Characterization of experimental complex fungal bioaerosols: Impact of analytical method on fungal composition measurements

References

• Amann, R., W. Ludwig, and K. Schleifer. 1995. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol. Rev. 59 (1):143–69.
   PubMedGoogle Scholar
• Bellemain, E. T., T. Carlsen, C. Brochmann, E. Coissac, P. Taberlet, and H. Kauserud. 2010. ITS as an environmental DNA barcode for fungi: An in silico approach reveals potential PCR biases. BMC Microbiol. 10 (1):189–98. doi: 10.1186/1471-2180-10-189.
   PubMed Web of Science ®Google Scholar
• Braun, U., P. W. Crous, F. Dugan, J. Z. Groenewald, and G. Sybren De Hoog. 2003. Phylogeny and taxonomy of cladosporium-like hyphomycetes, including davidiella gen. nov., the teleomorph of cladosporium s. str. Mycol. Progr. 2 (1):3–18. doi: 10.1007/s11557-006-0039-2.
   Google Scholar
• Bru-Adan, V., N. Wéry, M. Moletta-Denat, P. Boiron, J.-P. Delgènes, and J.-J. Godon. 2009. Diversity of bacteria and fungi in aerosols during screening in a green waste composting plant. Curr. Microbiol. 59 (3):326–35. doi: 10.1007/s00284-009-9438-3.
   PubMed Web of Science ®Google Scholar
• Burton, N. C., S. A. Grinshpun, and T. Reponen. 2007. Physical collection efficiency of filter materials for bacteria and viruses. Ann. Occup. Hyg. 51 (2):143–51. doi: 10.1093/annhyg/mel073.
   PubMed Web of Science ®Google Scholar
• Caporaso, J. G., J. Kuczynski, J. Stombaugh, K. Bittinger, F. D. Bushman, E. K. Costello, N. Fierer, A. G. Peña, J. K. Goodrich, J. I. Gordon, et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat. Meth. 7 (5):335–36. doi: 10.1038/nmeth.f.303.
   PubMed Web of Science ®Google Scholar
• Coronado, J. M., J. Soria, J. C. Conesa, R. Bellod, C. Adán, H. Yamaoka, V. Loddo, and V. Augugliaro. 2005. Photocatalytic inactivation of Legionella pneumophila and an aerobic bacteria consortium in water over TiO2/SiO2 fibres in a continuous reactor. Top. Catal. 35 (3–4):279–86. doi: 10.1007/s11244-005-3835-z.
   Web of Science ®Google Scholar
• Dannemiller, K. C., D. Reeves, K. Bibby, N. Yamamoto, and J. Peccia. 2014. Fungal high-throughput taxonomic identification tool for use with next-generation sequencing (FHiTINGS). J. Basic Microbiol. 54 (4):315–21. doi: 10.1002/jobm.201200507.
   PubMed Web of Science ®Google Scholar
• Dannemiller, K. C., N. Lang-Yona, N. Yamamoto, Y. Rudich, and J. Peccia. 2014. Combining real-time PCR and next-generation DNA sequencing to provide quantitative comparisons of fungal aerosol populations. Atmos. Environ. 84:113–21. doi: 10.1016/j.atmosenv.2013.11.036.
   Web of Science ®Google Scholar
• Degois, J., F. Clerc, X. Simon, C. Bontemps, P. Leblond, and P. Duquenne. 2017. First metagenomic survey of the microbial diversity in bioaerosols emitted in waste sorting plants. Ann. Work Expos. Health 61 (9):1076–86. doi: 10.1093/annweh/wxx075.
   PubMed Web of Science ®Google Scholar
• Desneux, J., and A. M. Pourcher. 2014. Comparison of DNA extraction kits and modification of DNA elution procedure for the quantitation of subdominant bacteria from piggery effluents with real-time PCR. Microbiol. Open 3 (4):437–45. doi: 10.1002/mbo3.178.
