Skip to main content
SpringerLink
Log in

Responses of Arbuscular Mycorrhizal Fungi and Grass Leersia hexandra Swartz Exposed to Soil with Crude Oil

  • Published:
Water, Air, & Soil Pollution Aims and scope Submit manuscript

Abstract

This study evaluated the effect of crude oil on the intraradical structures and morphospecies of arbuscular mycorrhizal fungi (AMF) and on the aerial and root dry matter of the grass Leersia hexandra Swartz in order to propose indicators of toxicity. An experiment was conducted in a microtunnel for 180 days. The concentrations (g kg−1) of crude oil in the Gleysol were 0.693 (control), 3, 10, 30, 60, 90, 120, 150, and 180. The growth of intraradical hyphae, arbuscules, vesicles, and spores in soil was stimulated by crude oil concentrations of 3, 10, 30 and 60 g, but concentrations of 90, 120, 150, and 180 g kg−1 inhibited it. Eight morphospecies of AMF were identified. The number of spores of Rhizophagus fasciculatus, Rhizophagus intraradices, Funneliformis geosporum, Diversispora eburnea, and Ambispora gerdemannii showed sensitivity to the concentration of crude oil (index values were lower than one). The number of spores of Diversispora sp. was stimulated by exposure to crude oil, with non-toxic values for the eight concentrations. The index based on the aerial dry matter of L. hexandra showed toxicity values lower than one with crude oil concentrations of 60, 90, 120, 150, and 180 g kg−1, but the root dry matter showed non-toxic values with the eight concentrations. We suggest using the number of spores and morphospecies as an index of toxicity of crude oil and recommend using Diversispora sp. and L. hexandra for the phytoremediation of Gleysol contaminated with crude oil in the Mexican humid tropics.

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

Access this article

Log in via an institution

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

Similar content being viewed by others

References

  • Akiyama, K., Matsuzaki, K., & Hayashi, H. (2005). Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature, 453, 824–827.

    Article  Google Scholar 

  • Al-Mutairi, N., Bufarsan, A., & Al-Rukaibi, F. (2008). Ecorisk evaluation and treatability potential of soils contaminated with petroleum hydrocarbon-based fuels. Chemosphere, 74, 142–148.

    Article  CAS  Google Scholar 

  • Balestrini, R., Lumini, E., Borriello, R., & Bianciotto, V. (2015). Plan-soil biota interactions. In E. A. Paul (Ed.), Soil microbiology, ecology, and biochemistry. Oxford: Elsevier.

    Google Scholar 

  • Basumatary, B., Saikia, R., Bordoloi, S., Chandra, D. H., & Prasad, H. S. (2012). Assessment of potential plant species for phytoremediation of hydrocarbon contaminated areas of upper Assam, India. Journal of Chemical Technology Biotechnology, 87, 1329–1334.

  • Besalatpour, A., Khoshgoftarmanesh, A. H., Hajabbasi, M. A., & Afyuni, M. (2008). Germination and growth of selected plants in a petroleum contaminated calcareous soil. Soil and Sediment Contamination, 17, 665–676.

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

    Article  CAS  Google Scholar 

  • Blaszkowski, J. (2015). Arbuscular mycorrhizal fungi (Glomeromycota), endogone and complexipes species deposited in the Department of Plant Pathology. University of Agriculture in Szczecin, Poland. http://www.zor.zut.edu.pl/Glomeromycota/index.html. Accessed 20 March 2015.

  • Brady, C. N., & Weil, R. R. (2008). The nature and properties of soil. New Jersey: Pearson Prentice Hall.

    Google Scholar 

  • Cabello, M. N. (1999). Effectiveness of indigenous arbuscular mycorrhizal fungi (AMF) isolated from hydrocarbon polluted soils. Journal Basic of Microbiology, 39, 89–95.

    Article  CAS  Google Scholar 

  • Calabrese, E. J. (2012). Hormesis: improving predictions in the low-dose zone. In A. Luch (Ed.), Molecular, clinical and environmental toxicology, experientia supplementum. Basel: Springer.

    Google Scholar 

  • Calabrese, E. J., & Baldwin, L. A. (2003). Hormesis: the dose-response revolution. Annual Review of Pharmacology and Toxicology, 43, 175–197.

