Abstract
Purpose of Review
The evolution of molecular-based methods over the last two decades has provided new approaches to identify and characterize fungal communities or “mycobiomes” at resolutions previously not possible using traditional hazard identification methods. The recent focus on fungal community assemblages within indoor environments has provided renewed insight into overlooked sources of fungal exposure. In occupational studies, internal transcribed spacer (ITS) region sequencing has recently been utilized in a variety of environments ranging from indoor office buildings to agricultural commodity and harvesting operations.
Recent Findings
Fungal communities identified in occupational environments have been primarily placed in the phylum Ascomycota and included classes typically identified using traditional fungal exposure methods such as the Eurotiomycetes, Dothideomycetes, Sordariomycetes, and Saccharomycetes. The phylum Basidiomycota has also been reported to be more prevalent than previously estimated and ITS region sequences have been primarily derived from the classes Agaricomycetes and Ustilaginomycetes. These studies have also resolved sequences placed in the Basidiomycota classes Tremellomycetes and Exobasidiomycetes that include environmental and endogenous yeast species.
Summary
These collective datasets have shown that occupational fungal exposures include a much broader diversity of fungi than once thought. Although the clinical implications for occupational allergy are an emerging field of research, establishing the mycobiome in occupational environments will be critical for future studies to determine the complete spectrum of worker exposures to fungal bioaerosols and their impact on worker health.
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References
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• Eduard W, Heederik D, Duchaine C, Green BJ. Bioaerosol exposure assessment in the workplace: the past, present and recent advances. J Environ Monit. 2012;14(2):334-339. Doi:https://doi.org/10.1039/c2em10717a . COMMENT: Brief overview of bioaerosol sources in occupational environments.
Green BJ, Schmechel D, Summerbell RC. Aerosolized fungal fragments. In: Adan OCG, R.A. S, editors. Fundamentals of mold growth in indoor environments and strategies for healthy living. Wageningen Wageningen Academic Publishers; 2011. p. 211–43.
Clark N, Ammann H, Brunekreef B, Eggleston P, Fisk W, Fullilove R et al. Damp indoor spaces and health. Washington, DC: The National Academies Press; 2004.
Heseltine E, Rosen J. WHO guidelines for indoor air quality: dampness and mould. Geneva: WHO Regional Office for Europe; 2009.
Jaakkola MS, Quansah R, Hugg TT, Heikkinen SA, Jaakkola JJ. Association of indoor dampness and molds with rhinitis risk: a systematic review and meta-analysis. J Allergy Clin Immunol. 2013;132(5):1099–110.e18. https://doi.org/10.1016/j.jaci.2013.07.028.
Mendell MJ, Mirer AG, Cheung K, Tong M, Douwes J. Respiratory and allergic health effects of dampness, mold, and dampness-related agents: a review of the epidemiologic evidence. Environ Health Perspect. 2011;119(6):748–56. https://doi.org/10.1289/ehp.1002410.
Quansah R, Jaakkola MS, Hugg TT, Heikkinen SA, Jaakkola JJ. Residential dampness and molds and the risk of developing asthma: a systematic review and meta-analysis. PLoS One. 2012;7(11):e47526. https://doi.org/10.1371/journal.pone.0047526.
Mudarri DH. Valuing the economic costs of allergic rhinitis, acute bronchitis, and asthma from exposure to indoor dampness and mold in the US. J Environ Public Health. 2016;2016:12. https://doi.org/10.1155/2016/2386596.
Eduard W. Fungal spores: a critical review of the toxicological and epidemiological evidence as a basis for occupational exposure limit setting. Crit Rev Toxicol. 2009;39(10):799–864. https://doi.org/10.3109/10408440903307333.
Rintala H, Pitkaranta M, Taubel M. Microbial communities associated with house dust. Adv Appl Microbiol. 2012;78:75–120. https://doi.org/10.1016/b978-0-12-394805-2.00004-x.
• Vesper S. Traditional mould analysis compared to a DNA-based method of mould analysis. Crit Rev Microbiol. 2011;37(1):15–24. https://doi.org/10.3109/1040841x.2010.506177 COMMENT: Review highlighting the differences between molecular-based methods and traditional methods to assess fungal exposure.
