Environmental Science and Pollution Research

, Volume 25, Issue 36, pp 36278–36286 | Cite as

Toxicity responses of bacterial community as a biological indicator after repeated exposure to lead (Pb) in the presence of decabromodiphenyl ether (BDE209)

  • Bo Liu
  • Rong Zhang
  • Xiaoqian Xia
  • Wei ZhangEmail author
  • Mengwen Gao
  • Qiang Lu
  • Kuangfei LinEmail author
Research Article


Continuous exposure of chemicals could cause various environmental impacts. Decabromodiphenyl ether (BDE209) and lead (Pb) can co-exist and are discharged simultaneously at e-waste recycling sites (EWRSs). Extensive concerns have been attracted by their toxic effects on soil microorganisms. Thus, by using high-throughput sequencing, this study explored bacterial community responses in a soil system after repeated Pb exposure in the presence of BDE209 in the laboratory during 90-day indoor incubation period. Gene sequencing of 16S rDNA performed on an Illumina MiSeq platform proved that one-off Pb exposure caused higher microbial abundance and community diversity. Additionally, both repetitive Pb treatment and exogenous BDE209 input could change bacterial community composition. Twenty-three different bacterial phyla were detected in the soil samples, while more than 90% of the sequences in each treatment belonged to a narrow variety. The sequence analyses elucidated that Proteobacteria, Acidobacteria, and Bacteroidetes were the top three dominant phyla. Our observations could provide a few insights into the ecological risks of Pb and BDE209 co-existed contamination in soils at EWRSs.


Pb BDE209 Repeated exposure Soil microorganism Bacterial community 


Funding information

The research was supported by the National Natural Science Foundation of China (41877124, 21737005, 51708223) and the Science and Technology Committee Research Program of Shanghai (17DZ1202304, 18DZ1204403).


