Seasonal Variations in the Characteristics of Microbial Community Structure and Diversity in Atmospheric Particulate Matter from Clean Days and Smoggy Days in Beijing

Abstract

Microorganisms are an important part of atmospheric particulate matter and are closely related to human health. In this paper, the variations in the characteristics of the chemical components and bacterial communities in PM10 and PM2.5 grouped according to season, pollution degree, particle size, and winter heating stage were studied. The influence of environmental factors on community structure was also analyzed. The results showed that seasonal variations were significant. NO3 contributed the most to the formation of particulate matter in spring and winter, while SO42− contributed the most in summer and autumn. The community structures in summer and autumn were similar, while the community structure in spring was significantly different. The dominant phyla were similar among seasons, but their proportions were different. The dominant genera were no-rank_c_Cyanobacteria, Acidovorax, Escherichia-Shigella and Sphingomonas in spring; Massilia, Bacillus, Acinetobacter, Rhodococcus, and Brevibacillus in summer and autumn; and Rhodococcus in winter. The atmospheric microorganisms in Beijing mainly came from soil, water, and plants. The few pathogens detected were mainly affected by the microbial source on the sampling day, regardless of pollution level. RDA (redundancy analysis) showed that the bacterial community was positively correlated with the concentration of particulate matter and that the wind speed in spring was positively correlated with NO3 levels, NH4+ levels, temperature, and relative humidity in summer and autumn, but there was no clear consistency among winter samples. This study comprehensively analyzed the variations in the characteristics of the airborne bacterial community in Beijing over one year and provided a reference for understanding the source, mechanism, and assessment of the health effects of different air qualities.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Data Availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

Code Availability

Not applicable.

References

  1. 1.

    Pui DYH, Chen S-C, Zuo Z (2014) PM2.5 in China: measurements, sources, visibility and health effects, and mitigation. Particuology 13:1–26. https://doi.org/10.1016/j.partic.2013.11.001

    CAS  Article  Google Scholar 

  2. 2.

    Sun Y, Jiang Q, Wang Z, Fu P, Li J, Yang T, Yin Y (2014) Investigation of the sources and evolution processes of severe haze pollution in Beijing in January 2013. J Geophys Res Atmos 119:4380–4398. https://doi.org/10.1002/2014JD021641

    Article  Google Scholar 

  3. 3.

    Billet S, Landkocz Y, Martin PJ, Verdin A, Ledoux F, Lepers C, André V, Cazier F, Sichel F, Shirali P, Gosset P, Courcot D (2018) Chemical characterization of fine and ultrafine PM, direct and indirect genotoxicity of PM and their organic extracts on pulmonary cells. J Environ Sci 71:168–178. https://doi.org/10.1016/j.jes.2018.04.022

    Article  Google Scholar 

  4. 4.

    Dong X, Liu D, Gao S (2013) Seasonal variations of atmospheric heterocyclic aromatic amines in Beijing, China. Atmos Res 120–121:287–297. https://doi.org/10.1016/j.atmosres.2012.09.010

    CAS  Article  Google Scholar 

  5. 5.

    Calvo AI, Alves C, Castro A, Pont V, Vicente AM, Fraile R (2013) Research on aerosol sources and chemical composition: past, current and emerging issues. Atmos Res 120–121:1–28. https://doi.org/10.1016/j.atmosres.2012.09.021

    CAS  Article  Google Scholar 

  6. 6.

    Romano S, Becagli S, Lucarelli F, Rispoli G, Perrone MR (2020) Airborne bacteria structure and chemical composition relationships in winter and spring PM10 samples over southeastern Italy. Sci Total Environ 730:138899. https://doi.org/10.1016/j.scitotenv.2020.138899

    CAS  Article  PubMed  Google Scholar 

  7. 7.

    Kim K-H, Kabir E, Jahan SA (2018) Airborne bioaerosols and their impact on human health. J Environ Sci 67:23–35. https://doi.org/10.1016/j.jes.2017.08.027

    Article  Google Scholar 

  8. 8.

