Abstract
The purpose of this study was to investigate the association among polycyclic aromatic hydrocarbons (PAHs) exposure and air pollutants and the diversity of microbiota. Daily average concentrations of six common air pollutants were obtained from China National Environmental Monitoring Centre. The PAHs exposure levels were evaluated by external and internal exposure detection methods, including monitoring atmospheric PAHs and urinary hydroxyl-polycyclic aromatic hydrocarbon (OH-PAH) metabolite levels. We analyzed the diversity of environmental and commensal bacterial communities with 16S rRNA gene sequencing and performed functional enrichment with Phylogenetic Investigation of Communities by Reconstruction of Unobserved States (PICRUSt) and Kyoto Encyclopedia of Genes and Genomes (KEGG). Correlation analysis and logistic regression modeling were conducted to evaluate the relationship of PAHs levels with air pollutants and microbial diversity. Correlation analysis found that the concentrations of atmospheric PAHs were significantly positively correlated with those of PM10, NO2, and SO2. There also was a positive correlation between the abundance of the genus Micrococcus (Actinobacteria) and high molecular weight PAHs, and Bacillus, such as genera and low molecular weight PAHs in the atmosphere. Logistic regression showed that the level of urinary 1-OHPyrene was associated with childhood asthma after sex and age adjustment. The level of urinary 1-OHPyrene was significantly positively correlated with that of PM2.5 and PM10. In addition, the level of 1-OHPyrene was positively correlated with oral Prevotella-7 abundance. Functional enrichment analysis demonstrated that PAHs exposure may disturb signaling pathways by the imbalance of commensal microbiota, such as purine metabolism, pyrimidine metabolites, lipid metabolism, and one carbon pool by folate, which may contribute to public health issues. Our results confirmed that atmospheric PAHs and urinary 1-OHPyrene were correlated with part of six common air pollutants and indicated that PAHs pollution may alter both environmental and commensal microbiota communities associated with health-related problems. The potential health and environmental impacts of PAHs should be further explored.
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The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
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Change history
30 March 2021
A Correction to this paper has been published: https://doi.org/10.1007/s00244-021-00822-6
References
Alegbeleye OO, Opeolu BO, Jackson V (2017) Bioremediation of polycyclic aromatic hydrocarbon (PAH) compounds: (acenaphthene and fluorene) in water using indigenous bacterial species isolated from the Diep and Plankenburg rivers, Western Cape, South Africa. Braz J Microbiol 48:314–325. https://doi.org/10.1016/j.bjm.2016.07.027
Benedek T, Vajna B, Tancsics A, Marialigeti K, Lanyi S, Mathe I (2013) Remarkable impact of PAHs and TPHs on the richness and diversity of bacterial species in surface soils exposed to long-term hydrocarbon pollution. World J Microbiol Biotechnol 29:1989–2002. https://doi.org/10.1007/s11274-013-1362-9
Bibi N, Hamayun M, Khan SA et al (2018) Anthracene biodegradation capacity of newly isolated rhizospheric bacteria Bacillus cereus S13. PLoS ONE 13:e0201620. https://doi.org/10.1371/journal.pone.0201620
Burton A (2009) Children’s health: methylation links prenatal PAH exposure to asthma. Environ Health Perspect 117:A195. https://doi.org/10.1289/ehp.117-a195
