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Seasonal variability of bacteria in fine and coarse urban air particulate matter

  • Environmental Biotechnology
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Abstract

The current knowledge about the microbial communities associated with airborne particulate matter, particularly in urban areas, is limited. This study aims to fill this gap by describing the microbial community associated with coarse (PM10) and fine (PM2.5) particulate matter using pyrosequencing. Particulate matter was sampled on Teflon filters over 3 months in summer and 3 months in winter in Milan (Italy), and the hypervariable V3 region of the gene 16S rRNA amplified from the DNA extracted from the filters. The results showed large seasonal variations in the microbial communities, with plant-associated bacteria dominating in summer and spore-forming bacteria in winter. Bacterial communities from PM10 and PM2.5 were also found to differ from each other by season. In all samples, a high species richness, comparable with that of soils, but a low evenness was found. The results suggest that not only can the sources of the particulate influence the presence of specific bacterial groups but also that environmental factors and stresses can shape the bacterial community.

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References

  • Angenent LT, Kelley ST, St Amand A, Pace NR, Hernandez MT (2005) Molecular identification of potential pathogens in water and air of a hospital therapy pool. Proc Nat Acad Sci USA 102:4860–4865

    Article  CAS  Google Scholar 

  • Ariya PA, Amyot M (2004) New directions: the role of bioaerosols in atmospheric chemistry and physics. Atmos Environ 38:1231–1232

    Article  CAS  Google Scholar 

  • Bell TJ, Newman A, Silverman BW, Turner SL, Lilley AK (2005) The contribution of species richness and composition to bacterial services. Nature 436:1157–1160

    Article  CAS  Google Scholar 

  • Bell ML, Dominici F, Ebisu K, Zeger SL, Samet JM (2007) Spatial and temporal variation in PM2.5 chemical composition in the United States for health effects studies. Environ Health Perspect 115:989–995

    Article  CAS  Google Scholar 

  • Bowers RM, Lauber CL, Wiedinmyer C, Hamady M, Hallar AG, Fall R, Knight R, Fierer N (2009) Characterization of airborne microbial communities at a high-elevation site and their potential to act as atmospheric ice nuclei. Appl Environ Microbiol 75:5121–5130

    Article  CAS  Google Scholar 

  • Brodie EL, DeSantis TZ, Parker JP M, Zubietta IX, Piceno YM, Andersen GL (2007) Urban aerosols harbor diverse and dynamic bacterial populations. Proc Natl Acad Sci USA 104:299–304

    Article  CAS  Google Scholar 

  • Camatini M, Mantecca P, Corvaja V, Gualtieri M (2009) PM10 in Milan: seasonal variations in eliciting biological effects on A549 cell line. Toxicol Lett 189:S79–S80

    Article  Google Scholar 

  • Cardinale BJ, Palmer MA, Collins SL (2002) Species diversity enhances ecosystem functioning through interspecific facilitation. Nature 415:426–429

    Article  CAS  Google Scholar 

  • Claesson MJ, O’Sullivan O, Wang Q, Nikkila J, Marchesi JR, Smidt H, de Vos WM, Ross RP, O’Toole PW (2009) Comparative analysis of pyrosequencing and a phylogenetic microarray for exploring microbial community structures in the human distal intestine. PLoS ONE 4:e6669

    Article  Google Scholar 

  • Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje JM (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141–D145

    Article  CAS  Google Scholar 

  • Cote V, Kos G, Mortazavi R, Ariya PA (2008) Microbial and de novo transformation of dicarboxylic acids by three airborne fungi. Sci Total Environ 390:530–537

    Article  CAS  Google Scholar 

  • Deguillaume L, Leriche M, Amato P, Ariya PA, Delort AM, Poschl U, Chaumerliac N, Bauer H, Flossmann AI, Morris CE (2008) Microbiology and atmospheric processes: chemical interactions of primary biological aerosols. Biogeosciences 5:1073–1084

    Article  CAS  Google Scholar 

  • Englert N (2004) Fine particles and human health—a review of epidemiological studies. Toxicol Lett 149:235–242

    Article  CAS  Google Scholar 

  • European Environmental Agency (EEA) (2009) Spatial assessment of PM10 and ozone concentrations in Europe (2005) Copenhagen. EEA, Denmark

    Google Scholar 

  • Fang ZG, Ouyang ZY, Zheng H, Wang XK, Hu LF (2007) Culturable airborne bacteria in outdoor environments in Beijing, China. Microb Ecol 54:487–496

    Article  Google Scholar 

  • Fierer N, Liu ZZ, Rodriguez-Hernandez M, Knight R, Henn M, Hernandez MT (2008) Short-term temporal variability in airborne bacterial and fungal populations. Appl Environ Microbiol 74:200–207

