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Metal-binding capacity of arbuscular mycorrhizal mycelium

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Abstract

Experiments with excised mycelium of several Glomus spp. with different histories of exposure to heavy metals were carried out to measure their capacities to bind Cd and Zn. Cd sorption was followed for up to 6 h of incubation to determine its time course relationships. Controls treated with a metabolic inhibitor were included to evaluate whether sorption was due to active uptake or passive adsorption. The effect of ion competition (effects of Ca or Zn on Cd sorption) and general measurements of cation exchange capacity (CEC) of roots and hyphae were also performed. The results showed that AM mycelium has a high metal sorption capacity relative to other microorganisms, and a CEC comparable to other fungi. Metal sorption was rapid (<30 min) and appeared mainly to be due to passive adsorption. Adsorption was highest in a metal-tolerant G. mosseae isolate and intermediate for a fungus isolated from a soil treated with metal-contaminated sludge. The former adsorbed up to 0.5 mg Cd per mg dry biomass, which was three times the binding capacity of non-tolerant fungi, and more than 10 times higher than reported values for, e.g., the commonly used biosorption organism Rhizopus arrhizus. The implications of these results for AM involvement in plant protection against excess heavy metal uptake are discussed.

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References

  • Abbott L K, Robson A D and De Boer G 1984 The effect of phosphorus on the formation of hyphae in soil by the vesicular-arbuscular mycorrhizal fungus, Glomus fasciculatum. New Phytol. 97, 437–446.

    Article  CAS  Google Scholar 

  • Angle J S and Chaney R L 1989 Cadmium resistance screening in nitrilotriacetate-buffered minimal media. Appl. Environ. Microbiol. 55, 2101–2104.

    PubMed  CAS  Google Scholar 

  • Bécard G and Fortin J A 1988 Early events of vesicular-arbuscular mycorrhiza formation on Ri T-DNA transformed roots. New Phytol. 108, 211–218.

    Article  Google Scholar 

  • Chaudri A M, Mcgrath S P, Giler K E, Rietz E and Sauerbeck D R 1993 Enumeration of indigenous Rhizobium leguminosarum biovar trifolii in soils previously treated with metal-contaminated sewage sludge. Soil Biol. Biochem. 25, 301–309.

    Article  CAS  Google Scholar 

  • Cotoras D, Viedma P, Cifuentes L and Mestre A 1992 Sorption of metal ions by whole cells of Bacillus and Micrococcus. Environ. Technol. 13, 551–559.

    CAS  Google Scholar 

  • Crooke W M 1964 The measurement of the cation-exchange capacity of plant roots. Plant Soil 21, 43–49.

    Article  Google Scholar 

  • Deneux-Mustin S, Rouiller J, Durecu S, Munier-Lamy C and Berthelin J 1994 Détermination de la capacité de fixation des métaux par la biomasse microbiennes des sol, des eaux et des sédiment: intérê t de la méthode de titrage potentiométrique. C. R. Acad. Sci. Paris Sér. II 319, 1057–1062.

    CAS  Google Scholar 

  • Denny H J and Ridge I 1995 Fungal slime and its role in the mycorrhizalamelioration of zinc toxicity to higher plants. New Phytol. 130, 251–257.

    Article  CAS  Google Scholar 

  • Gadd G M 1990 Heavy metal accumulation by bacteria and other microorganisms. Experientia 46, 834–840.

    Article  CAS  Google Scholar 

  • Gadd GM1993 Interactions of fungi with toxic metals. New Phytol. 124, 25–60.

    Article  CAS  Google Scholar 

  • Gran G 1952 Determination of the equivalence point in potentiometric titrations. Part II. Anal. Am. 77, 661–671.

    CAS  Google Scholar 

  • Hanssen J F, Thingstad T F and Goksöyr J 1974 Evaluation of hyphal lengths and fungal biomass in soil by a membrane filter technique. Oikos 25, 102–107.

    Google Scholar 

  • Huang C and Huang C P 1996 Application of Aspergillus oryzae and Rhizopus oryzae for Cu(II) removal. Water Res. 9, 1985–1990.

    Article  Google Scholar 

  • Ibekwe A M, Angle J S, Chaney R L and van Berkum P 1996 Zinc and cadmium toxicity to alfalfa and its microsymbiont. J. Environ. Qual. 25, 1032–1040.

    Article  CAS  Google Scholar 

  • Joner E J and 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 

  • Kapoor A and Viraraghavan T 1998 Biosorption of heavy metals on Aspergillus niger: effect of pretreatment. Biores. Technol. 63, 109–113.

    Article  CAS  Google Scholar 

  • Kinniburgh D G, Kackson M L and Syers J K 1976 Adsorption of alkaline earth, transition, and heavy metal cations by hydrous oxide gels of iron and aluminium. Soil Sci. Soc. Am. J. 40, 796–799.