    Lindemann J, Constantinidou HA, Barchet WR, Upper CD (1982) Plants as sources of airborne bacteria, including ice nucleation-active bacteria. Appl Environ Microbiol 44:1059–1063. https://doi.org/10.1128/AEM.44.5.1059-1063.1982

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. 9.

    Lighthart B, Kim J (1989) Simulation of airborne microbial droplet transport. Appl Environ Microbiol 55:2349

    CAS  Article  Google Scholar 

  10. 10.

    Gao M, Jia R, Qiu T, Han M, Wang X (2017) Size-related bacterial diversity and tetracycline resistance gene abundance in the air of concentrated poultry feeding operations. Environ Pollut 220:1342–1348. https://doi.org/10.1016/j.envpol.2016.10.101

    CAS  Article  PubMed  Google Scholar 

  11. 11.

    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. https://doi.org/10.1016/j.atmosenv.2012.01.005

    CAS  Article  Google Scholar 

  12. 12.

    Maron P-A, Lejon DPH, 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. https://doi.org/10.1016/j.atmosenv.2005.03.002

    CAS  Article  Google Scholar 

  13. 13.

    Wang B, Li Y, Xie Z, Du S, Zeng X, Hou J, Ma T (2020) Characteristics of microbial activity in atmospheric aerosols and its relationship to chemical composition of PM2.5 in Xi’an. China. J Aerosol Sci 146:105572. https://doi.org/10.1016/j.jaerosci.2020.105572

    CAS  Article  Google Scholar 

  14. 14.

    Gandolfi I, Bertolini V, Bestetti G, Ambrosini R, Innocente E, Rampazzo G, Papacchini M, Franzetti A (2015) Spatio-temporal variability of airborne bacterial communities and their correlation with particulate matter chemical composition across two urban areas. Appl Microbiol Biotechnol 99:4867–4877. https://doi.org/10.1007/s00253-014-6348-5

    CAS  Article  PubMed  Google Scholar 

  15. 15.

    Bowers RM, Sullivan AP, Costello EK, Collett JL, Knight R, Fierer N (2011) Sources of bacteria in outdoor air across cities in the midwestern United States. Appl Environ Microbiol 77:6350. https://doi.org/10.1128/AEM.05498-11

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. 16.

    Cao C, Jiang W, Wang B, Fang J, Lang J, Tian G, Jiang J, Zhu TF (2014) Inhalable microorganisms in Beijing’s PM2.5 and PM10 pollutants during a severe smog event. Environ Sci Technol 48:1499–1507. https://doi.org/10.1021/es4048472

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  17. 17.

    Shi W, Li M, Wei G, Tian R, Li C, Wang B, Lin R, Shi C, Chi X, Zhou B, Gao Z (2019) The occurrence of potato common scab correlates with the community composition and function of the geocaulosphere soil microbiome. Microbiome 7:14. https://doi.org/10.1186/s40168-019-0629-2

    Article  PubMed  PubMed Central  Google Scholar 

  18. 18.

    Chan CK, Yao X (2008) Air pollution in mega cities in China. Atmos Environ 42:1–42. https://doi.org/10.1016/j.atmosenv.2007.09.003

    CAS  Article  Google Scholar 

  19. 19.

    Yue DL, Hu M, Wu ZJ, Guo S, Wen MT, Nowak A, Wehner B, Wiedensohler A, Takegawa N, Kondo Y, Wang XS, Li YP, Zeng LM, Zhang YH (2010) Variation of particle number size distributions and chemical compositions at the urban and downwind regional sites in the Pearl River Delta during summertime pollution episodes. Atmos Chem Phys 10:9431–9439. https://doi.org/10.5194/acp-10-9431-2010

    CAS  Article  Google Scholar 

  20. 20.

