1887

Abstract

Environmental populations of the opportunistic pathogen have been shown to be genotypically diverse and to contain a range of isolates with varying pathogenic potential. In this study, we combined two RAPD primers to investigate the genetic diversity of environmental isolates from Manchester collected monthly over 1 year alongside Dublin environmental isolates and clinical isolates from patients. RAPD analysis revealed a diverse genotype, but with three major clinical isolate clusters. When the pathogenicity of clinical and Dublin isolates was compared with a random selection of Manchester isolates in a larvae model, as a group, clinical isolates were significantly more pathogenic than environmental isolates. Moreover, when relative pathogenicity of individual isolates was compared, clinical isolates were the most pathogenic, Dublin isolates were the least pathogenic and Manchester isolates showed a range in pathogenicity. Overall, this suggests that the environmental population is genetically diverse, displaying a range in pathogenicity, and that the most pathogenic strains from the environment are selected during patient infection.

Funding
This study was supported by the:
  • government of Saudi Arabia
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2014-04-01
2021-07-27
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References

  1. Abad A., Fernández-Molina J. V., Bikandi J., Ramírez A., Margareto J., Sendino J., Hernando F. L., Pontón J., Garaizar J., Rementeria A. ( 2010). What makes Aspergillus fumigatus a successful pathogen? Genes and molecules involved in invasive aspergillosis. Rev Iberoam Micol 27:155–182 [View Article][PubMed]
    [Google Scholar]
  2. Alp S., Arikan S. ( 2008). Investigation of extracellular elastase, acid proteinase and phospholipase activities as putative virulence factors in clinical isolates of Aspergillus species. J Basic Microbiol 48:331–337 [View Article][PubMed]
    [Google Scholar]
  3. Alshareef F., Robson G. D. ( 2014). Prevalence, persistence and phenotypic variation of Aspergillus fumigatus in the outdoor environment in Manchester (UK) over a two year period. Med Mycol
    [Google Scholar]
  4. Alvarez-Perez S., Blanco J. L., Alba P., Garcia M. E. ( 2010). Mating type and invasiveness are significantly associated in Aspergillus fumigatus. Med Mycol 48:273–277 [View Article][PubMed]
    [Google Scholar]
  5. Amich J., Krappmann S. ( 2012). Deciphering metabolic traits of the fungal pathogen Aspergillus fumigatus: redundancy vs. essentiality. Front Microbiol 3:414 [View Article][PubMed]
    [Google Scholar]
  6. Amich J., Schafferer L., Haas H., Krappmann S. ( 2013). Regulation of sulphur assimilation is essential for virulence and affects iron homeostasis of the human-pathogenic mould Aspergillus fumigatus. PLoS Pathog 9:e1003573 [View Article][PubMed]
    [Google Scholar]
  7. Anderson M. J., Gull K., Denning D. W. ( 1996). Molecular typing by random amplification of polymorphic DNA and M13 southern hybridization of related paired isolates of Aspergillus fumigatus. J Clin Microbiol 34:87–93[PubMed]
    [Google Scholar]
  8. Andrejko M., Mizerska-Dudka M., Jakubowicz T. ( 2009). Antibacterial activity in vivo and in vitro in the hemolymph of Galleria mellonella infected with Pseudomonas aeruginosa. Comp Biochem Physiol B Biochem Mol Biol 152:118–123 [View Article][PubMed]
    [Google Scholar]
  9. Araujo R., Amorim A., Gusmão L. ( 2010). Genetic diversity of Aspergillus fumigatus in indoor hospital environments. Med Mycol 48:832–838 [View Article][PubMed]
    [Google Scholar]
  10. Arné P., Thierry S., Wang D., Deville M., Le Loc’h G., Desoutter A., Féménia F., Nieguitsila A., Huang W. & other authors ( 2011). Aspergillus fumigatus in poultry. Int J Microbiol 2011:746356 [View Article][PubMed]