   Web of Science ®Google Scholar
• Ding, W., L. Li, Y. Han, J. Liu, and J. Liu. 2016. Site-related and seasonal variation of bioaerosol emission in an indoor wastewater treatment station: Level, characteristics of particle size, and microbial structure. Aerobiologia 32 (2):211–24. doi: 10.1007/s10453-015-9391-5.
   Web of Science ®Google Scholar
• Douwes, J., P. Thorne, N. Pearce, and D. Heederik. 2003. Bioaerosol health effects and exposure assessment: Progress and prospects. Ann. Occup. Hyg. 47 (3):187–200. doi: 10.1093/annhyg/meg032.
   PubMed Web of Science ®Google Scholar
• Duquenne, P. 2018. On the identification of culturable microorganisms for the assessment of biodiversity in bioaerosols. Ann. Work Expos. Health 62 (2):139–46. doi: 10.1093/annweh/wxx096.
   PubMed Web of Science ®Google Scholar
• Duquenne, P., G. Marchand, and C. Duchaine. 2013. Measurement of endotoxins in bioaerosols at workplace: A critical review of literature and a standardization issue. Ann. Occup. Hyg. 57 (2):137–72. doi: 10.1093/annhyg/mes051.
   PubMedGoogle Scholar
• Duquenne, P., X. Simon, V. Koehler, S. Goncalves-Machado, G. Greff, T. Nicot, and P. Poirot. 2012. Documentation of bioaerosol concentrations in an indoor composting facility in France. J. Environ. Monit. 14 (2):409–19. doi: 10.1039/c2em10714g.
   PubMedGoogle Scholar
• Dyląg, M. 2017. Fungi present in home and their impact on human health - A short review. Insights Biol. Med. 1:16–25.
   Google Scholar
• Edgar, R. C., B. J. Haas, J. C. Clemente, C. Quince, and R. Knight. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27 (16):2194–200. doi: 10.1093/bioinformatics/btr381.
   PubMed Web of Science ®Google Scholar
• Fahlgren, C., G. Bratbak, R.-A. Sandaa, R. Thyrhaug and U. L. Zweifel. 2010. Diversity of airborne bacteria in samples collected using different devices for aerosol collection. Aerobiologia 27 (2):107–20. doi: 10.1007/s10453-010-9181-z.
   Web of Science ®Google Scholar
• Feinstein, L. M., W. J. Sul, and C. B. Blackwood. 2009. Assessment of bias associated with incomplete extraction of microbial DNA from soil. Appl. Environ. Microbiol. 75 (16):5428–33. doi: 10.1128/AEM.00120-09.
   PubMed Web of Science ®Google Scholar
• Flannigan, B. 1997. Air sampling for fungi in indoor environments. J. Aerosol Sci. 28 (3):381–92. doi: 10.1016/S0021-8502(96)00441-7.
   Web of Science ®Google Scholar
• Forthomme, A., Y. Andres, A. Joubert, X. Simon, P. Duquenne, D. Bemer, and F. Le Coq. 2013. Evolution of microbial aerosol behaviour in heating, ventilating and air-conditioning systems – Quantification of Staphylococcus epidermidis and penicillium oxalicum viability. Environ. Technol. 34 (8):993–97. doi: 10.1080/09593330.2012.728731.
   PubMed Web of Science ®Google Scholar
• Fredricks, D. N., C. Smith, and A. Meier. 2005. Comparison of six DNA extraction methods for recovery of fungal DNA as assessed by quantitative PCR. J. Clin. Microbiol. 43 (10):5122–28. doi: 10.1128/JCM.43.10.5122-5128.2005.
   PubMed Web of Science ®Google Scholar
• Fung, F., and W. G. Hughson. 2003. Health effects of indoor fungal bioaerosol exposure. Appl. Occup. Environ. Hygiene 18 (7):535–44. doi: 10.1080/10473220301451.
   PubMedGoogle Scholar
• Guo, H., Z. Yu, and H. Zhang. 2015. Phylogenetic diversity of microbial communities associated with coalbed methane gas from Eastern ordos basin, China. Int. J. Coal Geol. 150–151:120–6. doi: 10.1016/j.coal.2015.08.012.