Cakmak S, Hebbern C, Cakmak JD, Dales RE (2017) The influence of polycyclic aromatic hydrocarbons on lung function in a representative sample of the Canadian population. Environ Pollut 228:1–7. https://doi.org/10.1016/j.envpol.2017.05.013
CDC Centers for Disease Control and Prevention U (2009) The fourth national report on human exposure to environmental chemicals 455–457
Chen L, Hu G, Fan R, Lv Y, Dai Y, Xu Z (2018) Association of PAHs and BTEX exposure with lung function and respiratory symptoms among a nonoccupational population near the coal chemical industry in Northern China. Environ Int 120:480–488. https://doi.org/10.1016/j.envint.2018.08.004
Chevron Cottin N, Merlin G (2007) Study of pyrene biodegradation capacity in two types of solid media. Sci Total Environ 380:116–123. https://doi.org/10.1016/j.scitotenv.2007.03.016
Delfino RJ (2002) Epidemiologic evidence for asthma and exposure to air toxics: linkages between occupational, indoor, and community air pollution research. Environ Health Perspect 110(Suppl 4):573–589. https://doi.org/10.1289/ehp.02110s4573
Ducker GS, Rabinowitz JD (2017) One-carbon metabolism in health and disease. Cell Metab 25:27–42. https://doi.org/10.1016/j.cmet.2016.08.009
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. https://doi.org/10.1093/bioinformatics/btr381
García-Suástegui WA, Huerta-Chagoya A, Carrasco-Colín KL et al (2011) Seasonal variations in the levels of PAH-DNA adducts in young adults living in Mexico City. Mutagenesis 26:385–391. https://doi.org/10.1093/mutage/geq104
Gunter MJ, Divi RL, Kulldorff M et al (2007) Leukocyte polycyclic aromatic hydrocarbon-DNA adduct formation and colorectal adenoma. Carcinogenesis 28:1426–1429. https://doi.org/10.1093/carcin/bgm022
Guo Y, Rene ER, Wang J, Ma W (2020) Biodegradation of polyaromatic hydrocarbons and the influence of environmental factors during the co-composting of sewage sludge and green forest waste. Bioresour Technol 297:122434. https://doi.org/10.1016/j.biortech.2019.122434
Hew KM et al (2015) Childhood exposure to ambient polycyclic aromatic hydrocarbons is linked to epigenetic modifications and impaired systemic immunity in T cells. Clin Exp Allergy 45:238–248. https://doi.org/10.1111/cea.12377
Hubbard HF, Sobus JR, Pleil JD, Madden MC, Tabucchi S (2009) Application of novel method to measure endogenous VOCs in exhaled breath condensate before and after exposure to diesel exhaust. J Chromatogr B Analyt Technol Biomed Life Sci 877:3652–3658. https://doi.org/10.1016/j.jchromb.2009.09.008
Jang E, Alam MS, Harrison RM (2013) Source apportionment of polycyclic aromatic hydrocarbons in urban air using positive matrix factorization and spatial distribution analysis. Atmos Environ 79:271–285. https://doi.org/10.1016/j.atmosenv.2013.06.056
Johnsen AR, Wick LY, Harms H (2005) Principles of microbial PAH-degradation in soil. Environ Pollut 133:71–84. https://doi.org/10.1016/j.envpol.2004.04.015
Jongeneelen FJ (2001) Benchmark guideline for urinary 1-hydroxypyrene as biomarker of occupational exposure to polycyclic aromatic hydrocarbons. Ann Occup Hyg 45:3–13
Jung KH, Perzanowski M, Rundle A et al (2014) Polycyclic aromatic hydrocarbon exposure, obesity and childhood asthma in an urban cohort. Environ Res 128:35–41. https://doi.org/10.1016/j.envres.2013.12.002
Keir JLA, Cakmak S, Blais JM, White PA (2020) The influence of demographic and lifestyle factors on urinary levels of PAH metabolites-empirical analyses of Cycle 2 (2009–2011) CHMS data. J Expo Sci Environ Epidemiol. https://doi.org/10.1038/s41370-020-0208-4