    Article  CAS  Google Scholar 

  • Krantz-Rülcker C, Allard B and Schnürer J 1996 Adsorption of IIBmetals by three common soil fungi-comparison and assessment of importance for metal distribution in natural soil systems. Soil Biol. Biochem. 28, 967–975.

    Article  Google Scholar 

  • Kurek E, Czaban J and Bollag JM 1982 Sorption of cadmium bymicroorganisms in competition with other soil constituents. Appl. Environ. Microbiol. 43, 1011–1015.

    PubMed  CAS  Google Scholar 

  • Laheurte F, Leyval C and Berthelin J 1990 Root exudates of maize, pine and beech seedlings influenced by mycorrhizal and bacterial inoculation. Symbiosis 9, 111–116.

    Google Scholar 

  • Leyval C, Turnau K and Haselwandter K 1997 Effect of heavy metal pollution on mycorrhizal colonization and function: physiological, ecological and applied aspects. Mycorrhiza 7, 139–153.

    Article  CAS  Google Scholar 

  • Li X L, George E and Marschner H 1991 Phosphorus depletion and pH decrease at the root- soil and hyphae- soil interfaces of VA mycorrhizal white clover fertilized with ammonium. New Phytol. 119, 397–404.

    Article  CAS  Google Scholar 

  • Maldonado-Mendoza I E and Harrison M J 1999 Regulation of the expression of a phosphate transporter from Glomus intraradices in response to exogenous levels of phosphate. In Plant Biology Division, 10th Anniversary Symposium Proceedings. Ed. R A Dixon, M J Harrison and M J Roossinck. pp 130–132. The Samuel Roberts Noble Foundation, Dallas.

    Google Scholar 

  • Marschner H 1986 Mineral Nutrition of Higher Plants. Academic Press, London. 674 p.

    Google Scholar 

  • Marschner P, Jentschke G and Godbold D L 1998 Cation exchange capacity and lead sorption in ectomycorrhizal fungi. Plant Soil 205, 93–98.

    Article  CAS  Google Scholar 

  • Mattuschka B and Straube G 1993 Biosorption of metals by a waste biomass. J. Chem. Tech. Biotechnol. 58, 57–63.

    CAS  Google Scholar 

  • McKnight K B, McKnight K H and Harper K T 1990 Cation exchange capacities and mineral element concentrations of macrofungal stipe tissue. Mycologia 82, 91–98.

    CAS  Google Scholar 

  • Morley G F and Gadd G M 1995 Sorption of toxic metals by fungi and clay minerals. Mycol. Res. 99, 1429–1438.

    Article  CAS  Google Scholar 

  • Mullen M D, Wolf D C, Beveridge T J and Bailey G W 1992 Sorption of heavy metals by the soil fungi Aspergillus niger and Mucor rouxii. Soil Biol. Biochem. 24, 129–135.

    Article  CAS  Google Scholar 

  • Olsson P A, Francis R, Read D J and Söderström B 1998 Growth of arbuscular mycorrhizal mycelium in calcareous dune sand and its interaction with other soil microorganisms as estimated by measurement of specific fatty acids. Plant Soil 201, 9–16.

    Article  CAS  Google Scholar 

  • Scot J A and Palmer S J 1990 Sites of cadmium uptake in bacteria used for biosorption. Appl. Microbiol. Biotechnol. 33, 221–225.

    Google Scholar 

  • Thompson J P 1996 Correction of dual phosphorus and zinc deficiencies of linseed (Linum usitatissimum L) with cultures of vesicular-arbuscular mycorrhizal fungi. Soil Biol. Biochem. 28, 941–951.

    Article  CAS  Google Scholar 

  • Tobin J M, Cooper D G and Neufeld R J 1984 Uptake of metalions by Rhizopus arrhizus biomass. Appl. Environ. Microbiol. 47, 821–824.

    PubMed  CAS  Google Scholar 

  • Weissenhorn I, Leyval C and Berthelin J 1993 Cd-tolerant arbuscular mycorrhizal (AM) fungi from heavy-metal polluted soils. Plant Soil 157, 247–256.

    Article  CAS  Google Scholar 

  • Zar J H 1984 Biostatistical Analysis. 2nd edition Prentice Hall, Englewood Cliffs, NJ. 718 p.

    Google Scholar 

  • Zhou J L 1999 Zn biosorption by Rhizopus arrhizus and other fungi. Appl. Microbiol. Biotechnol. 51, 686–693.

    Article  CAS  Google Scholar 

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Joner, E.J., Briones, R. & Leyval, C. Metal-binding capacity of arbuscular mycorrhizal mycelium. Plant and Soil 226, 227–234 (2000). https://doi.org/10.1023/A:1026565701391

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