    Wang T, Gao T, Zhang H, Ge M, Lei H, Zhang P, Zhang P, Lu C, Liu C, Zhang H, Zhang Q, Liao H, Kan H, Feng Z, Zhang Y, Qie X, Cai X, Li M, Liu L, Tong S (2019) Review of Chinese atmospheric science research over the past 70 years: atmospheric physics and atmospheric environment. Sci China Earth Sci 62:1903–1945. https://doi.org/10.1007/s11430-019-9536-1

    Article  Google Scholar 

  21. 21.

    Huang L, Wang G (2014) Chemical characteristics and source apportionment of atmospheric particles during heating period in Harbin, China. J Environ Sci 26:2475–2483. https://doi.org/10.1016/j.jes.2014.04.008

    Article  Google Scholar 

  22. 22.

    Xie Y, Wu D, Zhu S (2021) Can new energy vehicles subsidy curb the urban air pollution? Empirical evidence from pilot cities in China. Sci Total Environ 754:142232. https://doi.org/10.1016/j.scitotenv.2020.142232

    CAS  Article  PubMed  Google Scholar 

  23. 23.

    Tan T, Hu M, Li M, Guo Q, Wu Y, Fang X, Gu F, Wang Y, Wu Z (2018) New insight into PM2.5 pollution patterns in Beijing based on one-year measurement of chemical compositions. Sci Total Environ 621:734–743. https://doi.org/10.1016/j.scitotenv.2017.11.208

    CAS  Article  PubMed  Google Scholar 

  24. 24.

    Wang H, Zhuang Y, Wang Y, Sun Y, Yuan H, Zhuang G, Hao Z (2008) Long-term monitoring and source apportionment of PM2.5/PM10 in Beijing, China. J Environ Sci 20:1323–1327. https://doi.org/10.1016/S1001-0742(08)62228-7

    CAS  Article  Google Scholar 

  25. 25.

    Sun Y, Xu S, Zheng D, Li J, Tian H, Wang Y (2018) Effects of haze pollution on microbial community changes and correlation with chemical components in atmospheric particulate matter. Sci Total Environ 637–638:507–516. https://doi.org/10.1016/j.scitotenv.2018.04.203

    CAS  Article  PubMed  Google Scholar 

  26. 26.

    Gao B, Ouyang W, Cheng H, Xu Y, Lin C, Chen J (2019) Interactions between rainfall and fine particulate matter investigated by simultaneous chemical composition measurements in downtown Beijing. Atmos Environ 218:117000. https://doi.org/10.1016/j.atmosenv.2019.117000

    CAS  Article  Google Scholar 

  27. 27.

    He K, Yang F, Ma Y, Zhang Q, Yao X, Chan CK, Cadle S, Chan T, Mulawa P (2001) The characteristics of PM2.5 in Beijing. China Atmos Environ 35:4959–4970. https://doi.org/10.1016/S1352-2310(01)00301-6

    CAS  Article  Google Scholar 

  28. 28.

    Cui J, Lang J, Chen T, Mao S, Cheng S, Wang Z, Cheng N (2019) A framework for investigating the air quality variation characteristics based on the monitoring data: case study for Beijing during 2013–2016. J Environ Sci 81:225–237. https://doi.org/10.1016/j.jes.2019.01.009

    Article  Google Scholar 

  29. 29.

    Lang J, Zhang Y, Zhou Y, Cheng S, Chen D, Guo X, Chen S, Li X, Xing X, Wang H (2017) Trends of PM2.5 and chemical composition in Beijing, 2000–2015. Aerosol Air Qual Res 17:412–425. https://doi.org/10.4209/aaqr.2016.07.0307

    CAS  Article  Google Scholar 

  30. 30.

    Su J, Zhao P, Ding J, Du X, Dou Y (2021) Insights into measurements of water-soluble ions in PM2.5 and their gaseous precursors in Beijing. J Environ Sci 102:123–137. https://doi.org/10.1016/j.jes.2020.08.031

    Article  Google Scholar 

  31. 31.

