Skip to main content
Springer Nature Link
Log in

Influence of three species of arbuscular mycorrhizal fungi on the persistence of aromatic hydrocarbons in contaminated substrates

  • Original Paper
  • Published:
Mycorrhiza Aims and scope Submit manuscript

Abstract

Aromatic hydrocarbons are pollutants which have mutagenic and carcinogenic properties as well as relatively high hydrosolubility. Their presence in soils makes techniques such as bioremediation an important topic for research. In this work, the effect of arbuscular mycorrhiza (AM) on the persistence of benzene, toluene, ethylbenzene and xylene (BTEX) in artificially contaminated substrates was evaluated. Leek plants were grown with three AM fungal species using a specially designed mesocosm system, in which internal air and substrate samples were analyzed by gas chromatography for BTEX content. Strong reductions in the BTEX concentration in substrates were generally observed in the presence of mycorrhizal plants. Residual BTEX content ranged between nearly total disappearance (<2%) and 40% of the original concentration, whereas there was a high persistence of hydrocarbons in the samples of substrate alone or with non-mycorrhizal plants. These results provide first evidence for an influence of AM activity in reducing pollution of substrates by aromatic hydrocarbons.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Bécard G, Piché Y (1992) Establishment of vesicular–arbuscular mycorrhiza in root organ culture: review and proposed methodology. In: Norris J, Read D, Varma A (eds) Techniques for the study of mycorrhiza. Academic, New York, pp 89–108

    Google Scholar 

  • Bertoni G, Bolognese F, Galli E, Barbieri P (1996) Cloning of the genes for and characterization of the early stages of toluene and o-xylene catabolism in Pseudomonas stutzeri OX1. Appl Environ Microbiol 62:3704–3711

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bertoni G, Bolognese F, Galli E, Barbieri P (1998) Analysis of the gene cluster encoding for toluene/o-xylene monooxygenase from Pseudomonas stutzeri OX1. Appl Environ Microbiol 64:3626–3632

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bianciotto V, Bandi C, Minerdi D, Sironi M, Tichy HV, Bonfante P (1996) An obligately endosymbiotic mycorrhizal fungus itself harbors obligately intracellular bacteria. Appl Environ Microbiol 62:3005–3010

    CAS  PubMed  PubMed Central  Google Scholar 

  • Binet P, Portal M, Leyval C (2000) Fate of polycyclic aromatic hydrocarbons (PAH) in the rhizosphere of ryegrass. Plant Soil 227:207–213

    Article  CAS  Google Scholar 

  • Binet P, Portal M, Leyval C (2001) Application of GC-MS to the study of anthracene disappearance in the rhizosphere of ryegrass. Org Geochem 32:217–222

    Article  CAS  Google Scholar 

  • Cabello MN (1997) Hydrocarbon pollution: its effect on native arbuscular mycorrhizal fungi (AMF). FEMS Microbiol Ecol 22:233–236

    Article  CAS  Google Scholar 

  • Cafaro V, Scognamiglio R, Viggiani A, Izzo V, Passaro I, Notomista E, Del Piaz F, Amoresano A, Casbarra A, Pucci P, Di Donato A (2002) Expression and purification of the recombinant subunits of toluene/o-xylene monooxygenase and reconstitution of the active complex. Eur J Biochem 269:5689–5699

    Article  CAS  PubMed  Google Scholar 

  • Chauhan S, Barbieri P, Wood TK (1998) Oxidation of trichloroethylene, 1,1-dichloroethylene, and chloroform by toluene/o-xylene monooxygenase from Pseudomonas stutzeri OX1. Appl Environ Microbiol 64:3023–3024

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Z, Huang GH, Chakma A (1998) Integrated environmental risk assessment for petroleum-contaminated sites—a North American case study. Water Sci Technol 38(4–5):131–138

    CAS  Google Scholar 

  • Christensen JS, Elton J (1996) Soil and groundwater pollution from BTEX. Groundwater pollution primer CE 4594: soil and groundwater pollution. Civil Engineering Dept., Virginia Tech. http://www.cee.vt.edu/program_areas/environmental/teach/gwprimer/btex/btex.html

  • Del Val C, Barea JM, Azcon-Aguilar C (1999) Diversity of arbuscular-mycorrhizal fungus populations in heavy-metal-contaminated soils. Appl Environ Microbiol 65(2):718–723

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fedorak PM, Westlake DWS (1986) Fungal metabolism of n-alkylbenzenes. Appl Env Microbiol 51(2):435–437