Khanna P, Goyal D, Khanna S (2012) Characterization of pyrene utilizing Bacillus spp. from crude oil contaminated soil. Braz J Microbiol 43:606–617. https://doi.org/10.1590/S1517-83822012000200024
Krewski D, Jerrett M, Burnett RT et al (2009) Extended follow-up and spatial analysis of the American Cancer Society study linking particulate air pollution and mortality. Res Rep Health Eff Inst 140:115–136
Larsen JM (2017) The immune response to Prevotella bacteria in chronic inflammatory disease. Immunology 151:363–374. https://doi.org/10.1111/imm.12760
Lopes MP et al (2020) Prevotella intermedia and periodontitis are associated with severe asthma. J Periodontol 91:46–54. https://doi.org/10.1002/JPER.19-0065
Loureiro CC, Oliveira AS, Santos M, Rudnitskaya A, Todo-Bom A, Bousquet J, Rocha SM (2016) Urinary metabolomic profiling of asthmatics can be related to clinical characteristics. Allergy 71:1362–1365. https://doi.org/10.1111/all.12935
Matalova P, Urbanek K, Anzenbacher P (2016) Specific features of pharmacokinetics in children. Drug Metab Rev 48:70–79. https://doi.org/10.3109/03602532.2015.1135941
McClean MD, Rinehart RD, Ngo L, Eisen EA, Kelsey KT, Wiencke JK, Herrick RF (2004) Urinary 1-hydroxypyrene and polycyclic aromatic hydrocarbon exposure among asphalt paving workers. Ann Occup Hyg 48:565–578. https://doi.org/10.1093/annhyg/meh044
Miettinen M, Leskinen A, Abbaszade G et al (2019) PM2.5 concentration and composition in the urban air of Nanjing, China: Effects of emission control measures applied during the 2014 Youth Olympic Games. Sci Total Environ 652:1–18. https://doi.org/10.1016/j.scitotenv.2018.10.191
Mu G, Fan L, Zhou Y et al (2019) Personal exposure to PM2.5-bound polycyclic aromatic hydrocarbons and lung function alteration: Results of a panel study in China. Sci Total Environ 684:458–465. https://doi.org/10.1016/j.scitotenv.2019.05.328
Mumtaz MM, George JD, Gold KW, Cibulas W, DeRosa CT (1996) ATSDR evaluation of health effects of chemicals. IV. Polycyclic aromatic hydrocarbons (PAHs): Understanding a complex problem. Toxicol Ind Health 12:742–971. https://doi.org/10.1177/074823379601200601
Niu HY, Wang H, Wang GH, Liu SS, Gao SX, Wang LS (2005) Source identification and pollution evaluation of polycyclic aromatic hydrocarbons in atmospheric aerosols in Nanjing City China. J Environ Sci-China 25(5):544–548 [in Chinese]
Noverr MC, Huffnagle GB (2005) The ‘microflora hypothesis’ of allergic diseases. Clin Exp Allergy 35:1511–1520
Nwachukwu SC, James P, Gurney TR (2001) Inorganic nutrient utilisation by “adapted” Pseudomonas putida strain used in the bioremediation of agricultural soil polluted with crude petroleum. J Environ Biol 22:153–162
Olowomofe TO, Oluyege JO, Aderiye BI, Oluwole OA (2019) Degradation of poly aromatic fractions of crude oil and detection of catabolic genes in hydrocarbon-degrading bacteria isolated from Agbabu bitumen sediments in Ondo State. AIMS Microbiol 5:308–323. https://doi.org/10.3934/microbiol.2019.4.308
Parks DH, Tyson GW, Hugenholtz P, Beiko RG (2014) STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30:3123–3124. https://doi.org/10.1093/bioinformatics/btu494
Parvez F, Lauer FT, Factor-Litvak P et al (2019) Assessment of arsenic and polycyclic aromatic hydrocarbon (PAH) exposures on immune function among males in Bangladesh. PLoS ONE 14:e0216662. https://doi.org/10.1371/journal.pone.0216662
Perera F, Tang WY, Herbstman J, Tang D, Levin L, Miller R, Ho SM (2009) Relation of DNA methylation of 5′-CpG island of ACSL3 to transplacental exposure to airborne polycyclic aromatic hydrocarbons and childhood asthma. PLoS ONE 4:e4488. https://doi.org/10.1371/journal.pone.0004488
