Abstract
The lack of information on biological risks in workplaces arises from the difficulty to measure bioaerosol. This study aimed to develop and improve the bioaerosol monitoring technique that uses proper biomarkers as a tool. Muramic and dipicolinic acids, and ergosterol were used as tracers for bacteria cells, bacterial spores, and fungal spores, respectively. Furthermore, 12- and 13-methyltetradecanoic acids (iso- and anteiso- C15:0) were used to study the presence of airborne bacteria and 3-hydroxy fatty acids were used to determine the concentration of peptidoglycan. Airborne particulate matter was sampled in a municipal indoor waste composting facility by multistage impactor samplers, during three main stages of composting process. The microorganism content, in airborne particles with aerodynamic diameter minor then 1 μm and between 1 and 10 μm, was determined starting from the aforementioned biomarker concentrations. For iso- and anteiso- C15:0, a conversion factor to transform its concentration into bacterial content was tentatively proposed. The results show that the chemical method covers some gaps in the information about bioaerosol presence in polluted atmospheres. Differences up to two orders of magnitude are observed, by comparing the results obtained by biomarkers and by cultivation-dependent methods. The microbial content, expressed as a percentage by mass on respect the PM, ranged from 4 to 28% with higher percentages during shredding and mixing stages and lower values during biocell opening operations. Bacterial spores, bacterial cells, and fungal spores detected were high in number, compared with the findings in similar studies elsewhere.
Similar content being viewed by others
References
Annous BA, Becker LA, Bayles DO, Labeda DP, Wilkinson BJ (1997) Critical role of Anteiso-C15:0 fatty acid in the growth of listeria monocytogenes at low temperatures. Appl Environ Microbiol 63(10):3887–3894 0099-2240/97/$04.0010
Black GE, Fox A, Fox K, Snyder AP, Smith PBW (1994) Electrospray tandem mass spectrometry for analysis of native muramic acid in whole bacterial cell Hydrolyzates. Anal Chem 66(23):4171–4176. https://doi.org/10.1021/ac00095a010
Bowers RM, Clements N, Emerson JB, Wiedinmyer C, Hannigan MP, Fierer N (2013) Seasonal variability in bacterial and fungal diversity of the near-surface atmosphere. Environ Sci Technol 47:12097–12106. https://doi.org/10.1021/es402970s
Bruni E, Simonetti G, Bovone B, Casagrande C, Castellani F, Riccardi C, Pomata D, Di Filippo P, Federici E, Buiarelli F, Uccelletti D (2020) Evaluation of bioaerosol bacterial components of a wastewater treatment plant through an integrate approach and in vivo assessment. IJERPH 17(1):273. https://doi.org/10.3390/ijerph17010273
Buiarelli F, Gallo V, Di Filippo P, Pomata D, Riccardi C (2013a) Development of a method for the analysis of underivatized amino acids by liquid chromatography/tandem mass spectrometry: application on standard reference material 1649a (urban dust). Talanta 115:966–972. https://doi.org/10.1016/j.talanta.2013.07.009
Buiarelli F, Canepari S, Di Filippo P, Perrino C, Pomata D, Riccardi C, Speziale R (2013b) Extraction and analysis of fungal spore biomarkers in atmospheric bioaerosol by HPLC–MS–MS and GC–MS. Talanta 105:142–151. https://doi.org/10.1016/j.talanta.2012.11.006
Buiarelli F, Sonego E, Uccelletti D, Bruni E, Di Filippo P, Pomata D, Riccardi C, Perrino C, Marcovecchio F, Simonetti G (2019a) Determination of the main bioaerosol components using chemical markers by liquid chromatography–tandem mass spectrometry. Microchem J 149:103974. https://doi.org/10.1016/j.microc.2019.103974
Buiarelli F, Di Filippo P, L Massimi D Pomata C Riccardi G Simonetti E Sonego (2019b) Ultrafine, fine and coarse airborne particle mass concentration in work places. Atmos Pollut Res 10(5):1685–1690. https://doi.org/10.1016/j.apr.2019.06.009