    CAS  Google Scholar 

  • Fusconi A, Gnavi E, Trotta A, Berta G (1999) Apical meristems of tomato roots and their modifications induced by arbuscular mycorrhizal and soilborne pathogenic fungi. New Phytol 142:505–516

    Article  Google Scholar 

  • Gamalero E, Trotta A, Massa N, Copetta A, Martinotti MG, Berta G (2004) Impact of two fluorescent pseudomonads and an arbuscular mycorrhizal fungus on tomato plant growth, root architecture and P acquisition. Mycorrhiza 14:185–192

    Article  PubMed  Google Scholar 

  • Gao Y, Zhu L (2004) Plant uptake, accumulation and translocation of phenantrene and pyrene in soils. Chemosphere 55:1169–1178

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez-Chavez C, D'Haen J, Vangronsveld J, Dodd JC (2002) Copper sorption and accumulation by the extraradical mycelium of different Glomus spp. (arbuscular mycorrhizal fungi) isolated from the same polluted soil. Plant Soil 240:287–297

    Article  CAS  Google Scholar 

  • Han M-J, Choi H-T, Song H-G (2004) Degradation of phenanthrene by Trametes versicolor and its laccase. J Microbiol 42(2):94–98

    CAS  PubMed  Google Scholar 

  • Harms HH (1996) Bioaccumulation and metabolic fate of sewage sludge derived organic xenobiotics in plants. Sci Total Environ 185:83–92

    Article  CAS  Google Scholar 

  • Haselwandter K, Leyval C, Sanders FE (1994) Impact of arbuscular mycorrhizal fungi on plant uptake of heavy metals and radionuclides from soil. In: Gianinazzi S, Schüepp H (eds) Impact of arbuscular mycorrhizas on sustainable agriculture and natural ecosystems. Birkhäuser, Basel, pp 179–190

    Chapter  Google Scholar 

  • Hayes RB, Yin SN, Dosemeci M, Li GL, Wacholder S, Chow WH, Rothman N, Wang YZ, Dai TR, Chao X-J, Jiang ZL, Ye P-Z, Zhao HB, Kou QR, Zhang WY, Meng JF, Zho JS, Lin XF, Ding CY, Li CY, Zhang Z-N, Li DG, Travis LB, Blot WJ, Linet MS (1996) Mortality among benzene-exposed workers in China. Environ Health Perspect 140(Suppl 6):1349–1352

    Article  Google Scholar 

  • Helgason T, Merryweather W, Denison J, Wilson P, Young JPW, Fitter AH (2002) Selectivity and functional diversity in arbuscular mycorrhizas of co-occurring fungi and plants from a temperate deciduous woodland. J Ecol 90:371–384

    Article  Google Scholar 

  • Hemida SK, Bagy MMK, Khallil AM (1993) Utilization of hydrocarbons by fungi. Cryptogam Mycol 14:207–213

    Google Scholar 

  • Henner P, Schiavon M, Druelle V, Lichtfouse E (1999) Phytotoxicity of ancient gaswork soils. Effect of polycyclic aromatic hydrocarbons (PAHs) on plant germination. Org Geochem 30:963–969

    Article  CAS  Google Scholar 

  • Hewitt EJ (1966) Sand and water culture methods used in the study of plant nutrition. Commonw Bur Hortic Plant Crops Tech Commun 22:190–191

    Google Scholar 

  • Irons RD, Stillman WS (1996) Impact of benzene on differentiation of bone marrow progenitor cells. Environ Health Perspect 104(Suppl 6):1247–1250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iturbe R, Flores RM, Flores CR, Torres LG (2003) Soil and water contamination levels in an out-of-service oil distribution and storage station in Michoacan, Mexico. Water Air Soil Pollut 146:261–281

    Article  CAS  Google Scholar 

  • Iturbe R, Flores RM, Torres LG (2004) TPH-contaminated Mexican refinery soil: health risk assessment and the first year of changes. Environ Monit Assess 91:237–255

    Article  CAS  PubMed  Google Scholar 

  • Joner EJ, Leyval C (1997) Uptake of 109Cd by roots and hyphae of a Glomus mosseae/Trifolium subterraneum mycorrhiza from soil amended with high and low concentrations of cadmium. New Phytol 135:353–360

    Article  CAS  Google Scholar 

  • Joner EJ, Leyval C (2001) Influence of arbuscular mycorrhiza on clover and ryegrass grown together in a soil spiked with polycyclic aromatic hydrocarbons. Mycorrhiza 10:155–159

    Article  CAS  Google Scholar 

  • Joner EJ, Leyval C (2003) Phytoremediation of organic pollutants using mycorrhizal plants: a new aspect of rhizosphere interactions. Agronomie 23:495–502