Ribière C, Peyret P, Parisot N et al (2016) Oral exposure to environmental pollutant benzo[a]pyrene impacts the intestinal epithelium and induces gut microbial shifts in murine model. Sci Rep 6:31027. https://doi.org/10.1038/srep31027
Ron-Harel N, Notarangelo G, Ghergurovich JM et al (2018) Defective respiration and one-carbon metabolism contribute to impaired naive T cell activation in aged mice. Proc Natl Acad Sci USA 115:13347–13352. https://doi.org/10.1073/pnas.1804149115
Roslund MI, Grönroos M, Rantalainen AL et al (2018) Half-lives of PAHs and temporal microbiota changes in commonly used urban landscaping materials. PeerJ 6:e4508. https://doi.org/10.7717/peerj.4508
Roslund MI, Rantala S, Oikarinen S et al (2019) Endocrine disruption and commensal bacteria alteration associated with gaseous and soil PAH contamination among daycare children. Environ Int 130:104894. https://doi.org/10.1016/j.envint.2019.06.004
Shen M, Liu G, Yin H, Zhou L (2020) Distribution, sources and health risk of PAHs in urban air-conditioning dust from Hefei, East China. Ecotoxicol Environ Saf 194:110442. https://doi.org/10.1016/j.ecoenv.2020.110442
Shi GL, Zhou XY, Jiang SY et al (2015) Further insights into the composition, source, and toxicity of PAHs in size-resolved particulate matter in a megacity in China. Environ Toxicol Chem 34:480–487. https://doi.org/10.1002/etc.2809
Skalska K, Lewandowska AU, Staniszewska M, Reindl A, Witkowska A, Falkowska L (2019) Sources, deposition flux and carcinogenic potential of PM2.5-bound polycyclic aromatic hydrocarbons in the coastal zone of the Baltic Sea (Gdynia, Poland). Air Qual Atmos Health 12:1291–1301. https://doi.org/10.1007/s11869-019-00741-5
Sobus JR, McClean MD, Herrick RF, Waidyanatha S, Nylander-French LA, Kupper LL, Rappaport SM (2009) Comparing urinary biomarkers of airborne and dermal exposure to polycyclic aromatic compounds in asphalt-exposed workers. Ann Occup Hyg 53:561–571. https://doi.org/10.1093/annhyg/mep042
Sowada J, Schmalenberger A, Ebner I, Luch A, Tralau T (2014) Degradation of benzo[a]pyrene by bacterial isolates from human skin. FEMS Microbiol Ecol 88:129–139. https://doi.org/10.1111/1574-6941.12276
Su D, Li PJ, Frank S, Xiong XZ (2006) Biodegradation of benzo[a]pyrene in soil by Mucor sp. SF06 and Bacillus sp. SB02 co-immobilized on vermiculite. J Environ Sci 18:1204–1209. https://doi.org/10.1016/s1001-0742(06)60063-6
Tsapakis M, Stephanou EG (2015) Occurrence of gaseous and particulate polycyclic aromatic hydrocarbons in the urban atmosphere: study of sources and ambient temperature effect on the gas/particle concentration and distribution. Environ Pollut 133:147–156
Wang GH, Huang LM, Zhao X, Niu HY, Dai ZX (2006) Aliphatic and polycyclic aromatic hydrocarbons of atmospheric aerosols in five locations of Nanjing urban area, China. Atmos Res 81:54–66. https://doi.org/10.1016/j.atmosres.2005.11.004
Wendell SG, Baffi C, Holguin F (2014) Fatty acids, inflammation, and asthma. J Allergy Clin Immunol 133:1255–1264. https://doi.org/10.1016/j.jaci.2013.12.1087
Worldwide variation in prevalence of symptoms of asthma, allergic rhinoconjunctivitis, and atopic eczema: ISAAC. The International Study of Asthma and Allergies in Childhood (ISAAC) Steering Committee (1998) Lancet 351:1225–1232
Xu N, Tan GC, Wang HY, Gai XP (2016) Effect of biochar additions to soil on nitrogen leaching, microbial biomass and bacterial community structure. Eur J Soil Biol 74:1–8. https://doi.org/10.1016/j.ejsobi.2016.02.004