    [Google Scholar]
  11. Arvanitis M., Glavis-Bloom J., Mylonakis E. ( 2013). Invertebrate models of fungal infection. Biochim Biophys Acta 1832:1378–1383 [View Article][PubMed]
    [Google Scholar]
  12. Askew D. S. ( 2008). Aspergillus fumigatus: virulence genes in a street-smart mold. Curr Opin Microbiol 11:331–337 [View Article][PubMed]
    [Google Scholar]
  13. Aufauvre-Brown A., Cohen J., Holden D. W. ( 1992). Use of randomly amplified polymorphic DNA markers to distinguish isolates of Aspergillus fumigatus. J Clin Microbiol 30:2991–2993[PubMed]
    [Google Scholar]
  14. Aufauvre-Brown A., Brown J. S., Holden D. W. ( 1998). Comparison of virulence between clinical and environmental isolates of Aspergillus fumigatus. Eur J Clin Microbiol Infect Dis 17:778–780 [View Article][PubMed]
    [Google Scholar]
  15. Bain J. M., Tavanti A., Davidson A. D., Jacobsen M. D., Shaw D., Gow N. A. R., Odds F. C. ( 2007). Multilocus sequence typing of the pathogenic fungus Aspergillus fumigatus. J Clin Microbiol 45:1469–1477 [View Article][PubMed]
    [Google Scholar]
  16. Balajee S. A., de Valk H. A., Lasker B. A., Meis J. F., Klaassen C. H. ( 2008). Utility of a microsatellite assay for identifying clonally related outbreak isolates of Aspergillus fumigatus. J Microbiol Methods 73:252–256 [View Article][PubMed]
    [Google Scholar]
  17. Bart-Delabesse E., Humbert J.-F., Delabesse E., Bretagne S. ( 1998). Microsatellite markers for typing Aspergillus fumigatus isolates. J Clin Microbiol 36:2413–2418[PubMed]
    [Google Scholar]
  18. Bart-Delabesse E., Cordonnier C., Bretagne S. ( 1999). Usefulness of genotyping with microsatellite markers to investigate hospital-acquired invasive aspergillosis. J Hosp Infect 42:321–327 [View Article][PubMed]
    [Google Scholar]
  19. Ben-Ami R., Lamaris G. A., Lewis R. E., Kontoyiannis D. P. ( 2010). Interstrain variability in the virulence of Aspergillus fumigatus and Aspergillus terreus in a Toll-deficient Drosophila fly model of invasive aspergillosis. Med Mycol 48:310–317 [View Article][PubMed]
    [Google Scholar]
  20. Bikandi J., San Millán R., Rementeria A., Garaizar J. ( 2004). In silico analysis of complete bacterial genomes: PCR, AFLP-PCR and endonuclease restriction. Bioinformatics 20:798–799 [View Article][PubMed]
    [Google Scholar]
  21. Birch M., Denning D. W., Robson G. D. ( 2004). Comparison of extracellular phospholipase activities in clinical and environmental Aspergillus fumigatus isolates. Med Mycol 42:81–86 [View Article][PubMed]
    [Google Scholar]
  22. Blanco J. L., Hontecillas R., Bouza E., Blanco I., Pelaez T., Muñoz P., Perez Molina J., Garcia M. E. ( 2002). Correlation between the elastase activity index and invasiveness of clinical isolates of Aspergillus fumigatus. J Clin Microbiol 40:1811–1813 [View Article][PubMed]
    [Google Scholar]
  23. Brennan M., Thomas D. Y., Whiteway M., Kavanagh K. ( 2002). Correlation between virulence of Candida albicans mutants in mice and Galleria mellonella larvae. FEMS Immunol Med Microbiol 34:153–157 [View Article][PubMed]
    [Google Scholar]
  24. Browne N., Heelan M., Kavanagh K. ( 2013). An analysis of the structural and functional similarities of insect hemocytes and mammalian phagocytes. Virulence 4:597–603 [View Article][PubMed]
    [Google Scholar]
  25. Chamilos G., Lionakis M. S., Lewis R. E., Kontoyiannis D. P. ( 2007). Role of mini-host models in the study of medically important fungi. Lancet Infect Dis 7:42–55 [View Article][PubMed]
    [Google Scholar]