Dannemiller KC, Gent JF, Leaderer BP, Peccia J. Indoor microbial communities: influence on asthma severity in atopic and nonatopic children. J Allergy Clin Immunol. 2016. https://doi.org/10.1016/j.jaci.2015.11.027.
•• Dannemiller KC, Mendell MJ, Macher JM, Kumagai K, Bradman A, Holland N, et al. Next-generation DNA sequencing reveals that low fungal diversity in house dust is associated with childhood asthma development. Indoor Air. 2014;24(3):236–47 COMMENT: Next generation sequencing analysis that identified a low diversity of Cryptococcus to be associated with asthma development.
•• National Academies of Sciences Engineering Medicine, Microbiomes of the built environment: a research agenda for indoor microbiology, human health, and buildings. Washington, DC: The National Academies Press; 2017. Report No.: 978–0–309-44980-9. COMMENT: Report published by the National Academies of Sciences, Engineering and Medicine that reviews the state of knowledge and knowledge gaps of microbiomes within the built environment.
Pitkäranta M, Meklin T, Hyvärinen A, Nevalainen A, Paulin L, Auvinen P, et al. Molecular profiling of fungal communities in moisture damaged buildings before and after remediation - a comparison of culture-dependent and culture-independent methods. BMC Microbiol. 2011;11(1):235. https://doi.org/10.1186/1471-2180-11-235.
Pitkaranta M, Meklin T, Hyvarinen A, Paulin L, Auvinen P, Nevalainen A, et al. Analysis of fungal flora in indoor dust by ribosomal DNA sequence analysis, quantitative PCR, and culture. Appl Environ Microbiol. 2008;74(1):233–44. https://doi.org/10.1128/aem.00692-07.
Green BJ, Lemons AR, Park Y, Cox-Ganser JM, Park JH. Assessment of fungal diversity in a water-damaged office building. J Occup Environ Hyg. 2017;14(4):285–93. https://doi.org/10.1080/15459624.2016.1252044.
Mbareche H, Veillette M, Dubuis ME, Bakhiyi B, Marchand G, Zayed J, et al. Fungal bioaerosols in biomethanization facilities. J Air Waste Manag Assoc. 2018. https://doi.org/10.1080/10962247.2018.1492472.
Degois J, Clerc F, Simon X, Bontemps C, Leblond P, Duquenne P. First metagenomic survey of the microbial diversity in bioaerosols emitted in waste sorting plants. Ann Work Expo Health. 2017;61(9):1076–86. https://doi.org/10.1093/annweh/wxx075.
•• Mbareche H, Veillette M, Bonifait L, Dubuis ME, Benard Y, Marchand G, et al. A next generation sequencing approach with a suitable bioinformatics workflow to study fungal diversity in bioaerosols released from two different types of composting plants. Sci Total Environ. 2017;601-602:1306–14. https://doi.org/10.1016/j.scitotenv.2017.05.235 COMMENT: Profile of fungal bioaerosols identified in composting plants using next generation sequencing.
Madsen AM, Zervas A, Tendal K, Nielsen JL. Microbial diversity in bioaerosol samples causing ODTS compared to reference bioaerosol samples as measured using Illumina sequencing and MALDI-TOF. Environ Res. 2015;140:255–67. https://doi.org/10.1016/j.envres.2015.03.027.
Pellissier L, Oppliger A, Hirzel AH, Savova-Bianchi D, Mbayo G, Mascher F, et al. Airborne and grain dust fungal community compositions are shaped regionally by plant genotypes and farming practices. Appl Environ Microbiol. 2016;82(7):2121–31. https://doi.org/10.1128/aem.03336-15.
Green BJ, Couch JR, Lemons AR, Burton NC, Victory KR, Nayak AP, et al. Microbial hazards during harvesting and processing at an outdoor United States cannabis farm. J Occup Environ Hyg. 2018;15(5):430–40. https://doi.org/10.1080/15459624.2018.1432863.
Haugland RA, Heckman JL. Identification of putative sequence specific PCR primers for detection of the toxigenic fungal species Stachybotrys chartarum. Mol Cell Probes. 1998;12(6):387–96. https://doi.org/10.1006/mcpr.1998.0197.
Haugland RA, Brinkman N, Vesper SJ. Evaluation of rapid DNA extraction methods for the quantitative detection of fungi using real-time PCR analysis. J Microbiol Methods. 2002;50(3):319–23.
