, Volume 28, Issue 7, pp 635–650 | Cite as

Arbuscular mycorrhizal inoculum sources influence bacterial, archaeal, and fungal communities’ structures of historically dioxin/furan-contaminated soil but not the pollutant dissipation rate

  • H. Meglouli
  • A. Lounès-Hadj Sahraoui
  • M. Magnin-Robert
  • B. Tisserant
  • M. Hijri
  • J. FontaineEmail author
Original Article


Little is known about the influence of arbuscular mycorrhizal fungi (AMF) inoculum sources on phytoremediation efficiency. Therefore, the aim of this study was to compare the effects of two mycorrhizal inocula (indigenous and commercial inocula) in association with alfalfa and tall fescue on the plant growth, the bacterial, fungal, and archaeal communities, and on the removal of dioxin/furan (PCDD/F) from a historically polluted soil after 24 weeks of culture in microcosms. Our results showed that both mycorrhizal indigenous and commercial inocula were able to colonize plant roots, and the growth response depends on the AMF inoculum. Nevertheless, the improvement of root dry weight in inoculated alfalfa with indigenous inoculum and in inoculated tall fescue with commercial inoculum was clearly correlated with the highest mycorrhizal colonization of the roots in both plant species. The highest shoot dry weight was obtained in inoculated alfalfa and tall fescue with the commercial inoculum. AMF inoculation differently affected the number of bacterial and archaeal OTUs and bacterial diversity, with elevated bacterial and archaeal OTUs and bacterial diversity observed with indigenous inoculum. Mycorrhizal inoculation increases the abundance of bacterial OTUs (in particular with indigenous inoculum) and microbial richness but it does not improve PCDD/F dissipation. Vegetation had no effect on the abundance of microbial OTUs nor on richness but stimulated specific communities (Planctomycetia and Gammaproteobacteria) likely to be involved in the dissipation of PCDD/F. The reduction of toxic equivalency PCDD/F concentration also could be explained by the stimulation of soil microbial activities estimated with dehydrogenase and fluorescein diacetate hydrolase.


Phytoremediation Mycorrhizae Inoculum sources Microbial community Dioxins/furans 



This work has been carried out in the Halluin3R project which is financed by the European Union (FEDER), the French Region of Hauts-de-France and the French Environment and Energy Management Agency (ADEME) and in the framework of the Alibiotech project which is financed by European Union, French State and the French Region of Hauts-de-France. The authors are grateful to the soil analysis laboratory of INRA (Arras, France) for help in PCDD/F analysis. Data presented in this paper were analyzed using the CALCULCO computing platform, supported by SCOSI/ULCO (Service commun du Système d’Information de l’Université du Littoral Côte d’Opale).

Supplementary material

572_2018_852_MOESM1_ESM.docx (368 kb)
ESM 1 (DOCX 367 kb)
572_2018_852_MOESM2_ESM.xlsx (3.5 mb)
ESM 2 (XLSX 3626 kb)