  1. Chou HL, Chang YT, Liao YF, Lin CH (2013) Biodegradation of decabromodiphenyl ether (BDE-209) by bacterial mixed cultures in a soil/water system. Int Biodeterior Biodegrad 85:671–682CrossRefGoogle Scholar
  2. Deng D, Tam NF (2015) Isolation of microalgae tolerant to polybrominated diphenyl ethers (PBDEs) from wastewater treatment plants and their removal ability. Bioresour Technol 177:289–297CrossRefGoogle Scholar
  3. Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364CrossRefGoogle Scholar
  4. Gump BB, Yun S, Kannan K (2014) Polybrominated diphenyl ether (PBDE) exposure in children: possible associations with cardiovascular and psychological functions. Environ Res 132:244–250CrossRefGoogle Scholar
  5. Hendershot W, Lalande H, Duquette M (1993) Ion exchange and exchangeable cations. Soil sampling and methods of analysis. 19:167–176Google Scholar
  6. Jez E, Lestan D (2015) Prediction of blood lead levels in children before and after remediation of soil samples in the upper Meza Valley, Slovenia. J Hazard Mater 296:138–146CrossRefGoogle Scholar
  7. Jones DL, Willett VB (2006) Experimental evaluation of methods to quantify dissolved organic nitrogen (DON) and dissolved organic carbon (DOC) in soil. Soil Biol Biochem 38:991–999CrossRefGoogle Scholar
  8. Jones RT, Robeson MS, Lauber CL, Hamady M, Knight R, Fierer N (2009) A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME J 3:442–453CrossRefGoogle Scholar
  9. Kalyuzhnaya MG, Bowerman S, Lara JC, Lidstrom ME, Chistoserdova L (2006) Methylotenera mobilis gen. nov., sp nov., an obligately methylamine-utilizing bacterium within the family Methylophilaceae. Int J Syst Evol Microbiol 56:2819–2823CrossRefGoogle Scholar
  10. Kim YM, Nam IH, Murugesan K, Schmidt S, Crowley DE, Chang YS (2007) Biodegradation of diphenyl ether and transformation of selected brominated congeners by Sphingomonas sp PH-07. Appl Microbiol Biotechnol 77:187–194CrossRefGoogle Scholar
  11. Kong AY, Scow KM, Córdovakreylos AL, Holmes WE, Six J (2011) Microbial community composition and carbon cycling within soil microenvironments of conventional, low-input, and organic cropping systems. Soil Biol Biochem 43:20–30CrossRefGoogle Scholar
  12. Langford K, Scrimshaw M, Lester J (2007) The impact of process variables on the removal of PBDEs and NPEOs during simulated activated sludge treatment. Arch Environ Contam Toxicol 53:1–7CrossRefGoogle Scholar
  13. Ligi T, Oopkaup K, Truu M, Preem JK, Nõlvak H, Mitsch WJ, Ülo M, Truu J (2014) Characterization of bacterial communities in soil and sediment of a created riverine wetland complex using high-throughput 16S rRNA amplicon sequencing. Ecol Eng 72:56–66CrossRefGoogle Scholar
  14. Meijer SN, Harner T, Helm PA, Halsall CJ, Johnston AE, Jones KC (2001) Polychlorinated naphthalenes in U.K. soils: time trends, markers of source, and equilibrium status. Environ Sci Technol 35:4205–4213CrossRefGoogle Scholar
  15. Niu X, Liu C, Song X (2015) Simulation research on the natural degradation process of PBDEs in soil polluted by e-waste under increased concentrations of atmospheric O3. Chemosphere 118:373–382CrossRefGoogle Scholar
  16. Peralta RM, Ahn C, Gillevet PM (2013) Characterization of soil bacterial community structure and physicochemical properties in created and natural wetlands. Sci Total Environ 443:725–732CrossRefGoogle Scholar
  17. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glöckner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196CrossRefGoogle Scholar
  18. Qian P-Y, Wang Y, Lee OO, Lau SCK, Yang J, Lafi FF, Al-Suwailem A, Wong TYH (2011) Vertical stratification of microbial communities in the Red Sea revealed by 16S rDNA pyrosequencing. ISME J 5:568–568CrossRefGoogle Scholar
  19. Quan SX, Yan B, Yang F, Li N, Xiao XM, Fu JM (2015) Spatial distribution of heavy metal contamination in soils near a primitive e-waste recycling site. Environ Sci Pollut Res 22:1290–1298CrossRefGoogle Scholar
  20. Robrock KR, Mohn WW, Eltis LD, Alvarez-Cohen L (2011) Biphenyl and ethylbenzene dioxygenases of rhodococcus jostii RHA1 transform PBDEs. Biotechnol Bioeng 108:313–321CrossRefGoogle Scholar
  21. Roesch LF, Fulthorpe RR, Riva A, Casella G, Hadwin AK, Kent AD, Daroub SH, Camargo FA, Farmerie WG, Triplett EW (2007) Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J 1:283–290CrossRefGoogle Scholar