    Article  CAS  Google Scholar 

  • Calabrese, E. J., & Blain, R. B. (2009). Hormesis and plant biology. Environmental Pollution, 157, 42–48.

    Article  CAS  Google Scholar 

  • Calonne, M., Fontaine, J., Tisserant, B., Dupré de Boulois, H., Grandmougin-Ferjani, A., Declerck, S., & Lournès-Hadj, S. A. (2014). Polyaromatic hydrocarbons impair phosphorus transport by the arbuscular mycorrhizal fungus Rhizophagus irregularis. Chemosphere, 104, 97–104.

    Article  CAS  Google Scholar 

  • Carpio, L. A., Davies, F. T., & Arnold, A. (2005). Arbuscular mycorrhizal fungi, organic and inorganic controlled release fertilizers-effect on growth and leachate of container-grown bush morning glory (Ipomea carnea subsp. fistulosa) under high production temperatures. Journal of the American Society for Horticultural Science, 130, 131–139.

    Google Scholar 

  • Cerniglia, C. E. (1992). Biodegradation of polycyclic aromatic hydrocarbons. Biodegradation, 3, 351–368.

    Article  CAS  Google Scholar 

  • Chaillan, F., Chaîneau, H. C., Point, V., Saliot, A., & Oudot, J. (2006). Factors inhibiting bioremediation of soil contaminated with weathered oils and drill cuttings. Environmental Pollution, 144, 255–265.

    Article  CAS  Google Scholar 

  • Chaîneau, C. H., Yepremian, C., Vidalie, J. F., Ducreux, J., & Ballerini, D. (2003). Bioremediation of a crude oil-polluted soil: biodegradation, leaching and toxicity assessments. Water, Air, and Soil Pollution, 144, 419–440.

    Article  Google Scholar 

  • Daniels, B., & Skipper, H. D. (1982). Methods for the recovery and quantitative estimation of propagules from soil. In N. C. Schenck (Ed.), Methods and principles of mycorrhizal research. Saint Paul: The American Phytopathological Society.

    Google Scholar 

  • Davies, F. T., Jr., Puryear, J. D., Newton, R. J., Egilla, J. N., & Saraiva, G. J. A. (2001). Mycorrhizal fungi enhance accumulation and tolerance of chromium in sunflower (Helianthus annuus). Journal of Plant Physiology, 158, 777–786.

    Article  CAS  Google Scholar 

  • de la Providencia, E. I., Stefani, F. O. P., Labridy, M., St-Arnaud, M., & Hijri, M. (2015). Arbuscular mycorrhizal fungal diversity associated with Eleocharis obtusa and Panicum capillare growing in an extreme petroleum hydrocarbon-polluted sedimentation basin. FEMS Microbiology Letters, 362, 1–9.

    Google Scholar 

  • Debiane, D., Garcon, G., Verdin, A., Fontaine, J., Durand, R., Shirali, P., Grandmougin-Ferjani, A., & Lournès-Hadj, S. A. (2009). Mycorrhization alleviates benzo[a]pyrene-induced oxidative stress in vitro chicory root model. Phytochemistry, 70, 1421–1427.

    Article  CAS  Google Scholar 

  • Debiane, D., Calonne, M., Fontaine, J., Laruelle, F., Grandmoungin-Ferjani, A., & Lournès-Hadj, S. A. (2011). Lipid content disturbance in the arbuscular mycorrhizal, Glomus irregulare grown in monoxenic conditions under PAHs pollution. Fungal Biology, 115, 782–792.

    Article  CAS  Google Scholar 

  • Escaso, S. F., Martínez, G. J. L., & Planelló, C. M. R. (2010). Fundamentos básicos de fisiología vegetal y animal. Madrid: Pearson Educación S.A.

    Google Scholar 

  • Franco-Ramírez, A., Ferrera-Cerrato, R., Varela-Fregoso, L., Pérez-Moreno, J., & Alarcón, A. (2007). Arbuscular mycorrhizal fungi in chronically petroleum contaminated soils in Mexico and the effects of petroleum hydrocarbons on spore germination. Journal of Basic Microbiology, 47, 378–383.

    Article  Google Scholar 

  • Gao, Y., Li, Q., Lingn, W., & Zhu, X. (2011). Arbuscular mycorrhizal phytoremediation of soils contaminated with phenanthrene and pyrene. Journal of Hazardous Materials, 185, 703–709.