   Web of Science ®Google Scholar
• Haig, C. W., W. G. Mackay, J. T. Walker, and C. Williams. 2016. Bioaerosol sampling: Sampling mechanisms, bioefficiency and field studies. J. Hosp. Infect. 93 (3):242–55. doi: 10.1016/j.jhin.2016.03.017.
   PubMed Web of Science ®Google Scholar
• Haugland, R. A., J. L. Heckman and L. J. Wymer. 1999. Evaluation of different methods for the extraction of DNA from fungal conidia by quantitative competitive PCR analysis. Journal of Microbiological Methods 37 (2):165–76. doi: 10.1016/S0167-7012(99)00061-5.
   PubMed Web of Science ®Google Scholar
• Haugland, R. A., N. Brinkman, and S. J. Vesper. 2002. Evaluation of rapid DNA extraction methods for the quantitative detection of fungi using real-time PCR analysis. J. Microbiol. Meth. 50 (3):319–23. doi: 10.1016/S0167-7012(02)00037-4.
   PubMed Web of Science ®Google Scholar
• Heidelberg, J. F., M. Shahamat, M. Levin, I. Rahman, G. Stelma, C. Grim, and R. R. Colwell. 1997. Effect of aerosolization on culturability and viability of gram-negative bacteria. Appl. Environ. Microbiol. 63:3585–88.
   PubMed Web of Science ®Google Scholar
• Hoisington, A. J., J. P. Maestre, M. D. King, J. A. Siegel, and K. A. Kinney. 2014. Impact of sampler selection on the characterization of the indoor microbiome via high-throughput sequencing. Build. Environ. 80:274–82. doi: 10.1016/j.buildenv.2014.04.021.
   Web of Science ®Google Scholar
• Hongxia, X. W., T. Reponen, A. Adhikari, K. Willeke, and S. A. Grinshpun. 2004. Effect of fluid type and microbial properties on the aerosolization of microorganisms from metalworking fluids. Aerosol Sci. Technol. 38 (12):1139–48. doi: 10.1080/027868290891488.
   Web of Science ®Google Scholar
• Hospodsky, D., N. Yamamoto, and J. Peccia. 2010. Accuracy, precision, and method detection limits of quantitative PCR for airborne bacteria and fungi. Appl. Environ. Microbiol. 76 (21):7004–12. doi: 10.1128/AEM.01240-10.
   PubMed Web of Science ®Google Scholar
• Jankowska, E., T. Reponen, K. Willeke, S. A. Grinshpun, and K. J. Choi. 2000. Collection of fungal spores on air filters and spore reentrainment from filters into air. J. Aerosol Sci. 31 (8):969–78. doi: 10.1016/S0021-8502(00)00017-3.
   Web of Science ®Google Scholar
• Jung, J. H., C. H. Lee, J. E. Lee, J. H. Lee, S. S. Kim, and B. U. Lee. 2009. Design and characterization of a fungal bioaerosol generator using multi-orifice air jets and a rotating substrate. J. Aerosol Sci. 40 (1):72–80. doi: 10.1016/j.jaerosci.2008.09.002.
   Web of Science ®Google Scholar
• Kanaani, H., M. Hargreaves, J. Smith, Z. Ristovski, V. Agranovski, and L. Morawska. 2008. Performances of UVAPS with respect to detection of airborne fungi. J. Aerosol Sci. 39 (2):175–89. doi: 10.1016/j.jaerosci.2007.10.007.
   Web of Science ®Google Scholar
• Karakousis, A., L. Tan, D. Ellis, H. Alexiou, and P. J. Wormald. 2006. An assessment of the efficiency of fungal DNA extraction methods for maximizing the detection of medically important fungi using PCR. J. Microbiol. Meth. 65 (1):38–48. doi: 10.1016/j.mimet.2005.06.008.