    Liu Z, Xie Y, Hu B, Wen T, Xin J, Li X, Wang Y (2017) Size-resolved aerosol water-soluble ions during the summer and winter seasons in Beijing: Formation mechanisms of secondary inorganic aerosols. Chemosphere 183:119–131. https://doi.org/10.1016/j.chemosphere.2017.05.095

    CAS  Article  PubMed  Google Scholar 

  32. 32.

    Du P, Du R, Ren W, Lu Z, Zhang Y, Fu P (2018) Variations of bacteria and fungi in PM2.5 in Beijing. China Atmos Environ 172:55–64. https://doi.org/10.1016/j.atmosenv.2017.10.048

    CAS  Article  Google Scholar 

  33. 33.

    Allen EB, Brown JS, Allen MF (2001) Restoration of animal, plant, and microbial diversity. In: Levin SA (ed) Encyclopedia of Biodiversity. Elsevier, New York, pp 185–202. https://doi.org/10.1016/B978-0-12-384719-5.00419-6

  34. 34.

    Ofek M, Hadar Y, Minz D (2012) Ecology of root colonizing Massilia (Oxalobacteraceae). PLoS ONE 7:e40117. https://doi.org/10.1371/journal.pone.0040117

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. 35.

    An S, Couteau C, Luo F, Neveu J, DuBow MS (2013) Bacterial diversity of surface sand samples from the Gobi and Taklamaken deserts. Microb Ecol 66:850–860. https://doi.org/10.1007/s00248-013-0276-2

    Article  PubMed  Google Scholar 

  36. 36.

    Zhang W, Wang H, Zhang R, Yu X-Z, Qian P-Y, Wong MH (2010) Bacterial communities in PAH contaminated soils at an electronic-waste processing center in China. Ecotoxicology 19:96–104. https://doi.org/10.1007/s10646-009-0393-3

    CAS  Article  PubMed  Google Scholar 

  37. 37.

    Cheng W, Zhang J, Wang Z, Wang M, Xie S (2014) Bacterial communities in sediments of a drinking water reservoir. Ann Microbiol 64:875–878. https://doi.org/10.1007/s13213-013-0712-z

    CAS  Article  Google Scholar 

  38. 38.

    Blatny JM, Ho J, Skogan G, Fykse EM, Aarskaug T, Waagen V (2011) Airborne Legionella bacteria from pulp waste treatment plant: aerosol particles characterized as aggregates and their potential hazard. Aerobiologia 27:147–162. https://doi.org/10.1007/s10453-010-9184-9

    Article  Google Scholar 

  39. 39.

    Xu L, Zhou Z, Zhu L, Han Y, Lin Z, Feng W, Liu Y, Shuai X, Chen H (2020) Antibiotic resistance genes and microcystins in a drinking water treatment plant. Environ Pollut 258:113718. https://doi.org/10.1016/j.envpol.2019.113718

    CAS  Article  PubMed  Google Scholar 

  40. 40.

    Wei K, Zou Z, Zheng Y, Li J, Shen F, Wu C, Wu Y, Hu M, Yao M (2016) Ambient bioaerosol particle dynamics observed during haze and sunny days in Beijing. Sci Total Environ 550:751–759. https://doi.org/10.1016/j.scitotenv.2016.01.137

    CAS  Article  PubMed  Google Scholar 

  41. 41.

    Yoo K, Lee TK, Choi EJ, Yang J, Shukla SK, Hwang S, Park J (2017) Molecular approaches for the detection and monitoring of microbial communities in bioaerosols: a review. J Environ Sci 51:234–247. https://doi.org/10.1016/j.jes.2016.07.002

    Article  Google Scholar 

  42. 42.

    Jin L, Luo X, Fu P, Li X (2017) Airborne particulate matter pollution in urban China: a chemical mixture perspective from sources to impacts. Natl Sci Rev 4:593–610. https://doi.org/10.1093/nsr/nww079

    CAS  Article  Google Scholar 

  43. 43.