    Article  CAS  Google Scholar 

  • Gaspar, M. L., Cabello, M. N., Cazau, M. C., & Pollero, R. J. (2002). Effect of phenanthrene and Rhodotorula glutinis on arbuscular mycorrhizal fungus colonization of maize roots. Mycorrhiza, 12, 55–59.

    Article  CAS  Google Scholar 

  • Gerdemann, J. W., & Nicholson, T. H. (1963). Spores of mycorrhizal endogone species extracted from soil by wet sieving and decanting. Transactions of Britsh Mycological Society, 46, 235–244.

    Article  Google Scholar 

  • Hernández-Ortega, H. A., Alarcón, A., Ferrera-Cerrato, R., Zavaleta-Mancera, H. A., López-Delgado, H. A., & Mendoza-López, M. R. (2012). Arbuscular mycorrhizal fungi on growth, nutrient status, and total antioxidant activity of Melilotus albus during phytoremediation of a diesel-contaminated substrate. Journal of Environmental Management, 95, S319–S324.

    Article  Google Scholar 

  • INVAM (International Culture Collection of Arbuscular & Vesicular-Arbuscular Mycorrhizal Fungi). (2015). http://invam.wvu.edu/the-fungi/classification/ambisporaceae/ambispora/gerdemannii, 20/07/2015; http://invam.wvu.edu/the-fungi/classification/claroideoglomeraceae/claroideoglomus/lamellosum, 21/07/2015. http://invam.wvu.edu/the-fungi/classification/diversisporaceae/diversispora/eburneum, 21/07/2015; http://invam.wvu.edu/the-fungi/classification/glomaceae/funneliformis/geosporum, 21/07/2015; http://invam.wvu.edu/the-fungi/classification/glomaceae/funneliformis/mosseae, 22/07/2015; http://invam.wvu.edu/the-fungi/classification/glomaceae/rhizophagus/clarum, 22/07/2015; http://invam.wvu.edu/the-fungi/classification/glomaceae/rhizophagus/intradices, 22/07/2015; http://invam.wvu.edu/the-fungi/classification/glomaceae/rhizophagus/fasciculatum, 23/07/2015.

  • Joner, E. J., & Leyval, C. (2003). Rhizosphere gradients of polycyclic aromatic hydrocarbon (PAH) dissipation in two industrial soils and the impact of arbuscular mycorrhiza. Environmental Science and Technology, 37, 2371–2375.

    Article  CAS  Google Scholar 

  • Ke, L., Wong, T., Wong, Y., & Tam, N. (2002). Fate of polycyclic aromatic hydrocarbon (PAH) contamination in a mangrove swamp in Hong Kong following an oil spill. Marine Pollution Bulletin, 45, 339–347.

    Article  CAS  Google Scholar 

  • Kisic, I., Mesic, S., Basic, F., Brkic, V., Mesic, M., Durn, G., Zgorelec, Z., & Bertovic, L. (2009). The effect of drilling fluids and crude oil on some chemical characteristics of soil and crops. Geoderma, 149, 209–216.

    Article  CAS  Google Scholar 

  • Li, J., Guo, C., Lu, G., Yi, X., & Dang, Z. (2016). Bioremediation of petroleum-contaminated acid soil by a constructed bacterial consortium immobilized on sawdust: influences of multiple factors. Water, Air, and Soil Pollution, 227, 444.

    Article  Google Scholar 

  • Lin, Q., Mendelssohn, I. A., Suidan, M. T., Lee, K., & Venosa, A. D. (2002). The dose response relationship between no. 2 fuel oil and the growth of the salt marsh grass Spartina alterniflora. Marine Pollution Bulletin, 44, 897–902.

    Article  CAS  Google Scholar 

  • Liu, H., Weisman, D., Ye, Y., Cui, B., Huang, Y., Colón-Carmona, A., & Wang, Z. (2009). An oxidative stress response to polycyclic aromatic hydrocarbon exposure is rapid and complex in Arabidopsis thaliana. Plant Science, 176, 375–382.

    Article  CAS  Google Scholar 

  • Media Cybernetics. (2001). Image-Pro Plus version 4.5.1.22 for windows. Silver Spring: Media Cybernetics Inc.

