Environmental Science and Pollution Research

, Volume 25, Issue 10, pp 9904–9914 | Cite as

Rhizospheric effects on the microbial community of e-waste-contaminated soils using phospholipid fatty acid and isoprenoid glycerol dialkyl glycerol tetraether analyses

  • Mengke Song
  • Zhineng Cheng
  • Chunling Luo
  • Longfei Jiang
  • Dayi Zhang
  • Hua Yin
  • Gan Zhang
Research Article


We performed the study of rhizospheric effects on soil microbial community structure, including bacteria, fungi, actinomycete, and archaea, at an electronic waste (e-waste) recycling site by analyzing the phospholipid fatty acid (PLFA) and isoprenoid glycerol dialkyl glycerol tetraether (GDGT) contents. By comparing PLFA and isoprenoid GDGT profiles of rhizospheric and surrounding bulk soils of 11 crop species, we observed distinct microbial community structures. The total PLFA concentration was significantly higher in rhizospheric soils than in non-rhizospheric soils, whereas no obvious difference was found in the total isoprenoid GDGT concentrations. The microbial community structure was also different, with higher ratios of fungal-to-bacterial PLFAs (F/B) and lower relative abundance of Gram-positive bacteria in rhizospheric soils. The extent of rhizospheric effects varied among plant species, and Colocasia esculenta L. had the greatest positive effects on the total microbial biomass. Dissolved organic carbon and pH were the main environmental factors affecting the microbial community represented by PLFAs, while the archaeal community was influenced by copper and zinc in all soils. These results offer a comprehensive view of rhizospheric effects on microbes in heavy metal and persistent organic pollutant co-contaminated soil, and provide fundamental knowledge regarding microbial ecology in e-waste-contaminated soils.


e-waste Phospholipid fatty acid (PLFA) Isoprenoid glycerol dialkyl glycerol tetraether (isoprenoid GDGT) Rhizospheric soil Microbial community 



This study was supported by the Scientific and Technological Planning Project of Guangzhou, China (No. 201707020034), the National Natural Science Foundation of China (Nos. U1501234 and 41673111), and the China Postdoctoral Science Foundation (2015 M582430).

Supplementary material

11356_2018_1323_MOESM1_ESM.docx (319 kb)
ESM 1 (DOCX 319 kb)