Haugland RA, Varma M, Wymer LJ, Vesper SJ. Quantitative PCR analysis of selected Aspergillus, Penicillium and Paecilomyces species. Syst Appl Microbiol. 2004;27(2):198–210. https://doi.org/10.1078/072320204322881826.
Vesper SJ, Wymer LJ, Meklin T, Varma M, Stott R, Richardson M, et al. Comparison of populations of mould species in homes in the UK and USA using mould-specific quantitative PCR. Lett Appl Microbiol. 2005;41(4):367–73. https://doi.org/10.1111/j.1472-765X.2005.01764.x.
Vesper S, Barnes C, Ciaccio CE, Johanns A, Kennedy K, Murphy JS, et al. Higher Environmental Relative Moldiness Index (ERMI) values measured in homes of asthmatic children in Boston, Kansas City, and San Diego. J Asthma. 2013;50(2):155–61. https://doi.org/10.3109/02770903.2012.740122.
Vesper S, McKinstry C, Ashley P, Haugland R, Yeatts K, Bradham K, et al. Quantitative PCR analysis of molds in the dust from homes of asthmatic children in North Carolina. J Environ Monit. 2007;9(8):826–30. https://doi.org/10.1039/b704359g.
Vesper S, McKinstry C, Haugland R, Neas L, Hudgens E, Heidenfelder B, et al. Higher Environmental Relative Moldiness Index (ERMIsm) values measured in Detroit homes of severely asthmatic children. Sci Total Environ. 2008;394(1):192–6. https://doi.org/10.1016/j.scitotenv.2008.01.031.
Reponen T, Lockey J, Bernstein DI, Vesper SJ, Levin L, Khurana Hershey GK et al. Infant origins of childhood asthma associated with specific molds. J Allergy Clin Immunol 2012;130(3):639–44.e5. doi:https://doi.org/10.1016/j.jaci.2012.05.030.
Levetin E, Horner WE, Scott JA. Taxonomy of allergenic fungi. J Allergy Clin Immunol Pract. 2016;4(3):375–85.e1. https://doi.org/10.1016/j.jaip.2015.10.012.
Lindahl BD, Nilsson RH, Tedersoo L, Abarenkov K, Carlsen T, Kjøller R et al. Fungal community analysis by high-throughput sequencing of amplified markers – a user’s guide. The New Phytol 2013;199(1):288–299. doi:https://doi.org/10.1111/nph.12243.
Blaalid R, Kumar S, Nilsson RH, Abarenkov K, Kirk PM, Kauserud H. ITS1 versus ITS2 as DNA metabarcodes for fungi. Mol Ecol Resour. 2013;13(2):218–24. https://doi.org/10.1111/1755-0998.12065.
Koljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AF, Bahram M, et al. Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol. 2013;22(21):5271–7. https://doi.org/10.1111/mec.12481.
Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, et al. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci U S A. 2012;109(16):6241–6. https://doi.org/10.1073/pnas.1117018109.
Wang XC, Liu C, Huang L, Bengtsson-Palme J, Chen H, Zhang JH, et al. ITS1: a DNA barcode better than ITS2 in eukaryotes? Mol Ecol Resour. 2015;15(3):573–86. https://doi.org/10.1111/1755-0998.12325.
Usyk M, Zolnik CP, Patel H, Levi MH, Burk RD. Novel ITS1 fungal primers for characterization of the mycobiome. mSphere. 2017;2(6). https://doi.org/10.1128/mSphere.00488-17.
Rezaei-Matehkolaei A, Mirhendi H, Makimura K, de Hoog GS, Satoh K, Najafzadeh MJ, et al. Nucleotide sequence analysis of beta tubulin gene in a wide range of dermatophytes. Med Mycol. 2014;52(7):674–88. https://doi.org/10.1093/mmy/myu033.
Ahmadi B, Mirhendi H, Shidfar MR, Nouripour-Sisakht S, Jalalizand N, Geramishoar M, et al. A comparative study on morphological versus molecular identification of dermatophyte isolates. J Mycol Med. 2015;25(1):29–35. https://doi.org/10.1016/j.mycmed.2014.10.022.