    Google Scholar 

  • Muratova, A. Y., Dmitrieva, T. V., Panchenko, L. V., & Turkovskaya, V. O. (2008). Phytoremediation of oil-sludge-contaminated soil. International Journal of Phytoremediation, 10, 486–502.

    Article  CAS  Google Scholar 

  • Nardini, C., Di Salvo, L., & García, D. S. I. (2011). Micorrizas arbusculares: asociaciones simbióticas e indicadores de calidad ambiental en sistemas de cultivos extensivos. Revista Argentina de Microbiología, 43, 311–312.

    Google Scholar 

  • OECD. (2003). OECD guideline for the testing of chemicals proposal for updating guideline 208 terrestrial plant test: 208: seedling emergence and seedling growth test. Paris, France.

  • Ortas, I. (2015). Comparative analyses of Turkey agricultural soils: potential communities of indigenous and exotic mycorrhiza species effect on maize (Zea mays L.) growth and nutrient uptakes. European Journal of Soil Biology, 69, 79–87.

    Article  Google Scholar 

  • Pérez-Hernández, I., Ochoa-Gaona, S., Adams, S. R. H., Rivera-Cruz, M. C., & Geissen, V. (2013). Tolerance of four tropical tree species to heavy petroleum contamination. Water, Air, and Soil Pollution, 224, 1637.

    Article  Google Scholar 

  • Phillips, J. M., & Hayman, D. S. (1970). Improved procedures of clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment to infection. Transactions of the British Mycological Society, 55, 158–161.

    Article  Google Scholar 

  • Porta, C. J., López-Acevedo, R. M., & Roquero, L. C. (2003). Edafología para la Agricultura y el Medio Ambiente (3ath ed.). Madrid: Editorial Mundi-Prensa.

    Google Scholar 

  • Porter, W. M., Robson, A. D., & Abbott, L. K. (1987). Fiels survey of the distribution of vesicular-arbuscular mycorrizal fungi in raltion to soil. Journal of Applied Ecology, 24, 659–667.

    Article  Google Scholar 

  • Redecker, D., Schüßler, A., Stockinger, H., Stürmer, S., Morton, J., & Walker, C. (2013). An evidence-based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota). Mycorrhiza, 23, 515–531.

    Article  Google Scholar 

  • Rivera-Cruz, M. C., Trujillo-Narcía, A., Trujillo-Rivera, E. A., Arias-Trinidad, A., & Mendoza- López, M. R. (2016). Natural attenuation of weathered oil using aquatic plants in a farm in southeast Mexico. International Journal of Phytoremediation, 18, 877–884.

    Article  CAS  Google Scholar 

  • Salanitro, J. P., Dorn, P. B., Huesemann, H. M., Moore, K. O., Rhodes, I. A., Rice, J. L. M., Vipond, T. E., Western, M. M., & Wisniewski, H. L. (1997). Crude oil hydrocarbon bioremediation and soil ecotoxicity assessment. Environmental Science and Technology, 31, 1769–1776.

    Article  CAS  Google Scholar 

  • SAS (Statistical Analysis System). (2005). User’s guide, versión 9.1.3. Cary: SAS Institute, Inc.

    Google Scholar 

  • Sbrana, C. (2006). Fungal reconognition response to host derived signals by arbuscular mycorrhizal fungi. In K. G. Mukerji, C. Manoharachary, & J. Singh (Eds.), Microbial activity in the rhizosphere. Berlin: Springer.

    Google Scholar 

  • Schübler, A., & Walker, C. (2010). The Glomeromycota. A species list with new families and new genera. www.amf-phylogeny.com. Accessed 20 March 2015.

  • Schüβler, A. (2015). Glomeromycota Philogeny. http://schuessler.userweb.mwn.de/amphylo/. Accessed 20 May 2015.

  • SEMARNAT. (2002). Norma oficial mexicana NOM-021-RECNAT-2000. Que establece especificaciones de fertilidad, salinidad y clasificación de suelos. Mexico: Estudios, muestreo y análisis.

    Google Scholar 

  • Shirdam, R., Zand, D. A., Nabi, B. G., & Mehrdadi, N. (2008). Phytoremediation of hydrocarbon-contaminated soils with emphasis on the effect of petroleum hydrocarbons on the growth of plant species. Phytoprotection, 89, 21–29.