  26. Chamilos G., Bignell E. M., Schrettl M., Lewis R. E., Leventakos K., May G. S., Haas H., Kontoyiannis D. P. ( 2010). Exploring the concordance of Aspergillus fumigatus pathogenicity in mice and Toll-deficient flies. Med Mycol 48:506–510 [View Article][PubMed]
    [Google Scholar]
  27. Chazalet V., Debeaupuis J. P., Sarfati J., Lortholary J., Ribaud P., Shah P., Cornet M., Vu Thien H., Gluckman E. & other authors ( 1998). Molecular typing of environmental and patient isolates of Aspergillus fumigatus from various hospital settings. J Clin Microbiol 36:1494–1500[PubMed]
    [Google Scholar]
  28. Cimon B., Symoens F., Zouhair R., Chabasse D., Nolard N., Defontaine A., Bouchara J. P. ( 2001). Molecular epidemiology of airway colonisation by Aspergillus fumigatus in cystic fibrosis patients. J Med Microbiol 50:367–374[PubMed]
    [Google Scholar]
  29. Coleman J. J., Muhammed M., Kasperkovitz P. V., Vyas J. M., Mylonakis E. ( 2011). Fusarium pathogenesis investigated using Galleria mellonella as a heterologous host. Fungal Biol 115:1279–1289 [View Article][PubMed]
    [Google Scholar]
  30. Cook S. M., McArthur J. D. ( 2013). Developing Galleria mellonella as a model host for human pathogens. Virulence 4:350–353 [View Article][PubMed]
    [Google Scholar]
  31. Dagenais T. R., Keller N. P. ( 2009). Pathogenesis of Aspergillus fumigatus in invasive aspergillosis. Clin Microbiol Rev 22:447–465 [View Article][PubMed]
    [Google Scholar]
  32. de Valk H. A., Meis J. F., de Pauw B. E., Donnelly P. J., Klaassen C. H. ( 2007). Comparison of two highly discriminatory molecular fingerprinting assays for analysis of multiple Aspergillus fumigatus isolates from patients with invasive aspergillosis. J Clin Microbiol 45:1415–1419 [View Article][PubMed]
    [Google Scholar]
  33. de Valk H. A., Klaassen C. H., Yntema J. B., Hebestreit A., Seidler M., Haase G., Müller F. M., Meis J. F. ( 2009). Molecular typing and colonization patterns of Aspergillus fumigatus in patients with cystic fibrosis. J Cyst Fibros 8:110–114 [View Article][PubMed]
    [Google Scholar]
  34. Debeaupuis J. P., Sarfati J., Chazalet V., Latgé J. P. ( 1997). Genetic diversity among clinical and environmental isolates of Aspergillus fumigatus. Infect Immun 65:3080–3085[PubMed]
    [Google Scholar]
  35. Denning D. W., Clemons K. V., Hanson L. H., Stevens D. A. ( 1990). Restriction endonuclease analysis of total cellular DNA of Aspergillus fumigatus isolates of geographically and epidemiologically diverse origin. J Infect Dis 162:1151–1158 [View Article][PubMed]
    [Google Scholar]
  36. Desbois A. P., Coote P. J. ( 2012). Utility of greater wax moth larva (Galleria mellonella) for evaluating the toxicity and efficacy of new antimicrobial agents. Adv Appl Microbiol 78:25–53 [View Article][PubMed]
    [Google Scholar]
  37. Duarte-Escalante E., Zúñiga G., Ramírez O. N., Córdoba S., Refojo N., Arenas R., Delhaes L., Reyes-Montes M. R. ( 2009). Population structure and diversity of the pathogenic fungus Aspergillus fumigatus isolated from different sources and geographic origins. Mem Inst Oswaldo Cruz 104:427–433 [View Article][PubMed]
    [Google Scholar]
  38. Dunphy G. B., Morton D. B., Kropinski A., Chadwick J. M. ( 1986). Pathogenicity of lipopolysaccharide mutants of Pseudomonas aeruginosa for larvae of Galleria mellonella: bacterial properties associated with virulence. J Invertebr Pathol 47:48–55 [View Article]
    [Google Scholar]
  39. Dunphy G. B., Oberholzer U., Whiteway M., Zakarian R. J., Boomer I. ( 2003). Virulence of Candida albicans mutants toward larval Galleria mellonella (Insecta, Lepidoptera, Galleridae). Can J Microbiol 49:514–524 [View Article][PubMed]
    [Google Scholar]