  1. Adam G, Duncan H (2001) Development of a sensitive and rapid method for the measurement of total microbial activity using fluorescein diacetate (FDA) in a range of soils. Soil Biol Biochem 33:943–951CrossRefGoogle Scholar
  2. Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals—concepts and applications. Chemosphere 91:869–881. CrossRefGoogle Scholar
  3. Artursson V, Finlay RD, Jansson JK (2006) Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ Microbiol 8:1–10. CrossRefPubMedGoogle Scholar
  4. Bago B and Azcon-Aguilar C (1997) Changes in the rhizosphere pH induced by arbuscular mycorrhiza formation in onion (Allium cepa L.). Z. Pflanzenernaehr-Bodenk, 180: 333–339Google Scholar
  5. Cabello MN (1999) Effectiveness of indigenous arbuscular mycorrhizal fungi (AMF) isolated from hydrocarbon polluted soils. J Basic Microbiol 39:89–95CrossRefGoogle Scholar
  6. Camprubi A, Calvet C, Estaun V (1995) Growth enhancement of Citrus reshni after inoculation with Glomus-Intraradices and Trichoderma aureoviride and associated effects on microbial populations and enzyme activity in potting mixes. Plant Soil 173:233–238CrossRefGoogle Scholar
  7. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336. CrossRefGoogle Scholar
  8. Cea M, Jorquera M, Rubilar O, Langer H, Tortella G, Diez MC (2010) Bioremediation of soil contaminated with pentachlorophenol by Anthracophyllum discolor and its effect on soil microbial community. J Hazard Mater 181:315–323. CrossRefPubMedGoogle Scholar
  9. Chekol T, Vough LR, Chaney RL (2004) Phytoremediation of polychlorinated biphenyl-contaminated soils: the rhizosphere effect. Environ Int 30:799–804. CrossRefPubMedGoogle Scholar
  10. Chen W-Y, Wu J-H, Lin Y-Y, Huang H-J, Chang J-E (2013) Bioremediation potential of soil contaminated with highly substituted polychlorinated dibenzo-p-dioxins and dibenzofurans: microcosm study and microbial community analysis. J Hazard Mater 261:351–361. CrossRefPubMedGoogle Scholar
  11. Del Val C, Barea JM, Azcón-Aguilar C (1999) Diversity of arbuscular mycorrhizal fungus populations in heavy-metal-contaminated soils. Appl Environ Microbiol 65:718–723PubMedPubMedCentralGoogle Scholar
  12. Duponnois R, Galiana A, Prin Y (2008) The mycorrhizosphere effect: a multitrophic interaction complex improves mycorrhizal symbiosis and plant growth. Mycorrhizae: sustainable agriculture and Forestry:227–240Google Scholar
  13. Dyke PH (2003) Releases of Polychlorinated Dibenzo-p-Dioxins and Polychlorinated Dibenzofurans to Land and Water and with Products. In: Fiedler H (ed) Persistent Organic Pollutants. The Handbook of Environmental Chemistry (Vol. 3 Series: Anthropogenic Compounds), vol vol 30. Springer, Berlin, HeidelbergGoogle Scholar
  14. Faiad W, Hanano A, Kabakibi MM, Abbady AQ (2016) Immuno-detection of dioxins using a recombinant protein of aryl hydrocarbon receptor (AhR) fused with sfGFP. BMC Biotechnol 16:1–11. CrossRefGoogle Scholar
  15. Frey-Klett P, Garbaye J, Tarkka M (2007) The mycorrhiza helper bacteria revisited. New Phytol 176:22–36. CrossRefPubMedGoogle Scholar
  16. Futamata H, Uchida T, Yoshida N, Yonemitsu Y, Hiraishi A (2004) Distribution of dibenzofuran-degrading bacteria in soils polluted with different levels of polychlorinated dioxins. Microbes Environ 19:172–177. CrossRefGoogle Scholar
  17. Galazka A, Galazka R (2015) Phytoremediation of polycyclic aromatic hydrocarbons in soils artificially polluted using plant-associated-endophytic bacteria and Dactylis glomerata as the bioremediation plant. Polish J Microbiol 64:241–252CrossRefGoogle Scholar
  18. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118. CrossRefGoogle Scholar
  19. Gasiewicz TA, Park SK (2003) Ah receptor: involvement in toxic responses. Dioxins and health, 2nd edn. p. 491–532CrossRefGoogle Scholar