Yang M, Vousden KH (2016) Serine and one-carbon metabolism in cancer. Nat Rev Cancer 16:650–662. https://doi.org/10.1038/nrc.2016.81
Yang L, Wang WC, Lung SC et al (2017) Polycyclic aromatic hydrocarbons are associated with increased risk of chronic obstructive pulmonary disease during haze events in China. Sci Total Environ 574:1649–1658. https://doi.org/10.1016/j.scitotenv.2016.08.211
Yu Y, Li Q, Wang H, Wang B, Wang X, Ren A, Tao S (2015) Risk of human exposure to polycyclic aromatic hydrocarbons: a case study in Beijing, China. Environ Pollut 205:70–77. https://doi.org/10.1016/j.envpol.2015.05.022
Yu M, Jia HM, Cui FX, Yang Y, Zhao Y, Yang MH, Zou ZM (2017) The effect of chinese herbal medicine formula mKG on allergic asthma by regulating lung and plasma metabolic alternations. Int J Mol Sci. https://doi.org/10.3390/ijms18030602
Zhang LP, Zhang X, Duan HW et al (2017) Long-term exposure to diesel engine exhaust induced lung function decline in a cross sectional study. Ind Health 55:13–26. https://doi.org/10.2486/indhealth.2016-0031
Funding
The National Natural Science Foundation of China (81728018 and 81530088), Natural Science Foundation of Jiangsu Province (BK20161571), Natural Science Foundation of the Higher Education Institution of Jiangsu Province (16KJA330002), and the open project of the key laboratory of modern toxicology of ministry education Nanjing Medical University (NMUAMT201802) supported this work. The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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Jinye Hu and Yuling Bao have equal contributions to the work.
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Conceived and designed the experiments: QW and LL. Performed the experiments: JYH, YQZ, RO, MFS, LW, and SYC. Analyzed the data: JYH and QW. Contributed reagents/materials/analysis tools: YLB, ZZ, QW, and LL. wrote the paper: JYH. All the authors read and approved the final manuscript.
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The Nanjing Medical University Clinical Research Ethics Committee, Nanjing, China, reviewed and approved the protocols of this study. Informed consent was obtained from the participants for the use of samples in this study.
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Fig. S1
Geographic coordinates for the sampling point. The sampling point was located in the entrance of Nanjing Medical University, Jiangning District, Nanjing, China. The black star represented the sampling point. (PNG 202 kb)
Fig. S2
Comparison of microbial diversity between the asthmatic and control groups. A and B: represented alpha diversity with Chao and ACE indices. C: PLS-DA on OTU level. COMP1 represented the principle feature vector, and COMP2 represented the secondary feature vector. *P < 0.05, ***P < 0.001. (TIFF 767 kb)
Fig. S3
Correlations of differential bacteria on genus and inferred metagenomic functions. Spearman correlation was performed for differential oral microbiota (Prevotella-7 and Veillonella) and KEGG pathway abundance. The heatmap was drawn with RStudio (version 1.0.143). Significant squares were marked with *P < 0.05 and **P < 0.01. (TIFF 772 kb)
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Hu, J., Bao, Y., Zhu, Y. et al. The Preliminary Study on the Association Between PAHs and Air Pollutants and Microbiota Diversity. Arch Environ Contam Toxicol 79, 321–332 (2020). https://doi.org/10.1007/s00244-020-00757-4
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DOI: https://doi.org/10.1007/s00244-020-00757-4