    Article  CAS  Google Scholar 

  • Joner EJ, Briones R, Leyval C (2000) Metal-binding capacity of arbuscular mycorrhizal mycelium. Plant Soil 226:227–234

    Article  CAS  Google Scholar 

  • Joner EJ, Johansen A, Loibner AP, de la Cruz MA, Szolar OH, Portal JM, Leyval C (2001) Rhizosphere effects on microbial community structure and dissipation and toxicity of polycyclic aromatic hydrocarbons (PAHs) in spiked soil. Environ Sci Technol 35(13):2773–2777

    Article  CAS  PubMed  Google Scholar 

  • Joner EJ, Corgié SC, Amellal N, Leyval C (2002) Nutritional constraints to degradation of polycyclic aromatic hydrocarbons in a simulated rhizosphere. Soil Biol Biochem 34:859–864

    Article  CAS  Google Scholar 

  • Klironomos JN, Ursic M, Rillig M, Allen MF (1998) Interspecific differences in the response of arbuscular mycorrhizal fungi to Artemisia tridentata grown under elevated CO2. New Phytol 138:599–605

    Article  Google Scholar 

  • Lee CH, Lee JY, Jang WY, Jeon YH, Lee KK (2002) Evaluation of air injection and extraction tests at a petroleum contaminated site, Korea. Water Air Soil Pollut 135:65–91

    Article  CAS  Google Scholar 

  • Leyval C, Binet P (1998) Effect of polyaromatic hydrocarbons (PAHs) in soil on arbuscular mycorrhizal plants. J Environ Qual 27:402–407

    Article  CAS  Google Scholar 

  • Leyval C, Joner EJ, Del Val C, Haselwandtler K (2002) Potential of arbuscular mycorrhizal fungi for bioremediation. In: Gianinazzi S, Schüepp H, Barea JM, Haselwandter K (eds) Mycorrhiza technology: from genes to bioproducts. Birkhäuser, Basel, pp 175–186

    Google Scholar 

  • Liao JP, Lin XG, Cao ZH, Shi YQ, Wong MH (2003) Interactions between arbuscular mycorrhizae and heavy metals under sand culture experiment. Chemosphere 50:847–853

    Article  CAS  PubMed  Google Scholar 

  • Malcovà R, Vosatka M, Gryndler M (2003) Effects of inoculation with Glomus intraradices on lead uptake by Zea mays L. and Agrostis capillaris L. Appl Soil Ecol 23:55–67

    Article  Google Scholar 

  • Margesin R, Walder G, Schinner F (2003) Bioremediation assessment of a BTEX-contaminated soil. Acta Biotechnol 23:29–36

    Article  CAS  Google Scholar 

  • Massa N, Copetta A, Barni E, Siniscalco C, Berta G (2002) Root morphometric analysis and soil AM inoculum potential evaluation in three different herbaceous communities (NW Appennines, Italy). Acts of the 4th international conference on mycorrhizae, Montreal, Quebec, Canada, abstract no. 617

  • Middelhoven WJ (1993) Catabolism of benzene compound by ascomycetous and basidiomycetous yeasts and yeastlike fungi. Antonie Van Leeuwenhoek 63:125–144

    Article  CAS  PubMed  Google Scholar 

  • Murata M, Tsujikawa M, Kawanishi S (1999) Oxidative DNA damage by minor metabolites of toluene may lead to carcinogenesis and reproductive disfunction. Biochem Biophys Res Commun 261:478–483

    Article  CAS  PubMed  Google Scholar 

  • Parke JL, Kaeppler SW (2000) Effects of genetic differences among crop species and cultivars upon the arbuscular mycorrhizal symbiosis. In: Kapulnick Y, Douds DD (eds) Arbuscular mycorrhizas, physiology and function. Kluwer, Dordrecht, pp 131–146

    Chapter  Google Scholar 

  • Prenafeta-Boldú FX, Kuhn FXA, Luykx DMAM, Anke H, van Groenestijn JW, de Bont JAM (2001) Isolation and characterisation of fungi growing on volatile aromatic hydrocarbons as their sole carbon and energy source. Mycol Res 105:477–484

    Article  Google Scholar 

  • Prenafeta-Boldú FX, Ballerstedt H, Gerritse J, Grotenhuis JTC (2004) Bioremediation of BTEX hydrocarbons: effect of soil inoculation with the toluene-growing fungus Cladophialophora sp. strain T1. Biodegradation 15:59–65