    Article  CAS  Google Scholar 

  • Finnerty K, Choi JE, Lau A, Davis-Gorman G, Diven C, Seaver N, Linak WP, Witten M, McDonagh PF (2007) Instillation of coarse ash particulate matter and lipopolysaccharide produces a systemic inflammatory response in mice. J Toxicol Environ Health A 70:1957–1966

    Article  CAS  Google Scholar 

  • Frohlich-Nowoisky J, Pickersgill DA, Despres VR, Poschl U (2009) High diversity of fungi in air particulate matter. Proc Natl Acad Sci USA 106:12814–12819

    Article  Google Scholar 

  • Fuzzi S, Mandrioli P, Perfetto A (1997) Fog droplets—an atmospheric source of secondary biological aerosol particles. Atmos Environ 31:287–290

    Article  CAS  Google Scholar 

  • Gini C (1912) Variability and mutuability (Variabilitá e mutuabilitá). In: Pinzetti TE, Salvemini (eds) Memories of methodological statistics (Memorie di metodologica statistica) (1955). Libreria Eredi Virgilio Veschi, Rome

    Google Scholar 

  • Gualtieri M, Mantecca P, Corvaja V, Longhin E, Perrone MG, Bolzacchini E, Camatini M (2009) Winter fine particulate matter from Milan induces morphological and functional alterations in human pulmonary epithelial cells (A549). Toxicol Lett 188:52–62

    Article  CAS  Google Scholar 

  • Handcock M, Morris M (1999) Relative distribution methods in the social sciences. Springer, New York

    Google Scholar 

  • Hill TCJ, Walsh KA, Harris JA, Moffett BF (2003) Using ecological diversity measures with bacterial communities. FEMS Microbiol Ecol 43:1–11

    Article  CAS  Google Scholar 

  • Hong SH, Bunge J, Jeon SO, Epstein SS (2006) Predicting microbial species richness. Proc Natl Acad Sci USA 103:117–122

    Article  CAS  Google Scholar 

  • Horner-Devine MC, Carney KM, Bohannan BJM (2004) An ecological perspective on bacterial biodiversity. Proc R Soc Lond B Biol Sci 271:113–122

    Article  Google Scholar 

  • Huse SM, Dethlefsen L, Huber JA, Welch DM, Relman DA, Sogin ML (2008) Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. PLoS Genet 4:e1000255

    Article  Google Scholar 

  • Kim H, Nishiyama M, Kunito T, Senoo K, Kawahara K, Murakami K, Oyaizu H (1998) High population of Sphingomonas species on plant surface. J Appl Microbiol 85:731–736

    Article  Google Scholar 

  • Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76

    Article  CAS  Google Scholar 

  • Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar BA, Lai T, Steppi S, Jobb G, Förster W, Brettske I, Gerber S, Ginhart A, Gross O, Grumann S, Hermann S, Jost R, König A, Liss T, Lüssmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer K (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371

    Article  CAS  Google Scholar 

  • Mancinelli RL, Shulls W (1978) Airborne bacteria in an urban-environment. Appl Environ Microbiol 35:1095–1101

    CAS  Google Scholar 

  • Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen YJ, Chen ZT, Dewell SB, Du L, Fierro JM, Gomes XV, Godwin BC, He W, Helgesen S, Ho CH, Irzyk GP, Jando SC, Alenquer MLI, Jarvie TP, Jirage KB, Kim JB, Knight JR, Lanza JR, Leamon JH, Lefkowitz SM, Lei M, Li J, Lohman KL, Lu H, Makhijani VB, McDade KE, McKenna MP, Myers EW, Nickerson E, Nobile JR, Plant R, Puc BP, Ronan MT, Roth GT, Sarkis GJ, Simons JF, Simpson JW, Srinivasan M, Tartaro KR, Tomasz A, Vogt KA, Volkmer GA, Wang SH, Wang Y, Weiner MP, Yu PG, Begley RF, Rothberg JM (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376–380

    CAS  Google Scholar 

  • Maron PA, Mougel C, Lejon DPH, Carvalho E, Bizet K, Marck G, Cubito N, Lemanceau P, Ranjard L (2006) Temporal variability of airborne bacterial community structure in an urban area. Atmos Environ 40:8074–8080

    Article  CAS  Google Scholar 

  • Matthias-Maser S, Obolkin V, Khodzer T, Jaenicke R (2000) Seasonal variation of primary biological aerosol particles in the remote continental region of Lake Baikal/Siberia. Atmos Environ 34:3805–3811

    Article  CAS  Google Scholar 

  • Mueller-Annelin L, Avol E, Peters JM, Thorne PS (2004) Ambient endotoxin concentrations in PM10 from Southern California. Environ Health Perspect 112:583–588