  1. Ayari A, Yang H, Wiesenberg GLB, Xie SC (2013) Distribution of archaeal and bacterial tetraether membrane lipids in rhizosphere-root systems in soils and their implication for paleoclimate assessment. Geochem J 47(3):337–347. CrossRefGoogle Scholar
  2. Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68(1):1–13. CrossRefGoogle Scholar
  3. Bourceret A, Cebron A, Tisserant E, Poupin P, Bauda P, Beguiristain T, Leyval C (2016) The bacterial and fungal diversity of an aged PAH- and heavy metal-contaminated soil is affected by plant cover and edaphic parameters. Microb Ecol 71:711–724CrossRefGoogle Scholar
  4. Chen C, Yang K, Yu CN, Huang RL, Chen X, Tang XJ, Shen CF, Hashmi MZ, Shi HX (2014) Influence of redox conditions on the microbial degradation of polychlorinated biphenyls in different niches of rice paddy fields. Soil Biol Biochem 78:307–315. CrossRefGoogle Scholar
  5. Cheng ZN, Wang Y, Wang SR, Luo CL, Li J, Chaemfa C, Jiang HY, Zhang G (2014) The influence of land use on the concentration and vertical distribution of PBDEs in soils of an e-waste recycling region of South China. Environ Pollut 191:126–131. CrossRefGoogle Scholar
  6. Corgie SC, Joner EJ, Leyval C (2003) Rhizospheric degradation of phenanthrene is a function of proximity to roots. Plant Soil 257(1):143–150. CrossRefGoogle Scholar
  7. Costa R, Gotz M, Mrotzek N, Lottmann J, Berg G, Smalla K (2006) Effects of site and plant species on rhizosphere community structure as revealed by molecular analysis of microbial guilds. FEMS Microbiol Ecol 56(2):236–249. CrossRefGoogle Scholar
  8. de Vries FT, Hoffland E, van Eekeren N, Brussaard L, Bloem J (2006) Fungal/bacterial ratios in grasslands with contrasting nitrogen management. Soil Biol Biochem 38:2092–2103CrossRefGoogle Scholar
  9. Deng S, Ke T, Li L, Cai S, Zhou Y, Liu Y, Guo L, Chen L, Zhang D (2018) Impacts of environmental factors on the whole microbial communities in the rhizosphere of a metal-tolerant plant: Elsholtzia haichowensis. Environ Pollut.
  10. Dijkstra FA, Carrillo Y, Pendall E, Morgan JA (2013) Rhizosphere priming: a nutrient perspective. Front Microbiol 4.
  11. Frostegard A, Tunlid A, Baath E (1993) Phospholipid fatty-acid composition, biomass, and activity of microbial communities from 2 soil types experimentally exposed to different heavy-metals. Appl Environ Microb 59:3605–3617Google Scholar
  12. Grayston SJ, Griffith GS, Mawdsley JL, Campbell CD, Bardgett RD (2001) Accounting for variability in soil microbial communities of temperate upland grassland ecosystems. Soil Biol Biochem 33(4-5):533–551. CrossRefGoogle Scholar
  13. Haichar FE, Marol C, Berge O, Rangel-Castro JI, Prosser JI, Balesdent J, Heulin T, Achouak W (2008) Plant host habitat and root exudates shape soil bacterial community structure. Isme J 2(12):1221–1230. CrossRefGoogle Scholar
  14. Hinsinger P, Plassard C, Tang CX, Jaillard B (2003) Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints: a review. Plant Soil 248(1/2):43–59. CrossRefGoogle Scholar
  15. Huguet C, Hopmans EC, Febo-Ayala W, Thompson DH, Damste JSS, Schouten S (2006) An improved method to determine the absolute abundance of glycerol dibiphytanyl glycerol tetraether lipids. Org Geochem 37(9):1036–1041. CrossRefGoogle Scholar
  16. Hur M, Kim Y, Song HR, Kim JM, Choi YI, Yi H (2011) Effect of genetically modified poplars on soil microbial communities during the phytoremediation of waste mine tailings. Appl Environ Microb 77(21):7611–7619. CrossRefGoogle Scholar
  17. Jia GD, Zhang J, Chen JF, Peng PA, Zhang CLL (2012) Archaeal tetraether lipids record subsurface water temperature in the South China Sea. Org Geochem 50:68–77. CrossRefGoogle Scholar
  18. Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442(7104):806–809. CrossRefGoogle Scholar
  19. Liang C, Jesus ED, Duncan DS, Quensen JF, Jackson RD, Balser TC, Tiedje JM (2016) Switchgrass rhizospheres stimulate microbial biomass but deplete microbial necromass in agricultural soils of the upper Midwest, USA. Soil Biol Biochem 94:173–180. CrossRefGoogle Scholar
  20. Liste HH, Alexander M (2000) Accumulation of phenanthrene and pyrene in rhizosphere soil. Chemosphere 40(1):11–14. CrossRefGoogle Scholar
  21. Liu DY, Ding WX, Yuan JJ, Xiang J, Lin YX (2014) Substrate and/or substrate-driven changes in the abundance of methanogenic archaea cause seasonal variation of methane production potential in species-specific freshwater wetlands. Appl Microbiol Biot 98(10):4711–4721. CrossRefGoogle Scholar