    Article  CAS  Google Scholar 

  • Singh, G. S., & Tuteja, N. (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry, 48, 909–930.

    Article  Google Scholar 

  • Smith, S. E., & Read, D. J. (2008). Mycorrhizal symbiosis (3rd ed.). A San Diego: Academic.

    Google Scholar 

  • Tang, J., Wang, M., Wang, F., Sun, Q., & Zhou, Q. (2011). Eco-toxicity of petroleum hydrocarbon contaminated soil. Journal of Environmental Sciences, 23, 845–851.

    Article  CAS  Google Scholar 

  • Timonen, S., & Marschner, P. (2006). Mycorrhizosphere concept. In K. G. Mukerji, C. Manoharachary, & J. Singh (Eds.), Microbial activity in the rhizosphere. Berlin: Springer.

    Google Scholar 

  • Tommerup, I. C. (1983). Temperature relations of spore germination and hyphal growth of vesicular-arbuscular mycorrhizal fungi in soil. Transactions of the British Mycological Society, 81, 381–387.

    Article  Google Scholar 

  • USEPA-3540C. (1996). Soxhlet extraction organics. SW-846 test methods for evaluating solid waste physical/chemical methods. http://www.epa.gov/wastes/hazard/testmethods/sw846/pdfs/3540c.pdf. Accessed 20 June 2012.

  • Verdin, A., Loun-es-Hadj Sahraoui, A., Fontaine, J., Grandmougin-Ferjani, A., & Durand, R. (2006). Effects of anthracene on development of an arbuscular mycorrhizal fungus and contribution of the symbiotic association to pollutant dissipation. Mycorrhiza, 16, 397–405.

    Article  CAS  Google Scholar 

  • Volante, A., Lingua, G., Cesaro, P., Cresta, A., Puppo, M., Ariati, L., & Berta, G. (2005). Influence of three species of arbuscular mycorrhizal fungi on the persistence of aromatic hydrocarbons in contaminated substrates. Mycorrhiza, 16, 43–50.

    Article  CAS  Google Scholar 

  • Watkinson, S. C., Money, N., & Boddy, L. (2016). The fungi (3rd ed.). New York: Academic.

    Google Scholar 

Download references

Acknowledgements

The authors acknowledge the financial support provided by the Colegio de Postgraduados en Ciencias Agrícolas, which funded this research through account numbers 40018 and 40019. Gratefully, we acknowledge the valuable corrections of the reviewers.

Author information

Authors and Affiliations

  1. Área Ambiental, Laboratorio de Microbiología Agrícola y Ambiental, Colegio de Postgraduados Campus Tabasco, Km 2 Periférico Carlos A. Molina. H. Cárdenas, CP 86570, Tabasco, Mexico

    A. Alejandro-Córdova, M. C. Rivera-Cruz & R. García-de la Cruz

  2. Centro de Investigación en Ciencias Biológicas, Universidad Autónoma de Tlaxcala, Carretera Tlaxcala-San Martín Texmelucan, km. 10.5, CP 90120, Ixtacuixtla, Tlaxcala, Mexico

    L. V. Hernández-Cuevas

  3. Área de Microbiología de Suelos, Colegio de Postgraduados Campus Montecillo, Carretera Mexico-Texcoco km 36.5 Montecillo, edo, CP 36230, Mexico, Mexico

    A. Alarcón

  4. Cuerpo Académico Energía y Medioambiente. Programa Educativo Químico Farmacéutico Biología, Universidad Popular de la Chontalpa, Carretera Cárdenas-Huimanguillo km 2, Ranchería Paso y Playa. H. Cárdenas, CP 86500, Tabasco, Mexico

    A. Trujillo-Narcía

Authors
  1. A. Alejandro-Córdova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. C. Rivera-Cruz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. L. V. Hernández-Cuevas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. Alarcón
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. Trujillo-Narcía
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. R. García-de la Cruz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. C. Rivera-Cruz.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alejandro-Córdova, A., Rivera-Cruz, M.C., Hernández-Cuevas, L.V. et al. Responses of Arbuscular Mycorrhizal Fungi and Grass Leersia hexandra Swartz Exposed to Soil with Crude Oil. Water Air Soil Pollut 228, 65 (2017). https://doi.org/10.1007/s11270-017-3247-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11270-017-3247-2

Keywords

Search

Navigation