    Article  Google Scholar 

  • Naeem S, Li SB (1997) Biodiversity enhances ecosystem reliability. Nature 390:507–509

    Article  CAS  Google Scholar 

  • Peccia J, Hernandez M (2006) Incorporating polymerase chain reaction-based identification, population characterization, and quantification of microorganisms into aerosol science: a review. Atmos Environ 40:3941–3961

    Article  CAS  Google Scholar 

  • Polymenakou PN, Mandalakis M, Stephanou EG, Tselepides A (2008) Particle size distribution of airborne microorganisms and pathogens during an intense African dust event in the Eastern Mediterranean. Environ Health Perspect 116:292–296

    Article  Google Scholar 

  • Purvis A, Hector A (2000) Getting the measure of biodiversity. Nature 405:212–219

    Article  CAS  Google Scholar 

  • Quince C, Lanzen A, Curtis TP, Davenport RJ, Hall N, Head IM, Read LF, Sloan WT (2009) Accurate determination of microbial diversity from 454 pyrosequencing data. Nat Methods 6:639–641

    Article  CAS  Google Scholar 

  • R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available at http://www.R-project.org

  • Roesch LF, Fulthorpe RR, Riva A, Casella G, Hadwin AKM, Kent AD, Daroub SH, SH CFAO, Farmerie WG, Triplett EW (2007) Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J 1:283–290

    CAS  Google Scholar 

  • Sankaran M, McNaughton SJ (1999) Determinants of biodiversity regulate compositional stability of communities. Nature 401:691–693

    Article  CAS  Google Scholar 

  • Sattler B, Puxbaum H, Psenner R (2001) Bacterial growth in supercooled cloud droplets. Geophys Res Lett 28:239–242

    Article  Google Scholar 

  • Schloss P, Westcott S, Ryabin T, Hall J, Hartmann M, Hollister E, Lesniewski R, Oakley B, Parks D, Robinson C, Sahl J, Stres B, Thallinger G, Van Horn D, Weber C (2009) Introducing Mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Sogin ML, Morrison HG, Huber JA, Mark Welch D, Huse SM, Neal PR, Arrieta JM, Herndl GJ (2006) Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Natl Acad Sci USA 103:12115–12120

    Article  CAS  Google Scholar 

  • Spurny KR (1996) Chemical mixtures in atmospheric aerosols and their correlation to lung diseases and lung cancer occurrence in the general population. Toxicol Lett 88:271–277

    Article  CAS  Google Scholar 

  • Tringe SG, Zhang T, Liu X, Yu Y, Lee WH, Yap J, Yao F, Suan ST, Ing SK, Haynes M, Rohwer F, Wei CL, Tan P, Bristow J, Rubin EM, Ruan Y (2008) The airborne metagenome in an indoor urban environment. PLoS ONE 3:10

    Article  Google Scholar 

  • U.S. Environmental Protection agency (EPA) (2004) Particulate matter research program five years of progress. EPA, Office of Research and Development, Washington

    Google Scholar 

  • Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    Article  CAS  Google Scholar 

  • Wittebolle L, Marzorati M, Clement L, Balloi A, Daffonchio D, Heylen K, De Vos P, Verstraete W, Boon N (2009) Initial community evenness favours functionality under selective stress. Nature 458:623–626

    Article  CAS  Google Scholar 

  • Yachi S, Loreau M (1999) Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc Natl Acad Sci USA 96:1463–1468

    Article  CAS  Google Scholar 

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Acknowledgements

We thank Ezio Bolzacchini and colleagues for PM sampling and Giuseppe Merlino for helping set up the methods. The authors are grateful to Christopher Quince for precious help on the de-noising process and to J. Bunge and L. Woodard for kindly providing the CatchAll beta.4 software and for assistance in calculations. This work was supported by CARIPLO FOUNDATION (Milan, Italy) in the frame of the project TOSCA (Toxicity of particulate matter and molecular markers of risk).

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Authors and Affiliations

  1. POLARIS Research Centre, Department of Environmental Sciences (DISAT), University of Milano–Bicocca, Piazza della Scienza, 1, 20126, Milan, Italy

    Andrea Franzetti, Isabella Gandolfi, Eleonora Gaspari & Giuseppina Bestetti

  2. Department of Biotechnology and Biosciences, University of Milano–Bicocca, Milan, Italy

    Roberto Ambrosini

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  1. Andrea Franzetti
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  2. Isabella Gandolfi
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  3. Eleonora Gaspari
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Correspondence to Andrea Franzetti.

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Franzetti, A., Gandolfi, I., Gaspari, E. et al. Seasonal variability of bacteria in fine and coarse urban air particulate matter. Appl Microbiol Biotechnol 90, 745–753 (2011). https://doi.org/10.1007/s00253-010-3048-7

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