  22. Liu J, He XX, Lin XR, Chen WC, Zhou QX, Shu WS, Huang LN (2015) Ecological effects of combined pollution associated with E-waste recycling on the composition and diversity of soil microbial communities. Environ Sci Technol 49(11):6438–6447. CrossRefGoogle Scholar
  23. Luo CL, Shen ZG, Li XD (2005) Enhanced phytoextraction of Cu, Pb, Zn and Cd with EDTA and EDDS. Chemosphere 59(1):1–11. CrossRefGoogle Scholar
  24. Ma B, Lyu XF, Zha T, Gong J, He Y, Xu JM (2015) Reconstructed metagenomes reveal changes of microbial functional profiling during PAHs degradation along a rice (Oryza sativa) rhizosphere gradient. J Appl Microbiol 118(4):890–900. CrossRefGoogle Scholar
  25. Martin BC, George SJ, Price CA, Ryan MH, Tibbett M (2014) The role of root exuded low molecular weight organic anions in facilitating petroleum hydrocarbon degradation: current knowledge and future directions. Sci Total Environ 472:642–653. CrossRefGoogle Scholar
  26. Massaccesi L, Benucci GMN, Gigliotti G, Cocco S, Corti G, Agnelli A (2015) Rhizosphere effect of three plant species of environment under periglacial conditions (Majella Massif, central Italy). Soil Biol Biochem 89:184–195. CrossRefGoogle Scholar
  27. McGrath SP, Shen ZG, Zhao FJ (1997) Heavy metal uptake and chemical changes in the rhizosphere of Thlaspi caerulescens and Thlaspi ochroleucum grown in contaminated soils. Plant Soil 188(1):153–159. CrossRefGoogle Scholar
  28. Mertens J, Broos K, Wakelin SA, Kowalchuk GA, Springael D, Smolders E (2009) Bacteria, not archaea, restore nitrification in a zinc-contaminated soil. Isme J 3(8):916–923. CrossRefGoogle Scholar
  29. Pietri JCA, Brookes PC (2009) Substrate inputs and pH as factors controlling microbial biomass, activity and community structure in an arable soil. Soil Biol Biochem 41(7):1396–1405. CrossRefGoogle Scholar
  30. Pollierer MM, Ferlian O, Scheu S (2015) Temporal dynamics and variation with forest type of phospholipid fatty acids in litter and soil of temperate forests across regions. Soil Biol Biochem 91:248–257CrossRefGoogle Scholar
  31. Qin H, Brookes PC, Xu JM (2014) Cucurbita spp. and Cucumis sativus enhance the dissipation of polychlorinated biphenyl congeners by stimulating soil microbial community development. Environ Pollut 184:306–312. CrossRefGoogle Scholar
  32. Schouten S, Forster A, Panoto FE, Damste JSS (2007) Towards calibration of the TEX86 palaeothermometer for tropical sea surface temperatures in ancient greenhouse worlds. Org Geochem 38(9):1537–1546. CrossRefGoogle Scholar
  33. Schouten S, Hopmans EC, Damste JSS (2013) The organic geochemistry of glycerol dialkyl glycerol tetraether lipids: a review. Org Geochem 54:19–61. CrossRefGoogle Scholar
  34. Seguin V, Gagnon C, Courchesne F (2004) Changes in water extractable metals, pH and organic carbon concentrations at the soil-root interface of forested soils. Plant Soil 260:1–17CrossRefGoogle Scholar
  35. Shen J, Zhang L, He J (2011) Abundance of archaea, crenarchaea and bacteria in selected agricultural soils of China. Chin J Appl Ecol 22:2996–3002Google Scholar
  36. Sliwinski MK, Goodman RM (2004) Comparison of crenarchaeal consortia inhabiting the rhizosphere of diverse terrestrial plants with those in bulk soil in native environments. Appl Environ Microb 70(3):1821–1826. CrossRefGoogle Scholar
  37. Smets W, Leff JW, Bradford MA, McCulley RL, Lebeer S, Fierer N (2016) A method for simultaneous measurement of soil bacterial abundances and community composition via 16S rRNA gene sequencing. Soil Biol Biochem 96:145–151. CrossRefGoogle Scholar
  38. Somers E, Vanderleyden J, Srinivasan M (2004) Rhizosphere bacterial signalling: a love parade beneath our feet. Crit Rev Microbiol 30:205–240CrossRefGoogle Scholar
  39. Song M, Luo CL, Jiang LF, Zhang DY, Wang YJ, Zhang G (2015a) Identification of benzo[a]pyrene-metabolizing bacteria in Forest soils by using DNA-based stable-isotope probing. Appl Environ Microb 81(21):7368–7376. CrossRefGoogle Scholar
  40. Song MK, Luo CL, Li FB, Jiang LF, Wang Y, Zhang DY, Zhang G (2015b) Anaerobic degradation of polychlorinated biphenyls (PCBs) and polychlorinated biphenyls ethers (PBDEs), and microbial community dynamics of electronic waste-contaminated soil. Sci Total Environ 502:426–433. CrossRefGoogle Scholar