   PubMed Web of Science ®Google Scholar
• Kristiansen, A., A. M. Saunders, A. A. Hansen, P. H. Nielsen, and J. L. Nielsen. 2012. Community structure of bacteria and fungi in aerosols of a pig confinement building. FEMS Microbiol. Ecol. 80 (2):390–401. doi: 10.1111/j.1574-6941.2012.01305.x.
   PubMed Web of Science ®Google Scholar
• Kumari, P., and H. Choi. 2015. Manure removal system influences the abundance and composition of airborne biotic contaminants in swine confinement buildings. Environ. Monit. Assess. 187 (8):1–10. doi: 10.1007/s10661-015-4759-0.
   PubMed Web of Science ®Google Scholar
• Lagier, J., F. Armougom, M. Million, P. Hugon, I. Pagnier, C. Robert, F. Bittar, G. Fournous, G. Gimenez, M. Maraninchi, et al. 2012. Microbial culturomics: Paradigm shift in the human gut microbiome study. Clin. Microbiol. Infect. 18 (12):1185–93. doi: 10.1111/1469-0691.12023.
   PubMed Web of Science ®Google Scholar
• Lagier, J. C., P. Hugon, S. Khelaifia, P. E. Fournier, B. La Scola, and D. Raoult. 2015. The rebirth of culture in microbiology through the example of culturomics to study human gut microbiota. Clin. Microbiol. Rev. 28 (1):237–64. doi: 10.1128/CMR.00014-14.
   PubMed Web of Science ®Google Scholar
• Lagier, J. C., S. Khelaifia, M. T. Alou, S. Ndongo, and N. Dione. 2016. Culture of previously uncultured members of the human gut microbiota by culturomics. Nat. Microbiol. 1: article 16203.
   PubMed Web of Science ®Google Scholar
• Lee, B. U., S. H. Kim, and S. S. Kim. 2002. Hygroscopic growth of E. coli and B. subtilis bioaerosols. J. Aerosol Sci. 33 (12):1721–23. doi: 10.1016/S0021-8502(02)00114-3.
   Web of Science ®Google Scholar
• Liebich, J., M. Schloter, A. Schäffer, H. Vereecken, and P. Burauel. 2007. Degradation and humification of maize straw in soil microcosms inoculated with simple and complex microbial communities. Eur. J. Soil Sci. 58 (1):141–51. doi: 10.1111/j.1365-2389.2006.00816.x.
   Web of Science ®Google Scholar
• Madsen, A. M., S. T. Larsen, I. K. Koponen, K. I. Kling, A. Barooni, D. G. Karottki, K. Tendal, and P. Wolkoff. 2016. Generation and characterization of indoor fungal aerosols for inhalation studies. Appl. Environ. Microbiol. 82 (8):2479–93. doi: 10.1128/AEM.04063-15.
   PubMed Web of Science ®Google Scholar
• Manian, S., S. Sreenivasaprasad, and P. R. Mills. 2001. DNA extraction method for PCR in mycorrhizal fungi. Lett. Appl. Microbiol. 33 (4):307–10. doi: 10.1046/j.1472-765X.2001.01001.x.
   PubMed Web of Science ®Google Scholar
• Mbareche, H., E. Brisebois, M. Veillette, and C. Duchaine. 2017. Bioaerosol sampling and detection methods based on molecular approaches: No pain no gain. Sci. Total Environ. 599:2095–104. doi: 10.1016/j.scitotenv.2017.05.076.
   PubMed Web of Science ®Google Scholar
• Morgan, J. L., A. E. Darling, and J. A. Eisen. 2010. Metagenomic sequencing of an in vitro-simulated microbial community. PLoS One. 5 (4):e10209. doi: 10.1371/journal.pone.0010209.
   PubMed Web of Science ®Google Scholar
• Nieguitsila, A., M. Deville, T. Jamal, L. Halos, M. Berthelemy, R. Chermette, S. Latouche, P. Arné, and J. Guillot. 2007. Evaluation of fungal aerosols using temporal temperature gradient electrophoresis (TTGE) and comparison with culture. J. Microbiol. Meth. 70 (1):86–95. doi: 10.1016/j.mimet.2007.03.021.