  22. Rousk J, Bååth E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG, Knight R, Fierer N (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4:1340–1351CrossRefGoogle Scholar
  23. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541CrossRefGoogle Scholar
  24. Shen C, Chen Y, Huang S, Wang Z, Yu C, Qiao M, Xu Y, Setty K, Zhang J, Zhu Y (2009) Dioxin-like compounds in agricultural soils near e-waste recycling sites from Taizhou area, China: chemical and bioanalytical characterization. Environ Int 35:50–55CrossRefGoogle Scholar
  25. Smolders E, Oorts K, Peeters S, Lanno R, Cheyns K (2015) Toxicity in lead salt spiked soils to plants, invertebrates and microbial processes: unraveling effects of acidification, salt stress and ageing reactions. Sci Total Environ 536:223–231CrossRefGoogle Scholar
  26. Tang XJ, Shen CF, Lei C, Xi X, Wu JY, Khan MI, Dou CM, Chen YX, Xu JM, Tang CX (2010) Inorganic and organic pollution in agricultural soil from an emerging E-waste recycling town in Taizhou area, China. J Soils Sediments 10:895–906CrossRefGoogle Scholar
  27. Tian W, Wang L, Li Y, Zhuang K, Li G, Zhang J, Xiao X, Xi Y (2015) Responses of microbial activity, abundance, and community in wheat soil after three years of heavy fertilization with manure-based compost and inorganic nitrogen. Agric Ecosyst Environ 213:219–227CrossRefGoogle Scholar
  28. Wang Y, Qian PY (2009) Conservative fragments in bacterial 16S rRNA genes and primer design for 16S ribosomal DNA amplicons in metagenomic studies. PLoS One 4:e7401CrossRefGoogle Scholar
  29. Wang F, Wang J, Dai J, Hu G, Wang J, Luo X, Mai B (2010) Comparative tissue distribution, biotransformation and associated biological effects by decabromodiphenyl ethane and decabrominated diphenyl ether in male rats after a 90-day oral exposure study. Environ Sci Technol 44:5655–5660CrossRefGoogle Scholar
  30. Wu K, Xu X, Liu J, Guo Y, Li Y, Huo X (2010) Polybrominated diphenyl ethers in umbilical cord blood and relevant factors in neonates from Guiyu, China. Environ Sci Technol 44:813–819CrossRefGoogle Scholar
  31. Xiao E, Krumins V, Tang S, Xiao T, Ning Z, Lan X, Sun W (2016) Correlating microbial community profiles with geochemical conditions in a watershed heavily contaminated by an antimony tailing pond. Environ Pollut 215:141–153CrossRefGoogle Scholar
  32. Yang H, Huo X, Yekeen TA (2013) Effects of lead and cadmium exposure from electronic waste on child physical growth. Environ Sci Pollut Res 20:4441–4447CrossRefGoogle Scholar
  33. Zhang S, Xu X, Wu Y, Ge J, Li W, Huo X (2014) Polybrominated diphenyl ethers in residential and agricultural soils from an electronic waste polluted region in South China: distribution, compositional profile, and sources. Chemosphere 102:55–60CrossRefGoogle Scholar
  34. Zhang R, Zhang W, Liu G, Lin K, Fu R (2016a) Changes of lead speciation and microbial toxicity in soil treated with repeated Pb exposure in the presence of BDE209. Environ Sci Pollut Res 23:4621–4628CrossRefGoogle Scholar
  35. Zhang W, Chen L, Zhang R, Lin K (2016b) High throughput sequencing analysis of the joint effects of BDE209-Pb on soil bacterial community structure. J Hazard Mater 301:1–7CrossRefGoogle Scholar
  36. Zheng S, Zhang M (2011) Effect of moisture regime on the redistribution of heavy metals in paddy soil. J Environ Sci 23:434–443CrossRefGoogle Scholar
  37. Zhong WH, Cai ZC (2007) Long-term effects of inorganic fertilizers on microbial biomass and community functional diversity in a paddy soil derived from quaternary red clay. Appl Soil Ecol 36:84–91CrossRefGoogle Scholar
  38. Zhu W, Liu L, Zou P, Xiao L, Yang L (2010) Effect of decabromodiphenyl ether (BDE 209) on soil microbial activity and bacterial community composition. World J Microbiol Biotechnol 26:1891–1899CrossRefGoogle Scholar
  39. Zhu D, Tanabe SH, Yang C, Zhang W, Sun J (2013) Bacterial community composition of South China Sea sediments through pyrosequencing-based analysis of 16S rRNA genes. PLoS One 8:528–534Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.State Environmental Protection Key Laboratory of Environmental Risk Assessment and Control on Chemical Process, School of Resource and Environmental EngineeringEast China University of Science and TechnologyShanghaiChina
  2. 2.Shanghai Pharmaceutical SchoolShanghaiChina
  3. 3.Shanghai Institute of Pollution Control and Ecological SecurityShanghaiChina
  4. 4.Baowu Group Environmental Resources Technology Co., Ltd.ShanghaiChina

Personalised recommendations