  40. Evans B. A., Rozen D. E. ( 2012). A Streptococcus pneumoniae infection model in larvae of the wax moth Galleria mellonella. Eur J Clin Microbiol Infect Dis 31:2653–2660 [View Article][PubMed]
    [Google Scholar]
  41. Fallon J. P., Troy N., Kavanagh K. ( 2011). Pre-exposure of Galleria mellonella larvae to different doses of Aspergillus fumigatus conidia causes differential activation of cellular and humoral immune responses. Virulence 2:413–421 [View Article][PubMed]
    [Google Scholar]
  42. Fedorova N. D., Khaldi N., Joardar V. S., Maiti R., Amedeo P., Anderson M. J., Crabtree J., Silva J. C., Badger J. H. & other authors ( 2008). Genomic islands in the pathogenic filamentous fungus Aspergillus fumigatus. PLoS Genet 4:e1000046 [View Article][PubMed]
    [Google Scholar]
  43. Fuchs B. B., Mylonakis E. ( 2006). Using non-mammalian hosts to study fungal virulence and host defense. Curr Opin Microbiol 9:346–351 [View Article][PubMed]
    [Google Scholar]
  44. Fuchs B. B., Eby J., Nobile C. J., El Khoury J. B., Mitchell A. P., Mylonakis E. ( 2010). Role of filamentation in Galleria mellonella killing by Candida albicans. Microbes Infect 12:488–496 [View Article][PubMed]
    [Google Scholar]
  45. Guinea J., García de Viedma D., Peláez T., Escribano P., Muñoz P., Meis J. F., Klaassen C. H., Bouza E. ( 2011). Molecular epidemiology of Aspergillus fumigatus: an in-depth genotypic analysis of isolates involved in an outbreak of invasive aspergillosis. J Clin Microbiol 49:3498–3503 [View Article][PubMed]
    [Google Scholar]
  46. Harding C. R., Schroeder G. N., Reynolds S., Kosta A., Collins J. W., Mousnier A., Frankel G. ( 2012). Legionella pneumophila pathogenesis in the Galleria mellonella infection model. Infect Immun 80:2780–2790 [View Article][PubMed]
    [Google Scholar]
  47. Harrison F., Browning L. E., Vos M., Buckling A. ( 2006). Cooperation and virulence in acute Pseudomonas aeruginosa infections. BMC Biol 4:21 [View Article][PubMed]
    [Google Scholar]
  48. Hartmann T., Sasse C., Schedler A., Hasenberg M., Gunzer M., Krappmann S. ( 2011). Shaping the fungal adaptome – stress responses of Aspergillus fumigatus. Int J Med Microbiol 301:408–416 [View Article][PubMed]
    [Google Scholar]
  49. Ibrahim-Granet O., Philippe B., Boleti H., Boisvieux-Ulrich E., Grenet D., Stern M., Latgé J. P. ( 2003). Phagocytosis and intracellular fate of Aspergillus fumigatus conidia in alveolar macrophages. Infect Immun 71:891–903 [View Article][PubMed]
    [Google Scholar]
  50. Jackson J. C., Higgins L. A., Lin X. ( 2009). Conidiation color mutants of Aspergillus fumigatus are highly pathogenic to the heterologous insect host Galleria mellonella. PLoS ONE 4:e4224 [View Article][PubMed]
    [Google Scholar]
  51. Jander G., Rahme L. G., Ausubel F. M. ( 2000). Positive correlation between virulence of Pseudomonas aeruginosa mutants in mice and insects. J Bacteriol 182:3843–3845 [View Article][PubMed]
    [Google Scholar]
  52. Joyce S. A., Gahan C. G. ( 2010). Molecular pathogenesis of Listeria monocytogenes in the alternative model host Galleria mellonella. Microbiology 156:3456–3468 [View Article][PubMed]
    [Google Scholar]
  53. Kavanagh K., Reeves E. P. ( 2004). Exploiting the potential of insects for in vivo pathogenicity testing of microbial pathogens. FEMS Microbiol Rev 28:101–112 [View Article][PubMed]
    [Google Scholar]
  54. Kim S. S., Kim Y. H., Shin K. S. ( 2013). The developmental regulators, FlbB and FlbE, are involved in the virulence of Aspergillus fumigatus. J Microbiol Biotechnol 23:766–770 [View Article][PubMed]
    [Google Scholar]
  55. Krappmann S., Bignell E. M., Reichard U., Rogers T., Haynes K., Braus G. H. ( 2004). The Aspergillus fumigatus transcriptional activator CpcA contributes significantly to the virulence of this fungal pathogen. Mol Microbiol 52:785–799 [View Article][PubMed]