Davis BD, Dulbecco R, Eisen HN, Ginsberg HS (1973) Bacterial physiology: microbiology (2nd edition), Harper and Row, New York. 96-97. https://doi.org/10.1002/jobm.19820220411
Deacon LJ, Pankhurst LJ, Drew GH, Hayes ET, Jackson S, Longhurst PJ, Longhurst JWS, Liu J, Pollard SJT, Tyrrel SF (2009) Particle size distribution of airborne Aspergillus fumigatus spores emitted from compost using membrane filtration. Atmos Environ 43:5698–5701. https://doi.org/10.1016/j.atmosenv.2009.07.042
Di Filippo P, Riccardi C, Pomata D, Buiarelli F (2010) Concentrations of PAHs, and nitro- and methyl- derivatives associated with a size-segregated urban aerosol. Atmos Environ 44:2742–2749. https://doi.org/10.1016/j.atmosenv.2010.04.035
Di Filippo P, Pomata D, Riccardi C, Buiarelli F, Perrino C (2013) Fungal contribution to size-segregated aerosol measured through biomarkers. Atmos Environ 64:132–140. https://doi.org/10.1016/j.atmosenv.2012.10.010
Di Filippo P, Pomata D, Riccardi C, Buiarelli F, Gallo V, Quaranta A (2014) Free and combined amino acids in size-segregated atmospheric aerosol samples. Atmos Environ 98:179–189. https://doi.org/10.1016/j.atmosenv.2014.08.069
Di Filippo P, Pomata D, Riccardi C, Buiarelli F, Uccelletti D, Zanni E (2017) Muramic and dipicolinic acids in atmospheric particulate matter as biomarkers of bacteria and bacterial spores. Anal Bioanal Chem 409:1657–1666. https://doi.org/10.1007/s00216-016-0111-y
Douwes J, Versloot P, Hollander A, Heederik D, Doekes G (1995) Influence of various dust sampling and extraction methods on the measurement of airborne endotoxin. Appl Environ Microbiol 61(5):1763–1769 0099-2240/95/$04.0010
Douwes J, Thorne P, Pearce N, Heederik D (2003) Bioaerosol health effects and exposure assessment: progress and prospects. Ann Occup Hyg 47(3):187–200. https://doi.org/10.1093/annhyg/meg032
Elbert W, Taylor PE, Andreae MO, Pöschl U (2007) Contribution of fungi to primary biogenic aerosols in the atmosphere: wet and dry discharged spores, carbohydrates, and inorganic ions. Atmos Chem Phys 7(17):4569–4588. https://doi.org/10.5194/acp-7-4569-2007
Fang Z, Ouyang Z, Zheng H, Wang X, Hu L (2007) Culturable airborne bacteria in outdoor environments in Beijing, China. Microb Ecol 54:487–496. https://doi.org/10.1007/s00248-007-9216-3
Ferguson RMW, Garcia-Alcega S, Coulon F, Dumbrell AJ, Whitby C, Colbeck I (2019) Bioaerosol biomonitoring: sampling optimization for molecular microbial ecology. Mol Ecol Resour 19:672–690. https://doi.org/10.1111/1755-0998.13002
French EA, Bertics SJ, Armentano LE (2012) Rumen and milk odd- and branched-chain fatty acid proportions are minimally influenced by ruminal volatile fatty acid infusions. J Dairy Sci 95:2015–2026. https://doi.org/10.3168/jds.2011-4827
Ghimire PS, Tripathee L, Chen P, Kang S (2019) Linking the conventional and emerging detection techniques for ambient bioaerosols: a review. Rev Environ Sci Bio 18(3):495–523. https://doi.org/10.1007/s11157-019-09506-z
Giorgio D, Di Trana A, Di Napoli MA, Sepe L, Cecchini S, Rossi R, Claps S (2019) Comparison of cheeses from goats fed 7 forages based on a new health index. J Dairy Sci 102:6790–6801. https://doi.org/10.3168/jds.2018-15857
Heldal KK, Madsø L, Eduard W (2015) Airway inflammation among compost workers exposed to actinomycetes spores. Ann Agric Environ Med 22(2):253–258. https://doi.org/10.5604/12321966.1152076
Heldal KK, Barregard L, Ellingsen DG (2016) Biomarkers of inflammation in workers exposed to compost and sewage dust. Int Arch Occup Environ Health 89:711–718. https://doi.org/10.1007/s00420-015-1109-z
Hollander A, Heederik D, Kauffman H (1994) Acute respiratory effects in the potato processing industry due to a bioaerosol exposure. Ann Occup Environ Med 51:73–78. https://doi.org/10.1136/oem.51.2.73
Kaneda T (1991) Iso- and anteiso-fatty acids in bacteria: biosynthesis, function, and taxonomic significance. Microbiol Rev 55(2):288–302 0146-0749/91/020288-15$02.00/0
