Spatio-temporal variability of airborne bacterial communities and their correlation with particulate matter chemical composition across two urban areas

Applied Microbiology and Biotechnology

Volumn 99, Issue 11, 2015, Pages 4867-4877

  Gandolfi, I ^a   Bertolini, V ^a   Bestetti, G ^a   Ambrosini, R ^a   Innocente, E ^b   Rampazzo, G ^b   Papacchini, M ^c   Franzetti, A ^a  

^a UNIVERSITY OF MILANO BICOCCA   (Italy)

^b CA' FOSCARI UNIVERSITY OF VENICE   (Italy)

^c ISPESL   (Italy)

Author keywords

Air pollution; Bioaerosol; Milan; NGS; Particulate matter; Venice

Indexed keywords

AIR POLLUTION; ATMOSPHERIC CHEMISTRY; ATMOSPHERIC MOVEMENTS; ATMOSPHERIC STRUCTURE; MICROORGANISMS; POLYMERASE CHAIN REACTION; RNA; SOCIAL SCIENCES; WIND;

BIOAEROSOLS; MILAN; NGS; PARTICULATE MATTER; VENICE;

BACTERIA;

BACTERIAL DNA; BARIUM; MAGNESIUM; PARTICULATE MATTER; RIBOSOME DNA; RNA 16S; SULFATE;

ANALYSIS; BACTERIAL LOAD; BACTERIUM; BIODIVERSITY; CHEMISTRY; CITY; CLASSIFICATION; CLUSTER ANALYSIS; DNA SEQUENCE; GENETICS; HUMAN; ISOLATION AND PURIFICATION; ITALY; METEOROLOGICAL PHENOMENA; MICROBIOLOGY; MOLECULAR GENETICS; PARTICULATE MATTER; PHYLOGENY; REAL TIME POLYMERASE CHAIN REACTION; SPATIOTEMPORAL ANALYSIS;

AIR MICROBIOLOGY; BACTERIA; BACTERIAL LOAD; BARIUM; BIODIVERSITY; CITIES; CLUSTER ANALYSIS; DNA, BACTERIAL; DNA, RIBOSOMAL; HUMANS; ITALY; MAGNESIUM; METEOROLOGICAL CONCEPTS; MOLECULAR SEQUENCE DATA; PARTICULATE MATTER; PHYLOGENY; REAL-TIME POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SPATIO-TEMPORAL ANALYSIS; SULFATES;

EID: 84939965621     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-014-6348-5     Document Type: Article

References (43)

1. Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188
2. Bertolini V, Gandolfi I, Ambrosini R, Bestetti G, Innocente E, Rampazzo G, Franzetti A (2013) Temporal variability and effect of environmental variables on airborne bacterial communities in an urban area of Northern Italy. Appl Microbiol Biotechnol 97:6561–6570. doi:10.1007/s00253-012-4450-0
3. Borchard D, Gillet F, Legendre F (2011) Numerical ecology with R. Springer, New York
4. 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. doi:10.1128/AEM. 00447-09
5. Bowers RM, McLetchie S, Knight R, Fierer N (2011a) Spatial variability in airborne bacterial communities across land-use types and their relationship to the bacterial communities of potential source environments. ISME J 5:601–612. doi:10.1038/ismej.2010.167
6. Bowers RM, Sullivan AP, Costello EK, Collett JL Jr, Knight R, Fierer N, Collett JL (2011b) Sources of bacteria in outdoor air across cities in the midwestern United States. Appl Environ Microbiol 77:6350–6356. doi:10.1128/AEM. 05498-11
7. Bowers RM, McCubbin IB, Hallar AG, Fierer N (2012) Seasonal variability in airborne bacterial communities at a high-elevation site. Atmos Environ 50:41–49. doi:10.1016/j.atmosenv.2012.01.005
8. 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. doi:10.1021/es402970s
9. Brodie EL, DeSantis TZ, Parker JPM, Zubietta IX, Piceno YM, Andersen GL, Moberg Parker JP (2007) Urban aerosols harbor diverse and dynamic bacterial populations. Proc Natl Acad Sci U S A 104:299–304. doi:10.1073/pnas.0608255104
10. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624. doi:10.1038/ismej.2012.8
11. 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
12. Córdova-Kreylos AL, Cao Y, Green PG, Hwang H-M, Kuivila KM, Lamontagne MG, Van De Werfhorst LC, Holden PA, Scow KM (2006) Diversity, composition, and geographical distribution of microbial communities in California salt marsh sediments. Appl Environ Microbiol 72:3357–3366. doi:10.1128/AEM. 72.5.3357-3366.2006
13. Dufrene M, Legendre P (2007) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67:345–366
14. European Environment Agency (2014) Air quality in Europe
15. 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. doi:10.1007/s00248-007-9216-3
16. 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. doi:10.1128/aem. 01467-07
17. Franzetti A, Gandolfi I, Gaspari E, Ambrosini R, Bestetti G (2011) Seasonal variability of bacteria in fine and coarse urban air particulate matter. Appl Microbiol Biotechnol 90:745–753. doi:10.1007/s00253-010-3048-7
18. Fu Y, Keats KF, Rivkin RB, Lang AS (2013) Water mass and depth determine the distribution and diversity of Rhodobacterales in an Arctic marine system. FEMS Microbiol Ecol 84:564–576. doi:10.1111/1574-6941.12085
19. Gandolfi I, Bertolini V, Ambrosini R, Bestetti G, Franzetti A (2013) Unravelling the bacterial diversity in the atmosphere. Appl Microbiol Biotechnol 97:4727–4736. doi:10.1007/s00253-013-4901-2
20. Gilbert JA, Steele JA, Caporaso JG, Steinbrück L, Reeder J, Temperton B, Huse S, McHardy AC, Knight R, Joint I, Somerfield P, Fuhrman JA, Field D (2012) Defining seasonal marine microbial community dynamics. ISME J 6:298–308. doi:10.1038/ismej.2011.107
21. Griffin DW (2007) Atmospheric movement of microorganisms in clouds of desert dust and implications for human health. Clin Microbiol Rev 20:459–77. doi:10.1128/CMR.00039-06, table of contents
22. Jarvis KE, Gray AL, Houk RS (2003) Handbook of inductively coupled plasma mass spectrometry
23. Karthikeyan S, Joshi UM, Balasubramanian R (2006) Microwave assisted sample preparation for determining water-soluble fraction of trace elements in urban airborne particulate matter: evaluation of bioavailability. Anal Chim Acta 576:23–30. doi:10.1016/j.aca.2006.05.051
24. Lee S-H, Lee HMH-J, Kim S-J, Kang H, Kim YP (2010) Identification of airborne bacterial and fungal community structures in an urban area by T-RFLP analysis and quantitative real-time PCR. Sci Total Environ 408:1349–1357. doi:10.1016/j.scitotenv.2009.10.061
25. Legendre P, Legendre L (1998) Numerical ecology, 2nd English edition. Elsevier, Amstrerdam
26. Mantecca P, Gualtieri M, Longhin E, Bestetti G, Palestini P, Bolzacchini E, Camatini M (2012) Adverse biological effects of Milan urban PM looking for suitable molecular markers of exposure. Chem Ind Chem Eng Q 18:635–641. doi:10.2298/CICEQ120206114M
27. Maron P-AA, Lejon DPHH, Carvalho E, Bizet K, Lemanceau P, Ranjard L, Mougel C (2005) Assessing genetic structure and diversity of airborne bacterial communities by DNA fingerprinting and 16S rDNA clone library. Atmos Environ 39:3687–3695. doi:10.1016/j.atosenv.2005.03.002
28. Maron PA, Mougel C, Lejon DP H, Carvalho E, Bizet K, Marck G, Cubito N, Lemanceau P, Ranjard L, Lejon DPH (2006) Temporal variability of airborne bacterial community structure in an urban area. Atmos Environ 40:8074–8080. doi:10.1016/j.atmosenv.2006.08.047
29. Nadkarni MA, Martin FE, Jacques NA, Hunter N (2002) Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology 148:257–266
30. O’Malley MA (2008) “Everything is everywhere: but the environment selects”: ubiquitous distribution and ecological determinism in microbial biogeography. Stud Hist Phil Biol Biomed Sci 39:314–325
31. 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. doi:10.1016/j.atmosenv.2006.02.029
32. Peres-Neto PR, Jackson DA, Somers KM (2005) How many principal components? stopping rules for determining the number of non-trivial axes revisited. Comput Stat Data Anal 49:974–997. doi:10.1016/j.csda.2004.06.015
33. Polymenakou PN (2012) Atmosphere: a source of pathogenic or beneficial microbes? Atmosphere (Basel) 3:87–102. doi:10.3390/atmos3010087
34. Rinsoz T, Duquenne P, Greff-Mirguet G, Oppliger A (2008) Application of real-time PCR for total airborne bacterial assessment: comparison with epifluorescence microscopy and culture-dependent methods. Atmos Environ 42:6767–6774. doi:10.1016/j.atmosenv.2008.05.018
35. Sánchez de la Campa A, García-Salamanca A, Solano J, de la Rosa J, Ramos J-L (2013) Chemical and microbiological characterization of atmospheric particulate matter during an intense African dust event in Southern Spain. Environ Sci Technol 47:3630–3638. doi:10.1021/es3051235
36. Scherer P, Sahm H (1981) Influence of sulphur-containing compounds on the growth of Methanosarcina barkeri in a defined medium. Eur J Appl Microbiol Biotechnol 12:28–35. doi:10.1007/BF00508115
37. Schwartz J, Laden F, Zanobetti A (2002) The concentration-response relation between PM2.5 and daily deaths. Environ Health Perspect 110:1025–1029
38. Smith DJ, Jaffe DA, Birmele MN, Griffin DW, Schuerger AC, Hee J, Roberts MS (2012) Free tropospheric transport of microorganisms from Asia to North America. Microb Ecol 64:973–985. doi:10.1007/s00248-012-0088-9
39. Squizzato S, Masiol M, Innocente E, Pecorari E, Rampazzo G, Pavoni B (2012) A procedure to assess local and long-range transport contributions to PM2.5 and secondary inorganic aerosol. J Aerosol Sci 46:64–76. doi:10.1016/j.jaerosci.2011.12.001
40. Team RDC (2008) R: A language and environment for statistical computing
41. Vaïtilingom M, Attard E, Gaiani N, Sancelme M, Deguillaume L, Flossmann AI, Amato P, Delort A-M (2012) Long-term features of cloud microbiology at the puy de Dôme (France). Atmos Environ 56:88–100. doi:10.1016/j.atmosenv.2012.03.072
42. Wainwright M (2003) Microorganisms cultured from stratospheric air samples obtained at 41 km. FEMS Microbiol Lett 218:161–165. doi:10.1016/S0378-1097(02)01138-2
43. 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 5261–5267. doi:10.1128/AEM.00062-07