  41. Steenwerth KL, Drenovsky RE, Lambert JJ, Kluepfel DA, Scow KM, Smart DR (2008) Soil morphology, depth and grapevine root frequency influence microbial communities in a Pinot noir vineyard. Soil Biol Biochem 40(6):1330–1340. CrossRefGoogle Scholar
  42. Syed JH, Malik RN, Li J, Wang Y, Xu Y, Zhang G, Jones KC (2013) Levels, profile and distribution of Dechloran Plus (DP) and polybrominated diphenyl ethers (PBDEs) in the environment of Pakistan. Chemosphere 93(8):1646–1653. CrossRefGoogle Scholar
  43. Tang XJ, Qiao JN, Chen C, Chen LT, Yu CN, Shen CF, Chen YX (2013) Bacterial communities of polychlorinated biphenyls polluted soil around an E-waste recycling workshop. Soil Sediment Contam 22(5):562–573. CrossRefGoogle Scholar
  44. Tang XJ, Hashmi MZ, Long DY, Chen LT, Khan MI, Shen CF (2014) Influence of heavy metals and PCBs pollution on the enzyme activity and microbial community of paddy soils around an E-waste recycling workshop. Int J Env Res Pub He 11(3):3118–3131. CrossRefGoogle Scholar
  45. Thion C, Cebron A, Beguiristain T, Leyval C (2012) Long-term in situ dynamics of the fungal communities in a multi-contaminated soil are mainly driven by plants. FEMS Microbiol Ecol 82(1):169–181. CrossRefGoogle Scholar
  46. Thomas G, Utz D, Wolfgang F (1996) Effects of ryegrass on biodegradation of hydrocarbons. Chemosphere 33:203–215CrossRefGoogle Scholar
  47. Thompson IP, Bailey MJ, Ellis RJ, Maguire N, Meharg AA (1999) Response of soil microbial communities to single and multiple doses of an organic pollutant. Soil Biol Biochem 31:95–105CrossRefGoogle Scholar
  48. Tkacz A, Cheema J, Chandra G, Grant A, Poole PS (2015) Stability and succession of the rhizosphere microbiota depends upon plant type and soil composition. Isme J 9(11):2349–2359. CrossRefGoogle Scholar
  49. Wang F, Huang Y, Wang X, Gao Z, Yu F, Xu F, Bao Q, Hu Y, Qiao M, Jin S, Huang Y, Li J, Xiang M (2014a) Effects of Cu stress on enzyme activity, bacteria and archaea quantity in soils. Asian Journal of Ecotoxicology 9:707–714Google Scholar
  50. Wang SR, Wang Y, Song MK, Luo CL, Li J, Zhang G (2016) Distributions and compositions of old and emerging flame retardants in the rhizosphere and non-rhizosphere soil in an e-waste contaminated area of south China. Environ Pollut 208(Pt B):619–625. CrossRefGoogle Scholar
  51. Wang Y, Luo CL, Li J, Yin H, Li XD, Zhang G (2011a) Characterization of PBDEs in soils and vegetations near an e-waste recycling site in south China. Environ Pollut 159(10):2443–2448. CrossRefGoogle Scholar
  52. Wang Y, Luo CL, Li J, Yin H, Li XD, Zhang G (2011b) Characterization and risk assessment of polychlorinated biphenyls in soils and vegetations near an electronic waste recycling site, south China. Chemosphere 85(3):344–350. CrossRefGoogle Scholar
  53. Wang Y, Luo CL, Li J, Yin H, Zhang G (2014b) Influence of plants on the distribution and composition of PBDEs in soils of an e-waste dismantling area: evidence of the effect of the rhizosphere and selective bioaccumulation. Environ Pollut 186:104–109. CrossRefGoogle Scholar
  54. Wenzel WW (2009) Rhizosphere processes and management in plant-assisted bioremediation (phytoremediation) of soils. Plant Soil 321(1-2):385–408. CrossRefGoogle Scholar
  55. Yang L, Wang GP, Cheng ZN, Liu Y, Shen ZG, Luo CL (2013) Influence of the application of chelant EDDS on soil enzymatic activity and microbial community structure. J Hazard Mater 262:561–570. CrossRefGoogle Scholar
  56. Ying T, Yongming L, Zhengao L (2006) Microbial diversity in polluted soils: an overview. Acta Pedol Sin 43:1018–1026Google Scholar
  57. Zhang W, Wang H, Zhang R, Yu XZ, Qian PY, Wong MH (2010) Bacterial communities in PAH contaminated soils at an electronic-waste processing center in China. Ecotoxicology 19(1):96–104. CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  • Mengke Song
    • 1
    • 2
  • Zhineng Cheng
    • 1
  • Chunling Luo
    • 1
    • 2
  • Longfei Jiang
    • 1
  • Dayi Zhang
    • 3
  • Hua Yin
    • 4
  • Gan Zhang
    • 1
  1. 1.Guangzhou Institute of GeochemistryChinese Academy of SciencesGuangzhouChina
  2. 2.College of Natural Resources and EnvironmentSouth China Agricultural UniversityGuangzhouChina
  3. 3.School of EnvironmentTsinghua UniversityBeijingChina
  4. 4.College of Environment and EnergySouth China University of TechnologyGuangzhouChina

Personalised recommendations