Rittenour WR, Ciaccio CE, Barnes CS, Kashon ML, Lemons AR, Beezhold DH, et al. Internal transcribed spacer rRNA gene sequencing analysis of fungal diversity in Kansas City indoor environments. Environ Sci Process Impacts. 2014;16(1):33–43. https://doi.org/10.1039/C3EM00441D.
Ahmed A. Analysis of metagenomics next generation sequence data for fungal ITS barcoding: do you need advance bioinformatics experience? Front Microbiol 2016;7(1061). doi:https://doi.org/10.3389/fmicb.2016.01061.
Asemaninejad A, Weerasuriya N, Gloor GB, Lindo Z, Thorn RG. New primers for discovering fungal diversity using nuclear large ribosomal DNA. PLoS One. 2016;11(7):e0159043. https://doi.org/10.1371/journal.pone.0159043.
Bokulich NA, Mills DA. Improved selection of internal transcribed spacer-specific primers enables quantitative, ultra-high-throughput profiling of fungal communities. Appl Environ Microbiol. 2013;79(8):2519–26. https://doi.org/10.1128/aem.03870-12.
Dannemiller KC, Reeves D, Bibby K, Yamamoto N, Peccia J. Fungal high-throughput taxonomic identification tool for use with next-generation sequencing (FHiTINGS). J Basic Microbiol. 2014;54(4):315–21. https://doi.org/10.1002/jobm.201200507.
Ihrmark K, Bodeker IT, Cruz-Martinez K, Friberg H, Kubartova A, Schenck J, et al. New primers to amplify the fungal ITS2 region--evaluation by 454-sequencing of artificial and natural communities. FEMS Microbiol Ecol. 2012;82(3):666–77. https://doi.org/10.1111/j.1574-6941.2012.01437.x.
Lee S, Yamamoto N. Accuracy of the high-throughput amplicon sequencing to identify species within the genus Aspergillus. Fungal Biol. 2015;119(12):1311–21. https://doi.org/10.1016/j.funbio.2015.10.006.
Mueller RC, Gallegos-Graves LV, Kuske CR. A new fungal large subunit ribosomal RNA primer for high-throughput sequencing surveys. FEMS Microbiol Ecol. 2016;92(2). doi:https://doi.org/10.1093/femsec/fiv153.
Rittenour WR, Park J-H, Cox-Ganser JM, Beezhold DH, Green BJ. Comparison of DNA extraction methodologies used for assessing fungal diversity via ITS sequencing. J Environ Monit. 2012;14(3):766–74. https://doi.org/10.1039/C2EM10779A.
Yahr R, Schoch CL, Dentinger BT. Scaling up discovery of hidden diversity in fungi: impacts of barcoding approaches. Philos Trans R Soc Lond Ser B Biol Sci. 2016;371(1702). https://doi.org/10.1098/rstb.2015.0336.
Fröhlich-Nowoisky J, Pickersgill DA, Després VR, Pöschl U. High diversity of fungi in air particulate matter. Proc Natl Acad Sci U S A. 2009;106(31):12814–9. https://doi.org/10.1073/pnas.0811003106.
Chen W, Hambleton S, Seifert KA, Carisse O, Diarra MS, Peters RD, et al. Assessing performance of spore samplers in monitoring aeromycobiota and fungal plant pathogen diversity in Canada. Appl Environ Microbiol. 2018;84(9). https://doi.org/10.1128/aem.02601-17.
Magurran AE. Measuring biological diversity. Oxford: Blackwell Publishing; 2004.
Hibbett DS, Bauer R, Binder M, Giachini AJ, Hosaka K, Justo A et al. 14 Agaricomycetes. In: McLaughlin JD, Spatafora WJ, editors. Systematics and evolution: part A. Berlin, Heidelberg: Springer Berlin Heidelberg; 2014. p. 373–429.
Dannemiller KC, Gent JF, Leaderer BP, Peccia J. Influence of housing characteristics on bacterial and fungal communities in homes of asthmatic children. Indoor Air. 2016;26(2):179–92. https://doi.org/10.1111/ina.12205.
Yoshida K, Suga M, Yamasaki H, Nakamura K, Sato T, Kakishima M, et al. Hypersensitivity pneumonitis induced by a smut fungus Ustilago esculenta. Thorax. 1996;51(6):650.
