-Hermoso D, Bretagne S, Miegeville M, Le Pape P (2012) High prevalence of triazole resistance in Aspergillus fumigatus, especially mediated by TR/L98H, in a French cohort of patients with cystic fibrosis. J Antimicrob Chemother 67:1870–1873. https://doi.org/10.1093/jac/dks160

    Article  CAS  PubMed  Google Scholar 

  52. Bader O, Weig M, U R, R L, Kuhns M, M C, Held J, S P, Schumacher U, Buchheidt D (2013) cyp51A-based mechanisms of Aspergillus fumigatus azole drug resistance present in clinical samples from Germany. Antimicrob Agents Chemother 57:3513–3517. https://doi.org/10.1128/AAC.00167-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Berkow EL, Nunnally NS, Bandea A, Kuykendall R, Beer K, Lockhart SR (2018) Detection of TR(34)/L98H CYP51A mutation through passive surveillance for azole-resistant Aspergillus fumigatus in the United States from 2015 to 2017. Antimicrob Agents Chemother:62. https://doi.org/10.1128/aac.02240-17

  54. Chowdhary A, Sharma C, Kathuria S, Hagen F, Meis JF (2015) Prevalence and mechanism of triazole resistance in Aspergillus fumigatus in a referral chest hospital in Delhi, India and an update of the situation in Asia. Front Microbiol 6:428. https://doi.org/10.3389/fmicb.2015.00428

    Article  PubMed  PubMed Central  Google Scholar 

  55. Lee HJ, Cho SY, Lee DG, Park C, Chun HS, Park YJ (2018) TR34/L98H mutation in cyp51A gene in Aspergillus fumigatus clinical isolates during posaconazole prophylaxis: first case in Korea. Mycopathologia 183:731–736. https://doi.org/10.1007/s11046-018-0271-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Ahangarkani F, Badali H, Abbasi K, Nabili M, Khodavaisy S, de Groot T, Meis JF (2020) Clonal expansion of environmental triazole resistant Aspergillus fumigatus in Iran. J Fungi 6:199. https://doi.org/10.3390/jof6040199

    Article  CAS  Google Scholar 

  57. Wu C-J, Wang H-C, Lee J-C, Lo H-J, Dai C-T, Chou P-H, Ko W-C, Chen Y-C (2015) Azole-resistant Aspergillus fumigatus isolates carrying TR34/L98H mutations in Taiwan. Mycoses 58:544–549. https://doi.org/10.1111/myc.12354

    Article  CAS  PubMed  Google Scholar 

  58. Risum M, Hare RK, Gertsen JB, Kristensen L, Johansen HK, Helweg-Larsen J, Abou-Chakra N, Pressler T, Skov M, Jensen-Fangel S, Arendrup MC (2020) Azole-resistant Aspergillus fumigatus among Danish cystic fibrosis patients: increasing prevalence and dominance of TR34/L98H. Front Microb 11. https://doi.org/10.3389/fmicb.2020.01850

  59. Pinto E, Monteiro C, Maia M, Faria MA, Lopes V, Lameiras C, Pinheiro D (2018) Aspergillus species and antifungals susceptibility in clinical setting in the North of Portugal: cryptic species and emerging azoles resistance in A. fumigatus. Front Microb:9. https://doi.org/10.3389/fmicb.2018.01656

  60. Rodriguez-Tudela JL, Alcazar-Fuoli L, Mellado E, Alastruey-Izquierdo A, Monzon A, Cuenca-Estrella M (2008) Epidemiological cutoffs and cross-resistance to azole drugs in Aspergillus fumigatus. Antimicrob Agents Chemother 52:2468–2472. https://doi.org/10.1128/aac.00156-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Won EJ, Joo M, Lee D, Kim M-N, Park Y-J, Kim SH, Shin M, Shin J (2020) Antifungal susceptibility tests and the cyp51 mutant strains among clinical Aspergillus fumigatus isolates from Korean multicenters. Mycobiology 48:148–152. https://doi.org/10.1080/12298093.2020.1744955

    Article  PubMed  PubMed Central  Google Scholar 

  62. Garcia-Rubio R, Alcazar-Fuoli L, Monteiro MC, Monzon S, Cuesta I, Pelaez T, Mellado E (2018) Insight into the significance of Aspergillus fumigatus cyp51A polymorphisms. antimicrob agents. Chemother 62:e00241–e00218. https://doi.org/10.1128/aac.00241-18

    Article  CAS  Google Scholar 

  63. Fan Y, Wang Y, Korfanty GA, Archer M, Xu J (2021) Genome-wide association analysis for triazole resistance in Aspergillus fumigatus. Pathogens. 10:701. https://doi.org/10.3390/pathogens10060701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Fan Y, Wang Y, Xu J (2020) Comparative genome sequence analyses of geographic samples of Aspergillus fumigatus-relevance for amphotericin B resistance. Microorganisms 8:1673. https://doi.org/10.3390/microorganisms8111673

    Article  CAS  PubMed Central  Google Scholar 

  65. Chang H, Ashu E, Sharma C, Kathuria S, Chowdhary A, Xu J (2016) Diversity and origins of Indian multi-triazole resistant strains of Aspergillus fumigatus. Mycoses. 59:450–466. https://doi.org/10.1111/myc.12494

    Article  CAS  PubMed  Google Scholar 

  66. Ashu EE, Xu J (2018) Strengthening the One Health agenda: the roles of molecular epidemiology in Aspergillus threat management. Genes. 9(7):E359. https://doi.org/10.3390/genes9070359

    Article  CAS  PubMed  Google Scholar 

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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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  1. State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, and Key Laboratory for Southwest Microbial Diversity of the Ministry of Education, Yunnan University, Kunming, 650032, Yunnan, People’s Republic of China

    Duanyong Zhou, Ruirui Wang, Xiao Li, Guangzhu Yang, Ke-Qin Zhang, Ying Zhang & Jianping Xu

  2. College of Life Science, Yunnan University, Kunming, 650032, Yunnan, People’s Republic of China

    Duanyong Zhou, Ruirui Wang, Xiao Li, Bin Peng & Guangzhu Yang

  3. School of Biology and Chemistry, Xingyi Normal University for Nationalities, Xingyi, 562400, Guizhou, People’s Republic of China

    Duanyong Zhou

  4. Department of Biology, McMaster University, Hamilton, Ontario, L8S 4K1, Canada

    Jianping Xu

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Contributions

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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Zhou, D., Wang, R., Li, X. et al. Genetic Diversity and Azole Resistance Among Natural Aspergillus fumigatus Populations in Yunnan, China. Microb Ecol 83, 869–885 (2022). https://doi.org/10.1007/s00248-021-01804-w

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  • DOI: https://doi.org/10.1007/s00248-021-01804-w

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