    [Google Scholar]
  56. Lair-Fulleringer S., Guillot J., Desterke C., Seguin D., Warin S., Bezille A., Chermette R., Bretagne S. ( 2003). Differentiation between isolates of Aspergillus fumigatus from breeding turkeys and their environment by genotyping with microsatellite markers. J Clin Microbiol 41:1798–1800 [View Article][PubMed]
    [Google Scholar]
  57. Latgé J. P. ( 1999). Aspergillus fumigatus and aspergillosis. Clin Microbiol Rev 12:310–350[PubMed]
    [Google Scholar]
  58. Lebreton F., Le Bras F., Reffuveille F., Ladjouzi R., Giard J. C., Leclercq R., Cattoir V. ( 2011). Galleria mellonella as a model for studying Enterococcus faecium host persistence. J Mol Microbiol Biotechnol 21:191–196 [View Article][PubMed]
    [Google Scholar]
  59. Leenders A. C., van Belkum A., Behrendt M., Luijendijk A., Verbrugh H. A. ( 1999). Density and molecular epidemiology of Aspergillus in air and relationship to outbreaks of Aspergillus infection. J Clin Microbiol 37:1752–1757[PubMed]
    [Google Scholar]
  60. Leuko S., Raivio T. L. ( 2012). Mutations that impact the enteropathogenic Escherichia coli Cpx envelope stress response attenuate virulence in Galleria mellonella. Infect Immun 80:3077–3085 [View Article][PubMed]
    [Google Scholar]
  61. Li H., Barker B. M., Grahl N., Puttikamonkul S., Bell J. D., Craven K. D., Cramer R. A. Jr ( 2011). The small GTPase RacA mediates intracellular reactive oxygen species production, polarized growth, and virulence in the human fungal pathogen Aspergillus fumigatus. Eukaryot Cell 10:174–186 [View Article][PubMed]
    [Google Scholar]
  62. Lin D., Lehmann P. F., Hamory B. H., Padhye A. A., Durry E., Pinner R. W., Lasker B. A. ( 1995). Comparison of three typing methods for clinical and environmental isolates of Aspergillus fumigatus. J Clin Microbiol 33:1596–1601[PubMed]
    [Google Scholar]
  63. Lionakis M. S., Lewis R. E., Torres H. A., Albert N. D., Raad I. I., Kontoyiannis D. P. ( 2005). Increased frequency of non-fumigatus Aspergillus species in amphotericin B- or triazole-pre-exposed cancer patients with positive cultures for aspergilli. Diagn Microbiol Infect Dis 52:15–20 [View Article][PubMed]
    [Google Scholar]
  64. Mak P., Zdybicka-Barabas A., Cytryńska M. ( 2010). A different repertoire of Galleria mellonella antimicrobial peptides in larvae challenged with bacteria and fungi. Dev Comp Immunol 34:1129–1136 [View Article][PubMed]
    [Google Scholar]
  65. Menotti J., Waller J., Meunier O., Letscher-Bru V., Herbrecht R., Candolfi E. ( 2005). Epidemiological study of invasive pulmonary aspergillosis in a haematology unit by molecular typing of environmental and patient isolates of Aspergillus fumigatus. J Hosp Infect 60:61–68 [View Article][PubMed]
    [Google Scholar]
  66. Mesa-Arango A. C., Forastiero A., Bernal-Martínez L., Cuenca-Estrella M., Mellado E., Zaragoza O. ( 2013). The non-mammalian host Galleria mellonella can be used to study the virulence of the fungal pathogen Candida tropicalis and the efficacy of antifungal drugs during infection by this pathogenic yeast. Med Mycol 51:461–472 [View Article][PubMed]
    [Google Scholar]
  67. Miyata S., Casey M., Frank D. W., Ausubel F. M., Drenkard E. ( 2003). Use of the Galleria mellonella caterpillar as a model host to study the role of the type III secretion system in Pseudomonas aeruginosa pathogenesis. Infect Immun 71:2404–2413 [View Article][PubMed]
    [Google Scholar]
  68. Mondon P., Thélu J., Lebeau B., Ambroise-Thomas P., Grillot R. ( 1995). Virulence of Aspergillus fumigatus strains investigated by random amplified polymorphic DNA analysis. J Med Microbiol 42:299–303 [View Article][PubMed]