    Article  PubMed  Google Scholar 

  • Qi B, Moe WM, Kinney KA (2002) Biodegradation of volatile organic compounds by five fungal species. Appl Microbiol Biotechnol 58:684–689

    Article  CAS  PubMed  Google Scholar 

  • Rivera-Beceril F, Calantzis C, Turnau K, Coussanel J-P, Belimov AA, Gianinazzi S, Strasser RJ, Gianinazzi-Pearson V (2002) Cadmium accumulation and buffering of cadmium-induced stress by arbuscular mycorrhiza in three Pisum sativum L. genotypes. J Exp Bot 53:1177–1185

    Article  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Song H-G (1997) Biodegradation of aromatic hydrocarbons by several white-rot fungi. J Microbiol 35:66–71

    CAS  Google Scholar 

  • Trotta A, Varese GC, Gnavi E, Fusconi A, Sampò S, Berta G (1996) Interactions between the soilborne root pathogen Phytophthora nicotianae var. parasitica and the arbuscular mycorrhizal fungus Glomus mosseae in tomato plants. Plant Soil 185:199–209

    Article  CAS  Google Scholar 

  • Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorrhization VA d'un système radiculaire. Recherche de méthodes d'estimation ayant une signification fonctionnelle. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Mycorrhizae: physiology and genetics. INRA, Paris, pp 217–221

    Google Scholar 

  • Vivas A, Vörös A, Birò B, Barea JM, Ruiz-Lozano JM, Azcòn R (2003) Beneficial effects of indigenous Cd-tolerant and Cd-sensitive Glomus mosseae associated with a Cd-adapted strain of Brevibacillus sp. in improving plant tolerance to Cd contamination. Appl Soil Ecol 24:177–186

    Article  Google Scholar 

  • Weber FJ, Hage KC, de Bont JAM (1995) Growth of the fungus Cladosporium sphaerospermum with toluene as the sole carbon and energy source. Appl Environ Microbiol 61:3562–3566

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xiaolin L, Chen B, Feng G, Christie P (2002) Role of arbuscular mycorrhizal fungi in alleviation of Zn phytotoxicity and mineral nutrition of host plants. Acts of the 17th World Congress of Soil Science, symposium no. 42, paper no. 1649

  • Yadav JS, Reddy CA (1993) Degradation of benzene, toluene, ethylbenzene, and xylenes (BTEX) by the lignin-degrading basidiomycete Phanerochaete chrysosporium. Appl Env Microbiol 59(3):756–762

    CAS  Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge Drs. Chiara Lotto, Lara Boatti, Elisa Bona, Andrea Copetta, Giulio Lanati, Nadia Massa and Paola Falaschi for their important support in all the phases of the work, and Mr. Guido Ronzat for his help in the building and setting up of the mesocosm cabinets. This work was funded by the EU-RTD project GENOMYCA (QLK5-2000-01319 NAS QLRT-CT-2001-02804).

Author information

Authors and Affiliations

  1. Dipartimento di Scienze dell'Ambiente e della Vita, Università degli Studi del Piemonte Orientale Amedeo Avogadro, Via G. Bellini 25/g, 15100, Alessandria, AL, Italy

    Andrea Volante, Guido Lingua, Patrizia Cesaro & Graziella Berta

  2. IDROCONS Srl, Strada Savonesa 9, 15050, Rivalta Scrivia, Tortona, AL, Italy

    Andrea Cresta & Manuela Puppo

  3. Dipartimento di Medicina Interna e Terapia Medica, Laboratorio di Idrologia Chimica e Analisi Ambientali, Università degli Studi di Pavia, Piazza Botta 11, 27100, Pavia, PV, Italy

    Luigi Ariati

Authors
  1. Andrea Volante
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Guido Lingua
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. Patrizia Cesaro
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. Andrea Cresta
    View author publications

    You can also search for this author inPubMed Google Scholar

  5. Manuela Puppo
    View author publications

    You can also search for this author inPubMed Google Scholar

  6. Luigi Ariati
    View author publications

    You can also search for this author inPubMed Google Scholar

  7. Graziella Berta
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to Graziella Berta.

Additional information

Andrea Volante and Guido Lingua contributed equally to this paper

Rights and permissions

Reprints and permissions

About this article

Cite this article

Volante, A., Lingua, G., Cesaro, P. et al. Influence of three species of arbuscular mycorrhizal fungi on the persistence of aromatic hydrocarbons in contaminated substrates. Mycorrhiza 16, 43–50 (2005). https://doi.org/10.1007/s00572-005-0012-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-005-0012-y

Keywords