Madsen AM, Tendal K, Schlunssen V, Heltberg I. Organic dust toxic syndrome at a grass seed plant caused by exposure to high concentrations of bioaerosols. Ann Occup Hyg. 2012;56(7):776–88. https://doi.org/10.1093/annhyg/mes012.
Sáenz-de-Santamaría M, Postigo I, Gutierrez-Rodríguez A, Cardona G, Guisantes J, Asturias J, et al. The major allergen of Alternaria alternata (Alt a 1) is expressed in other members of the Pleosporaceae family. Mycoses. 2006;49(2):91–5.
Williamson B, Tudzynski B, Tudzynski P, Van Kan JAL. Botrytis cinerea: the cause of grey mould disease. Mol Plant Path. 2007;8(5):561–80. https://doi.org/10.1111/j.1364-3703.2007.00417.x.
McPartland JM. A review of Cannabis diseases. J Int Hemp Assoc. 1996;3(1):19–23.
Rodriguez G, Kibler A, Campbell P, Punja ZK. Fungal diseases of Cannabis sativa in British Columbia, Canada. http://www.apsnet.org/meetings/Documents/2015_meeting_abstracts/aps2015abP319.htm, Annual Phytopathological Society Annual Meeting. 2015. Accessed 7/26/2017.
Monso E, Magarolas R, Badorrey I, Radon K, Nowak D, Morera J. Occupational asthma in greenhouse flower and ornamental plant growers. Am J Respir Crit Care Med. 2002;165(7):954–60. https://doi.org/10.1164/ajrccm.165.7.2106152.
Radon K, Danuser B, Iversen M, Monso E, Weber C, Hartung J, et al. Air contaminants in different European farming environments. Ann Agric Environ Med. 2002;9(1):41–8.
Groenewoud GC, de Graaf in ‘t Veld C, vVan Oorschot-van Nes AJ, de Jong NW, Vermeulen AM, van Toorenenbergen AW et al. Prevalence of sensitization to the predatory mite Amblyseius cucumeris as a new occupational allergen in horticulture. Allergy 2002;57(7):614–619.
Groenewoud GC, de Jong NW, Burdorf A, de Groot H, van Wyk RG. Prevalence of occupational allergy to Chrysanthemum pollen in greenhouses in the Netherlands. Allergy. 2002;57(9):835–40.
Groenewoud GC, de Jong NW, van Oorschot-van Nes AJ, Vermeulen AM, van Toorenenbergen AW, Mulder PG, et al. Prevalence of occupational allergy to bell pepper pollen in greenhouses in the Netherlands. Clin Exp Allergy. 2002;32(3):434–40.
Jarvis W. The dispersal of spores of Botrytis cinerea Fr. in a raspberry plantation. Trans Brit Mycol Soc. 1962;45(4):549–59.
Jeebhay MF, Baatjies R, Chang YS, Kim YK, Kim YY, Major V, et al. Risk factors for allergy due to the two-spotted spider mite (Tetranychus urticae) among table grape farm workers. Int Arch Allergy Immunol. 2007;144(2):143–9. https://doi.org/10.1159/000103226.
Popp W, Ritschka L, Zwick H, Rauscher H. “Berry sorter’s lung” or wine grower’s lung--an exogenous allergic alveolitis caused by Botrytis cinerea spores. Prax Klin Pneumol. 1987;41(5):165–9.
McKernan K, Spangler J, Helbert Y, Lynch RC, Devitt-Lee A, Zhang L, et al. Metagenomic analysis of medicinal Cannabis samples; pathogenic bacteria, toxigenic fungi, and beneficial microbes grow in culture-based yeast and mold tests. F1000 Res. 2016;5:2471. https://doi.org/10.12688/f1000research.9662.1.
McKernan K, Spangler J, Zhang L, Tadigotla V, Helbert Y, Foss T et al. Cannabis microbiome sequencing reveals several mycotoxic fungi native to dispensary grade Cannabis flowers. F1000 Res. 2015;4:1422. doi:https://doi.org/10.12688/f1000research.7507.2.
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Green, B.J. Emerging Insights into the Occupational Mycobiome. Curr Allergy Asthma Rep 18, 62 (2018). https://doi.org/10.1007/s11882-018-0818-2
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DOI: https://doi.org/10.1007/s11882-018-0818-2