    [Google Scholar]
  69. Mondon P., De Champs C., Donadille A., Ambroise-Thomas P., Grillot R. ( 1996). Variation in virulence of Aspergillus fumigatus strains in a murine model of invasive pulmonary aspergillosis. J Med Microbiol 45:186–191 [View Article][PubMed]
    [Google Scholar]
  70. Mondon P., Brenier M. P., Symoens F., Rodriguez E., Coursange E., Chaib F., Lebeau B., Piens M. A., Tortorano A. M. & other authors ( 1997). Molecular typing of Aspergillus fumigatus strains by sequence-specific DNA primer (SSDP) analysis. FEMS Immunol Med Microbiol 17:95–102 [View Article][PubMed]
    [Google Scholar]
  71. Mukherjee K., Altincicek B., Hain T., Domann E., Vilcinskas A., Chakraborty T. ( 2010). Galleria mellonella as a model system for studying Listeria pathogenesis. Appl Environ Microbiol 76:310–317 [View Article][PubMed]
    [Google Scholar]
  72. Mylonakis E., Moreno R., El Khoury J. B., Idnurm A., Heitman J., Calderwood S. B., Ausubel F. M., Diener A. ( 2005). Galleria mellonella as a model system to study Cryptococcus neoformans pathogenesis. Infect Immun 73:3842–3850 [View Article][PubMed]
    [Google Scholar]
  73. O’Gorman C. M. ( 2011). Airborne Aspergillus fumigatus conidia: a risk factor for aspergillosis. Fungal Biol Rev 25:151–157 [View Article]
    [Google Scholar]
  74. O’Gorman C. M., Fuller H., Dyer P. S. ( 2009). Discovery of a sexual cycle in the opportunistic fungal pathogen Aspergillus fumigatus. Nature 457:471–474 [View Article][PubMed]
    [Google Scholar]
  75. O’Hanlon K. A., Cairns T., Stack D., Schrettl M., Bignell E. M., Kavanagh K., Miggin S. M., O’Keeffe G., Larsen T. O., Doyle S. ( 2011). Targeted disruption of nonribosomal peptide synthetase pes3 augments the virulence of Aspergillus fumigatus. Infect Immun 79:3978–3992 [View Article][PubMed]
    [Google Scholar]
  76. Olias P., Gruber A. D., Hafez H. M., Lierz M., Slesiona S., Brock M., Jacobsen I. D. ( 2011). Molecular epidemiology and virulence assessment of Aspergillus fumigatus isolates from white stork chicks and their environment. Vet Microbiol 148:348–355 [View Article][PubMed]
    [Google Scholar]
  77. Papaioannou E., Utari P. D., Quax W. J. ( 2013). Choosing an appropriate infection model to study quorum sensing inhibition in Pseudomonas infections. Int J Mol Sci 14:19309–19340 [View Article][PubMed]
    [Google Scholar]
  78. Peleg A. Y., Jara S., Monga D., Eliopoulos G. M., Moellering R. C. Jr, Mylonakis E. ( 2009). Galleria mellonella as a model system to study Acinetobacter baumannii pathogenesis and therapeutics. Antimicrob Agents Chemother 53:2605–2609 [View Article][PubMed]
    [Google Scholar]
  79. Philippe B., Ibrahim-Granet O., Prévost M. C., Gougerot-Pocidalo M. A., Sanchez Perez M., Van der Meeren A., Latgé J. P. ( 2003). Killing of Aspergillus fumigatus by alveolar macrophages is mediated by reactive oxidant intermediates. Infect Immun 71:3034–3042 [View Article][PubMed]
    [Google Scholar]
  80. Reeves E. P., Messina C. G., Doyle S., Kavanagh K. ( 2004). Correlation between gliotoxin production and virulence of Aspergillus fumigatus in Galleria mellonella. Mycopathologia 158:73–79 [View Article][PubMed]
    [Google Scholar]
  81. Rementeria A., López-Molina N., Ludwig A., Vivanco A. B., Bikandi J., Pontón J., Garaizar J. ( 2005). Genes and molecules involved in Aspergillus fumigatus virulence. Rev Iberoam Micol 22:1–23 [View Article][PubMed]
    [Google Scholar]
  82. Rhodes J. C. ( 2006). Aspergillus fumigatus: growth and virulence. Med Mycol 44:Suppl. 177–81 [View Article][PubMed]
    [Google Scholar]