   PubMed Web of Science ®Google Scholar
• Nilsson, R. H., M. Ryberg, K. Abarenkov, E. Sjökvist, and E. Kristiansson. 2009. The ITS region as a target for characterization of fungal communities using emerging sequencing technologies. FEMS Microbiol. Lett. 296 (1):97–101. doi: 10.1111/j.1574-6968.2009.01618.x.
   PubMed Web of Science ®Google Scholar
• Ovaskainen, O.,. J. Nokso-Koivisto, J. Hottola, T. Rajala, T. Pennanen, H. Ali-Kovero, O. Miettinen, P. Oinonen, P. Auvinen, L. Paulin, K.-H. Larsson, and R. Mäkipää. 2010. Identifying wood-inhabiting fungi with 454 sequencing – What is the probability that BLAST gives the correct species?. Fungal Ecol. 3 (4):274–83. doi: 10.1016/j.funeco.2010.01.001.
   Web of Science ®Google Scholar
• Perrott, P.,. N. Turgeon, L. Gauthier-Levesque, and C. Duchaine. 2017. Preferential aerosolization of bacteria in bioaerosols generated in vitro. J. Appl. Microbiol. 123 (3):688–97. doi: 10.1111/jam.13514.
   PubMed Web of Science ®Google Scholar
• Raper, K. B., and D. I. Fennell. 1965. The genus aspergillus. Baltimore, MA: Williams & Wilkins Company, 686 p.
   Google Scholar
• Reponen, T. 2011. Methodologies for assessing bioaerosol exposures. In Encyclopedia of environmental health, ed. E.-I.-C. J. O. Nriagu, 722–30. Burlington: Elsevier.
   Google Scholar
• Reponen, T., K. Willeke, S. Grinshpun, and A. Nevalainen. 2011. Biological particle sampling. In Aerosols measurement – Principles, techniques and applications, 3rd ed., ed. P. Kulkani, P. A. Baron, and K. Willeke, 549–70. New York, NY: A John Willey & Sons, Inc.
   Google Scholar
• Reponen, T., K. Willeke, V. Ulevicius, A. Reponen, and S. A. Grinshpun. 1996. Effect of relative humidity on the aerodynamic diameter and respiratory deposition of fungal spores. Atmos. Environ. 30 (23):3967–74. doi: 10.1016/1352-2310(96)00128-8.
   Web of Science ®Google Scholar
• Samson, R. A., E. Hoekstra, J. C. Friswald, and O. Filtenborg. 1995. Introduction to foodborne fungi, 3rd ed. Baarn, Delft: Centraalbureau voor Schimmelcultures, The Netherlands.
   Google Scholar
• Schäfer, J., S. Weiß, and U. Jäckel. 2017. Preliminary validation of a method combining cultivation and cloning-based approaches to monitor airborne bacteria. Ann. Work Expos. Health 61 (6):633–42. doi: 10.1093/annweh/wxx038.
   PubMed Web of Science ®Google Scholar
• Scheermeyer, E., and I. E. Agranovski. 2009. Design and evaluation of a new device for fungal spore aerosolization for laboratory applications. J. Aerosol Sci. 40 (10):879–89. doi: 10.1016/j.jaerosci.2009.06.003.
   Web of Science ®Google Scholar
• Schloss, P. D., S. L. Westcott, T. Ryabin, J. R. Hall, M. Hartmann, E. B. Hollister, R. A. Lesniewski, B. B. Oakley, D. H. Parks, C. J. Robinson, et al. 2009. Introducing mothur: Open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75 (23):7537–41. doi: 10.1128/AEM.01541-09.
   PubMed Web of Science ®Google Scholar
• Shogren, E. S., and J. H. Park. 2011. Pre-sampling contamination of filters used in measurements of airborne (1,3)-beta-d-glucan based on glucan-specific limulus amebocyte lysate assay. J. Environ. Monit. 13 (4):1082–87. doi: 10.1039/c0em00495b.