Lee AKY, Chan CK, Fang M, Lau APS (2004) The 3-hydroxy fatty acids as biomarkers for quantification and characterization of endotoxins and Gram-negative bacteria in atmospheric aerosols in Hong Kong. Atmos Environ 38:6307–6317. https://doi.org/10.1016/j.atmosenv.2004.08.013
Leo RF, Parker PL (1966) Branched-Chain Fatty Acids in Sediments. Science 152(3722):649-650. https://doi.org/10.1126/science.152.3722.649
Madsen AM, Frederiksen MW, Bjerregaard M, Tendal K (2020) Measures to reduce the exposure of waste collection workers to handborne and airborne microorganisms and inflammogenic dust. Waste Manag 101:241–249. https://doi.org/10.1016/j.wasman.2019.10.023
Mielniczuk Z, Mielniczuk E, Larsson L (1993) Gas chromatography-mass spectrometry methods for analysis of 2- and 3-hydroxylated fatty acids: application for endotoxin measurement. J Microbiol Methods 17(2):91–102 10.1016/0167-7012(93)90002-Y
Moustafa M (2017) Concentration and size distribution of biological particles in school classrooms. J Adv Phys 13(8):5085–5091. https://doi.org/10.24297/jap.v13i8.6339
Nirmalkar J, Deb MK, Deshmukh DK, Tsai YI, Verma SK (2015a) Molecular markers in ambient aerosol in the Mahanadi Riverside Basin of eastern central India during winter. Environ Sci Pollut Res Int 22(2):1220–1231. https://doi.org/10.1007/s11356-014-3416-4
Nirmalkar J, Deb MK, Tsai YI, Deshmukh DK (2015b) Arabitol and mannitol as tracer for fungal contribution to size-differentiated particulate matter of rural atmospheric aerosols. IJESD 6(6):460–463. https://doi.org/10.7763/IJESD.2015.V6.637
Nirmalkar J, Deshmukh DK, Deb MK, Tsai YI, Sopajaree K (2015c) Mass loading and episodic variation of molecular markers in PM2.5 aerosols over a rural area in eastern central India. Atmos Environ 117:41–50. https://doi.org/10.1016/j.atmosenv.2015.07.003
Nirmalkar J, Deshmukh DK, Deb MK, Tsai YI, Pervez S (2019) Characteristics of aerosol during major biomass burning events over eastern central India in winter: a tracer-based approach. Atmos Pollut Res 10(3):817–826. https://doi.org/10.1016/j.apr.2018.12.010
Nordström KM, Laakso SV (1992) Effect of growth temperature on fatty acid composition of ten Thermus strains. Appl Environ Microbiol 58(5):1656–1660 0099-2240/92/051656-05$02.00/0
Pomata D, Di Filippo P, Riccardi C, Buiarelli F, Gallo V (2014) Determination of non-certified levoglucosan, sugar polyols and ergosterol in NIST standard reference material 1649a. Atmos Environ 84:332–338. https://doi.org/10.1016/j.atmosenv.2013.11.069
Robertson S, Douglas P, Jarvis D, Marczylo E (2019) Bioaerosol exposure from composting facilities and health outcomes inworkers and in the community: a systematic review update. Int J Hyg Environ Health 222(3):364–386. https://doi.org/10.1016/j.ijheh.2019.02.006
Shaffer BT, Lighthart B (1997) Survey of Culturable airborne Bacteria at four diverse locations in Oregon: urban, rural, forest, and coastal. Microb Ecol 34:167–177. https://doi.org/10.1007/s002489900046
Stagg S, Bowry A, Kelsey A, Crook B (2010) Bioaerosol emissions from waste composting and the potential for workers’ exposure. Health and Safety Executive research report
Wei M, Xu C, Xu X, Zhu C, Li J, Lv G (2019) Characteristics of atmospheric bacterial and fungal communities in PM2.5following biomass burning disturbance in a rural area of North China Plain. Sci Total Environ 651(2):2727–2739. https://doi.org/10.1016/j.scitotenv.2018.09.399
Funding
This study was funded by the Italian Workers’ Compensation Authority (INAIL) (grant number BRIC2016 ID23).
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Di Filippo, P., Pomata, D., Riccardi, C. et al. Concentrations of bacteria and bacterial and fungal spores calculated from chemical tracers associated with size-segregated aerosol in a composting plant. Air Qual Atmos Health 13, 469–476 (2020). https://doi.org/10.1007/s11869-020-00802-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11869-020-00802-0