  83. Richie D. L., Hartl L., Aimanianda V., Winters M. S., Fuller K. K., Miley M. D., White S., McCarthy J. W., Latgé J. P. & other authors ( 2009). A role for the unfolded protein response (UPR) in virulence and antifungal susceptibility in Aspergillus fumigatus. PLoS Pathog 5:e1000258 [View Article][PubMed]
    [Google Scholar]
  84. Rinyu E., Varga J., Ferenczy L. ( 1995). Phenotypic and genotypic analysis of variability in Aspergillus fumigatus. J Clin Microbiol 33:2567–2575[PubMed]
    [Google Scholar]
  85. Rodriguez E., De Meeüs T., Mallie M., Renaud F., Symoens F., Mondon P., Piens M. A., Lebeau B., Viviani M. A. & other authors ( 1996). Multicentric epidemiological study of Aspergillus fumigatus isolates by multilocus enzyme electrophoresis. J Clin Microbiol 34:2559–2568[PubMed]
    [Google Scholar]
  86. Sales-Campos H., Tonani L., Cardoso C. R., Kress M. R. ( 2013). The immune interplay between the host and the pathogen in Aspergillus fumigatus lung infection. Biomed Res Int 2013:693023 [View Article][PubMed]
    [Google Scholar]
  87. Schrettl M., Haas H. ( 2011). Iron homeostasis – Achilles’ heel of Aspergillus fumigatus. Curr Opin Microbiol 14:400–405 [View Article][PubMed]
    [Google Scholar]
  88. Scully L. R., Bidochka M. J. ( 2009). An alternative insect pathogenic strategy in an Aspergillus flavus auxotroph. Mycol Res 113:230–239 [View Article][PubMed]
    [Google Scholar]
  89. Slater J. L., Gregson L., Denning D. W., Warn P. A. ( 2011). Pathogenicity of Aspergillus fumigatus mutants assessed in Galleria mellonella matches that in mice. Med Mycol 49:Suppl. 1S107–S113 [View Article][PubMed]
    [Google Scholar]
  90. Soukup A. A., Farnoodian M., Berthier E., Keller N. P. ( 2012). NosA, a transcription factor important in Aspergillus fumigatus stress and developmental response, rescues the germination defect of a laeA deletion. Fungal Genet Biol 49:857–865 [View Article][PubMed]
    [Google Scholar]
  91. Spreadbury C. L., Bainbridge B. W., Cohen J. ( 1990). Restriction fragment length polymorphisms in isolates of Aspergillus fumigatus probed with part of the intergenic spacer region from the ribosomal RNA gene complex of Aspergillus nidulans. J Gen Microbiol 136:1991–1994 [View Article][PubMed]
    [Google Scholar]
  92. Tang C. M., Cohen J., Rees A. J., Holden D. W. ( 1994). Molecular epidemiological study of invasive pulmonary aspergillosis in a renal transplantation unit. Eur J Clin Microbiol Infect Dis 13:318–321 [View Article][PubMed]
    [Google Scholar]
  93. Thomas R. J., Hamblin K. A., Armstrong S. J., Müller C. M., Bokori-Brown M., Goldman S., Atkins H. S., Titball R. W. ( 2013). Galleria mellonella as a model system to test the pharmacokinetics and efficacy of antibiotics against Burkholderia pseudomallei. Int J Antimicrob Agents 41:330–336 [View Article][PubMed]
    [Google Scholar]
  94. Vanhee L. M., Nelis H. J., Coenye T. ( 2009). Rapid detection and quantification of Aspergillus fumigatus in environmental air samples using solid-phase cytometry. Environ Sci Technol 43:3233–3239 [View Article][PubMed]
    [Google Scholar]
  95. Vanhee L. M., Nelis H. J., Coenye T. ( 2010). What can be learned from genotyping of fungi?. Med Mycol 48:Suppl. 1S60–S69 [View Article][PubMed]
    [Google Scholar]
  96. Vos P., Hogers R., Bleeker M., Reijans M., van de Lee T., Hornes M., Frijters A., Pot J., Peleman J. & other authors ( 1995). AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414 [View Article][PubMed]
    [Google Scholar]
  97. Wand M. E., Müller C. M., Titball R. W., Michell S. L. ( 2011). Macrophage and Galleria mellonella infection models reflect the virulence of naturally occurring isolates of B. pseudomallei, B. thailandensis and B. oklahomensis. BMC Microbiol 11:11 [View Article][PubMed]
    [Google Scholar]
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