  20. Hanano A, Almousally I, Shaban M (2014) Phytotoxicity effects and biological responses of Arabidopsis thaliana to 2,3,7,8-tetrachlorinated dibenzo-p-dioxin exposure. Chemosphere 104:76–84. CrossRefPubMedGoogle Scholar
  21. Hanano A, Almousally I, Shaban M, Moursel N, Shahadeh A, Alhajji E (2015) Differential tissue accumulation of 2,3,7,8-Tetrachlorinated dibenzo-p-dioxin in Arabidopsis thaliana affects plant chronology, lipid metabolism and seed yield. BMC Plant Biol 15:193. CrossRefPubMedPubMedCentralGoogle Scholar
  22. Herlemann DP, Labrenz M, Jürgens K, Bertilsson S, Waniek JJ, Andersson AF (2011) Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISMEJ 5:1571–1579. CrossRefGoogle Scholar
  23. Hiraishi A (2003) Biodiversity of dioxin-degrading microorganisms and potential utilization in bioremediation. Microbes Environ 18:105–125CrossRefGoogle Scholar
  24. Iffis B, St-Arnaud M, Hijri M (2016) Petroleum hydrocarbon contamination, plant identity and arbuscular mycorrhizal fungal (AMF) community determine assemblages of the AMF spore-associated microbes. Environ Microbiol 18:2689–2704. CrossRefPubMedGoogle Scholar
  25. Ionescu M, Beranova K, Dudkova V, Kochankova L, Demnerova K, Macek T, Mackova M (2009) Isolation and characterization of different plant associated bacteria and their potential to degrade polychlorinated biphenyls. Int Biodeterior Biodegrad 63:667–672. CrossRefGoogle Scholar
  26. Karlson U, Dowling DN, O’Gara F, Rivilla R, Bittens M, Francesconi S Pritchard HC, Pedersen HC (1998) “Development of self-contained plant/GMM systems for soil.” Bioremediation. Past, Present and Future Risk Assessment When Using GMO’s. pp. 23–31.Google Scholar
  27. Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect VA mycorrhizas. Mycol Res 92:486–488. CrossRefGoogle Scholar
  28. Kulkarni PS, Crespo JG, Afonso CAM (2008) Dioxins sources and current remediation technologies—a review. Environ Int 34:139–153. CrossRefPubMedGoogle Scholar
  29. Lenoir I, Fontaine J, Lounès-Hadj Sahraoui A (2016a) Arbuscular mycorrhizal fungal responses to abiotic stresses: a review. Phytochemistry 123:4–15. CrossRefPubMedGoogle Scholar
  30. Lenoir I, Lounès-Hadj Sahraoui A, Laruelle F, Yolande D, Fontaine J (2016b) Arbuscular mycorrhizal wheat inoculation promotes alkane and polycyclic aromatic hydrocarbon biodegradation: microcosm experiment on aged-contaminated soil. Environ Pollut 213:549–560. CrossRefGoogle Scholar
  31. Li Y, Liang F, Zhu Y, Wang F (2013) Phytoremediation of a PCB-contaminated soil by alfalfa and tall fescue single and mixed plants cultivation. J Soils Sedi 13:925–931. CrossRefGoogle Scholar
  32. Lu M, Zhang Z, Sun S, Wei X, Wang Q, Su Y (2010) The use of goosegrass (Eleusine indica) to remediate soil contaminated with petroleum. Water Air Soil Pollut 209:181–189. CrossRefGoogle Scholar
  33. Macek T, Macková M, Káš J (2000) Exploitation of plants for the removal of organics in environmental remediation. Biotechnol Adv 18:23–34. CrossRefPubMedGoogle Scholar
  34. Mansfeld-Giese K, Larsen J, Bodker L (2002) Bacterial populations associated with mycelium of the arbuscular mycorrhizal fungus Glomus intraradices. FEMS Microbiol Ecol 41:133–140. CrossRefPubMedGoogle Scholar
  35. Margesin R, Zimmerbauer A, Schinner F (2000) Monitoring of bioremediation by soil biological activities. Chemosphere 40:339–346. CrossRefPubMedGoogle Scholar
  36. Margesin R (2005) Mannual for soil analysis – Monitoring and Assessing soil bioremediation. XVI, 366p, HardcoverGoogle Scholar
  37. Marschner P, Baumann K (2003) Changes in bacterial community structure induced by mycorrhizal colonisation in split-root maize. Plant Soil 251:279–289. CrossRefGoogle Scholar