    Sun X, Li D, Li B, Sun S, Yabo SD, Geng J, Ma L, Qi H (2020) Exploring the disparity of inhalable bacterial communities and antibiotic resistance genes between hazy days and non-hazy days in a cold megacity in Northeast China. J Hazard Mater 398:122984. https://doi.org/10.1016/j.jhazmat.2020.122984

    CAS  Article  PubMed  Google Scholar 

  44. 44.

    Zhai Y, Li X, Wang T, Wang B, Li C, Zeng G (2018) A review on airborne microorganisms in particulate matters: composition, characteristics and influence factors. Environ Int 113:74–90. https://doi.org/10.1016/j.envint.2018.01.007

    Article  PubMed  Google Scholar 

  45. 45.

    Savage D, Barbetti MJ, MacLeod WJ, Salam MU, Renton M (2012) Mobile traps are better than stationary traps for surveillance of airborne fungal spores. Crop Prot 36:23–30. https://doi.org/10.1016/j.cropro.2012.01.015

    Article  Google Scholar 

  46. 46.

    Xu C, Wei M, Chen J, Wang X, Zhu C, Li J, Zheng L, Sui G, Li W, Wang W, Zhang Q, Mellouki A (2017) Bacterial characterization in ambient submicron particles during severe haze episodes at Ji’nan, China. Sci Total Environ 580:188–196. https://doi.org/10.1016/j.scitotenv.2016.11.145

    CAS  Article  PubMed  Google Scholar 

  47. 47.

    Li X, Rui J, Mao Y, Yannarell A, Mackie R (2014) Dynamics of the bacterial community structure in the rhizosphere of a maize cultivar. Soil Biol Biochem 68:392–401. https://doi.org/10.1016/j.soilbio.2013.10.017

    CAS  Article  Google Scholar 

  48. 48.

    Wei M, Liu H, Chen J, Xu C, Li J, Xu P, Sun Z (2020) Effects of aerosol pollution on PM25-associated bacteria in typical inland and coastal cities of northern China during the winter heating season. Environ Pollut 262:114188. https://doi.org/10.1016/j.envpol.2020.114188

    CAS  Article  PubMed  Google Scholar 

Download references

Funding

This study was supported by the National Natural Science Foundation of China (Grant Nos. 51178048, 51378064 and 51678054).

Author information

Affiliations

Authors

Contributions

Conceptualization: [Yujiao Sun]; Project administration: [Yujiao Sun]; Formal analysis and investigation: [Yujia Huang], [Shangwei Xu], [Jie Li], [Meng Yin]; Data Curation: [Yujia Huang], [Shangwei Xu]; Writing—original draft preparation: [Yujia Huang], [Shangwei Xu]; Writing—review and editing: [Yujia Huang]; Funding acquisition: [Yujiao Sun]; Resources: [Yujiao Sun], [Hezhong Tian]; Supervision: [Yujiao Sun].

Corresponding authors

Correspondence to Shangwei Xu or Hezhong Tian.

Ethics declarations

Ethics Approval and Consent to Participate

The authors declare that the work described was an original research that has not been published previously, and not under consideration for publication elsewhere, in whole or in part. The content and authorship of the submitted manuscript has been approved by all authors, and that all prevailing local, national, and international regulations and conventions, and normal scientific ethical practices, have been respected. Informed consent was obtained from all individual participants included in the study.

Consent for Publication

Informed consent was obtained from all individual participants included in the study.

Competing Interests

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 142 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Sun, Y., Huang, Y., Xu, S. et al. Seasonal Variations in the Characteristics of Microbial Community Structure and Diversity in Atmospheric Particulate Matter from Clean Days and Smoggy Days in Beijing. Microb Ecol (2021). https://doi.org/10.1007/s00248-021-01764-1

Download citation

Keywords

  • Atmospheric particulate matter
  • Microbial community
  • Smog pollution
  • Seasonal variation
  • Pathogen