   PubMedGoogle Scholar
• Simon, X., and P. Duquenne. 2013. Feasibility of generating peaks of bioaerosols for laboratory experiments. Aerosol Air Qual. Res. 13 (3):877–86. doi: 10.4209/aaqr.2012.12.0340.
   Web of Science ®Google Scholar
• Simon, X., P. Duquenne, V. Koehler, C. Piernot, C. Coulais, and M. Faure. 2011. Aerosolisation of Escherichia coli and associated endotoxin using an improved bubbling bioaerosol generator. J. Aerosol Sci. 42 (8):517–31. doi: 10.1016/j.jaerosci.2011.05.002.
   Web of Science ®Google Scholar
• Tolvanen, O. K. 2001. Airborne bio-aerosols and noise in a dry waste treatment plant in pietarsaari, Finland. Waste Manag. Res. 19 (2):108–14. doi: 10.1177/0734242X0101900203.
   PubMed Web of Science ®Google Scholar
• Vishnivetskaya, T. A., A. C. Layton, M. C. Y. Lau, A. Chauhan, K. R. Cheng, A. J. Meyers, J. R. Murphy, A. W. Rogers, G. S. Saarunya, D. E. Williams, et al. 2014. Commercial DNA extraction kits impact observed microbial community composition in permafrost samples. FEMS Microbiol. Ecol. 87 (1):217–30. doi: 10.1111/1574-6941.12219.
   PubMed Web of Science ®Google Scholar
• Wang, C.-H., B. T. Chen, B.-C. Han, A. C.-Y. Liu, P.-C. Hung, C.-Y. Chen, and H. J. Chao. 2015. Field evaluation of personal sampling methods for multiple bioaerosols. PLoS ONE. 10 (3):e0120308. doi: 10.1371/journal.pone.0120308.
   PubMed Web of Science ®Google Scholar
• Wang, Q., G. M. Garrity, J. M. Tiedje, and J. R. Cole. 2007. Naïve bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73 (16):5261–67. doi: 10.1128/AEM.00062-07.
   PubMed Web of Science ®Google Scholar
• White, P. L., M. D. Perry, J. Loeffler, W. Melchers, L. Klingspor, S. Bretagne, E. McCulloch, M. Cuenca-Estrella, N. Finnstrom, J. P. Donnelly, and R. A. Barnes. 2010. Critical stages of extracting DNA from Aspergillus fumigatus in whole-blood specimens. J. Clin. Microbiol. 48 (10):3753–55. doi: 10.1128/JCM.01466-10.
   PubMed Web of Science ®Google Scholar
• Yamamoto, N., K. C. Dannemiller, K. Bibby, and J. Peccia. 2014. Identification accuracy and diversity reproducibility associated with internal transcribed spacer-based fungal taxonomic library preparation. Environ. Microbiol. 16 (9):2764–76. doi: 10.1111/1462-2920.12338.
   PubMed Web of Science ®Google Scholar
• Yoo, K., T. K. Lee, E. J. Choi, J. Yang, S. K. Shukla, S-I Hwang, and J. Park. 2017. Molecular approaches for the detection and monitoring of microbial communities in bioaerosols: A review. J. Environ. Sci. 51:234–47. doi: 10.1016/j.jes.2016.07.002.
   Web of Science ®Google Scholar
• Zalar, P., G. Sybren de Hoog, H. J. Schroers, J. M. Frank, and N. Gunde-Cimerman. 2005. Taxonomy and phylogeny of the xerophilic genus wallemia (Wallemiomycetes and wallemiales, cl. et ord. nov.). Antonie Van Leeuwenhoek. 87 (4):311–28. doi: 10.1007/s10482-004-6783-x.
   PubMed Web of Science ®Google Scholar
• Zeng, Q. Y., S. O. Westermark, Å. Rasmuson-Lestander, And, and X. R. Wang. 2004. Detection and quantification of wallemia sebi in aerosols by real-time PCR, conventional PCR, and cultivation. Appl. Environ. Microbiol. 70 (12):7295–302. doi: 10.1128/AEM.70.12.7295-7302.2004.
   PubMed Web of Science ®Google Scholar