  38. McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A new method which gives an objective measure of colonization of roots by vesicular- arbuscular mycorrhizal fungi. New Phytol 115:495–501. CrossRefGoogle Scholar
  39. Meier S, Borie F, Curaqueo G, Bolan N, Cornejo P (2012) Effects of arbuscular mycorrhizal inoculation on metallophyte and agricultural plants growing at increasing copper levels. Appl Soil Ecol 61:280–287. CrossRefGoogle Scholar
  40. Middleton EL, Rihardson S, Koziol L, Palmer CE, Yermakov ZY, Henning JA, Schultz PA, Bever JD (2015) Locally adapted arbuscular mycorrhizal fungi improve vigor and resistance to herbivory of native prairie plant species. Ecosphere 6:1–16. CrossRefGoogle Scholar
  41. Oh K, Cao T, Li T, Cheng H (2014) Study on application of phytoremediation technology in management and remediation of contaminated soils. J Clean Energy Technol 2:216–220. CrossRefGoogle Scholar
  42. OrłowskaE GB, Turnau K (2012) Effect of different arbuscular mycorrhizal fungal isolates on growth and arsenic accumulation in Plantago lanceolata L. Environ Pollut 168:121–130. CrossRefGoogle Scholar
  43. Passatore L, Rossetti S, Juwarkar AA, Massacci A (2014) Phytoremediation and bioremediation of polychlorinated biphenyls (PCBs): state of knowledge and research perspectives. J Hazard Mater 278:189–202. CrossRefPubMedGoogle Scholar
  44. Petrić I, Bru D, Udiković-Kolić N, Hršak D, Philippot L, Martin-Laurent F (2011) Evidence for shifts in the structure and abundance of the microbial community in a long-term PCB-contaminated soil under bioremediation. J Hazard Mater 195:254–260. CrossRefPubMedGoogle Scholar
  45. Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–IN18. CrossRefGoogle Scholar
  46. Qin H, Brookes PC, Xu J (2016) Arbuscular mycorrhizal fungal hyphae alter soil bacterial community and enhance polychlorinated biphenyls dissipation. Front Microbiol 7:1–10. CrossRefGoogle Scholar
  47. Revathi K, Haribabu TE, Sudha PN (2011) Phytoremediation of chromium contaminated soil using sorghum plant. Int J Environ Sci 2:417–428. CrossRefGoogle Scholar
  48. Rodríguez-Caballero G, Caravaca F, Fernández-González AJ, Alguacil MM, Fernández-LópezM RA (2017) Arbuscular mycorrhizal fungi inoculation mediated changes in rhizosphere bacterial community structure while promoting revegetation in a semiarid ecosystem. Sci Total Environ 585:838–848. CrossRefGoogle Scholar
  49. Roesti D, Kurt Ineichen K, Braissant O, Redecker D, Wiemken A, Aragno M (2005) Bacteria associated with spores of the arbuscular mycorrhizal fungi Glomus geosporum and Glomus constrictum. Appl Environ Microbiol 71:6673–6679CrossRefGoogle Scholar
  50. Rowe HI, Brown CS, Claassen VP (2007) Comparisons of mycorrhizal responsiveness with field soil and commercial inoculum for six native montane species and Bromus tectorum. Restor Ecol 15:44–52CrossRefGoogle Scholar
  51. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing Mothur: opensource, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541. CrossRefGoogle Scholar
  52. Smith FA, Smith SE (1996) Mutualism and parasitism: diversity in function and structure in the arbuscular (VA) mycorrhizal symbiosis. In: Callow JA (ed) Advances in botanical research, vol 22. Academic Press, London, pp 1–43Google Scholar
  53. Solís-Domínguez FA, Valentín-Vargas A, Chorover J, Maier RM (2011) Effect of arbuscular mycorrhizal fungi on plant biomass and the rhizosphere microbial community structure of mesquite grown in acidic lead/zinc mine tailings. Sci Total Environ 409:1009–1016. CrossRefPubMedPubMedCentralGoogle Scholar
  54. Sun M, Fu D, Teng Y, Shen Y, Luo Y, Li Z, Christie P (2011) In situ phytoremediation of PAH-contaminated soil by intercropping alfalfa (Medicago sativa L.) with tall fescue (Festuca arundinacea Schreb.) and associated soil microbial activity. J Soils Sedi 11:980–989. CrossRefGoogle Scholar
  55. Tabatabai MA (1982) Soil enzymes. In methods of soil analysis. II. Chemical and microbiological properties, eds a. L. Page, R. H. Miller and D. R. Keeney, 2nd edn., pp. 903–947. American Society of Agronomy, Madison.Google Scholar
  56. Tangahu BV, Sheikh Abdullah SR, Basri H, Idris M, Anuar N, Mukhlisin M (2011) A review on heavy metals (As, Pb, and Hg) uptake by plants through phytoremediation. Int J Chem Eng 2011. CrossRefGoogle Scholar
  57. The World Health Organization (2005) Re-evaluation of Human and Mammalian Toxic Equivalency Factors for Dioxins and Dioxin-like CompoundsGoogle Scholar
  58. Toljander JF, Lindahl BD, Paul LR, Elfstrand M, Finlay RD (2007) Influence of arbuscular mycorrhizal mycelial exudates on soil bacterial growth and community structure. FEMS Microbiol Ecol 61:295–304. CrossRefPubMedGoogle Scholar
  59. Trabelsi D, Mhamdi R, Trabelsi D, Mhamdi R (2013) Microbial inoculants and their impact on soil microbial communities: a review. Biomed Res Int 2013:1–11. CrossRefGoogle Scholar
  60. Tu C, Teng Y, Luo Y, Sun X, Deng S, Li Z, Liu W, Xu Z (2011) PCB removal, soil enzyme activities, and microbial community structures during the phytoremediation by alfalfa in field soils. J Soils Sedi 11:649–656. CrossRefGoogle Scholar
  61. Villacieros M, Power B, Sánchez-Contreras M, Lloret J, Oruezabal RI, Martín M, Fernández-Piñas F, Bonilla I, Whelan C, Dowling DN, Rivilla R (2003) Colonization behaviour of Pseudomonas fluorescens and Sinorhizobium meliloti in the alfalfa (Medicago sativa) rhizosphere. Plant Soil 251:47–54. CrossRefGoogle Scholar
  62. Wang Y, Oyaizu H (2009) Evaluation of the phytoremediation potential of four plant species for dibenzofuran-contaminated soil. J Hazard Mater 168:760–764. CrossRefPubMedGoogle Scholar
  63. Wang Y, Qian P (2009) Conservative fragments in bacterial 16S rRNA genes and primer design for 16S ribosomal DNA amplicons in metagenomic studies. PLoS One 10:e74014. CrossRefGoogle Scholar
  64. Weissenhorn I, Leyval C, Belgy G, Berthelin J (1995) Arbuscular mycorrhizal contribution to heavy metal uptake by maize (Zea mays L.) in pot culture with contaminated soil. Mycorrhiza 5:245–251Google Scholar
  65. White TJ, Bruns TD, Lee SB, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR Protocols: a Guide to Methods and Applications. Academic Press, New York, pp 315–322Google Scholar
  66. Wright SF, Upadhyaya A (1996) Extraction of an abundant and unusual protein from soil and comparison with hyphal protein of arbuscular mycorrhizal fungi. Soil Sci 161:575–586CrossRefGoogle Scholar
  67. Wright SF, Franke-Snyder M, Morton JB, Upadhyaya A (1996) Time-course study and partial characterization of a protein on hyphae of arbuscular mycorrhizal fungi during active colonization of roots. Plant Soil 181:193–203Google Scholar
  68. Zeeb BA, Amphlett JS, Rutter A, Reimer KJ (2006) Potential for phytoremediation of polychlorinated biphenyl-(PCB)-contaminated soil. Int J Phytorem 8:199–221. CrossRefGoogle Scholar
  69. Zhou X, Zhou J, Xiang X (2013) Impact of four plant species and arbuscular mycorrhizal (AM) fungi on polycyclic aromatic hydrocarbon (PAH) dissipation in spiked soil. Polish J Environ Stud 22:1239–1245 Available at: Google Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Unité de Chimie Environnementale et Interactions sur le Vivant (UCEIV)Université du Littoral Côte d’OpaleCalaisFrance
  2. 2.Institut de Recherche en Biologie Végétale, Département de Sciences BiologiquesUniversité de MontréalMontréalCanada

Personalised recommendations