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Biochemical Responses of Ten Ectomycorrhizal Fungal Isolates to Manganese

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Abstract

Manganese (Mn) is one of the heavy metals that pollute the environment. However, there are still few studies concerning Mn pollution. Our study focused on the ectomycorrhizal fungi (EMF), an important organism in the forest. We selected ten isolates of EMF, including Pt.2 (Pi solithus tinctorius 2), Cg.1 (Cenococcum geophilum 1), Br (Boletus reticulatus), Sb (Suillus bovinus), Pt.chdx (P. tinctorius chdx), Pt.104 (P. tinctorius 104), Sg (Suillus granulatus), Av (Amanita virgineoides), Sl.1 (Suillus luteus 1), and Sl.chdx (S. luteus chdx), to investigate their responses to Mn stress (0 to 3000 mg L−1) on liquid MMN medium. EMF isolates showed different responses to Mn stress after 60 days growth. According to their growth, they were classified into three groups: sensitive, moderately sensitive, and tolerant. Three isolates showed tolerance to Mn stress. The mycelia of the four sensitive EMF isolates grew slowly along with the increasing Mn level, and the growth was significantly inhibited in 3000 mg L−1 Mn. The accumulation of Mn in EMF mycelium was increased and the secretion of oxalic acid was stimulated by the increasing Mn concentration for all isolates. However, the sensitive isolates secreted significantly more oxalic acid than the tolerant isolates. A scanning electron microscope showed that hyphae were distorted and severely swollen and a transmission electron microscope revealed that Mn enriched in the cytoplasm and organelles of hyphae cells when EMF grew under 3000 mg L−1 Mn stress. In addition, we found that antioxidative enzyme activities, glutathione S-transferase (GST), and superoxide dismutase (SOD) were higher under the stress of Mn. In conclusion, we identified three isolates (Pt.2, Pt.104, and Br) that showed high Mn tolerance. This might demonstrate the great potential of those EMF in the reforestation of Mn mine lands.

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References

  • Bellion, M., Courbot, M., Jacob, C., Blaudez, D., & Chalot, M. (2006). Extracellular and cellular mechanisms sustaining metal tolerance in ectomycorrhizal fungi. FEMS Microbiology Letters, 254(2), 173–181.

    Article  CAS  Google Scholar 

  • Blaudez, D., Jacob, C., Turnau, K., Colpaert, J., Ahonen-Jonnarth, U., Finlay, R., et al. (2000). Differential responses of ectomycorrhizal fungi to heavy metals in vitro. Mycological Research, 104(11), 1366–1371.

    Article  CAS  Google Scholar 

  • Canton, G.C., Bertolazi, A.A., Cogo, A.J., Eutrópio, F.J., Melo, J., de Souza, S.B., et al. (2016). Biochemical and ecophysiological responses to manganese stress by ectomycorrhizal fungus Pisolithus tinctorius and in association with Eucalyptus grandis. Mycorrhiza, 1–13.

  • Colpaert, J., & Van Assche, J. (1987). Heavy metal tolerance in some ectomycorrhizal fungi. Functional Ecology, 415–421.

  • Colpaert, J. V., Muller, L. A., Lambaerts, M., Adriaensen, K., & Vangronsveld, J. (2004). Evolutionary adaptation to Zn toxicity in populations of Suilloid fungi. New Phytologist, 162(2), 549–559.

    Article  CAS  Google Scholar 

  • Culotta, V. C., Joh, H.-D., Lin, S.-J., Slekar, K. H., & Strain, J. (1995). A physiological role for Saccharomyces cerevisiae copper/zinc superoxide dismutase in copper buffering. Journal of Biological Chemistry, 270(50), 29991–29997.

    Article  CAS  Google Scholar 

  • Denny, H., & Ridge, I. (1995). Fungal slime and its role in the mycorrhizal amelioration of zinc toxicity to higher plants. New Phytologist, 130(2), 251–257.

    Article  CAS  Google Scholar 

  • Dučić, T., Parladé, J., & Polle, A. (2008). The influence of the ectomycorrhizal fungus Rhizopogon subareolatus on growth and nutrient element localisation in two varieties of Douglas fir (Pseudotsuga menziesii var. menziesii and var. glauca) in response to manganese stress. Mycorrhiza, 18(5), 227–239.

    Article  Google Scholar 

  • Estaun, V., Calvet, C., Pera, J., Camprubi, A., & Parlade, X. (2007). Heavy metals and mycorrhizal symbiosis: phytoremediation strategies. Afinidad, 64(528), 167–170.

    CAS  Google Scholar 

  • Filgueiras, A., Capelo, J., Lavilla, I., & Bendicho, C. (2000). Comparison of ultrasound-assisted extraction and microwave-assisted digestion for determination of magnesium, manganese and zinc in plant samples by flame atomic absorption spectrometry. Talanta, 53(2), 433–441.

    Article  CAS  Google Scholar 

  • Galli, U., Meier, M., & Brunold, C. (1993). Effects of cadmium on non-mycorrhizal and mycorrhizal Norway spruce seedlings [Picea abies (L.) Karst.] and its ectomycorrhizal fungus Laccaria laccata (Scop, ex Fr.) Bk. & Br.: Sulphate reduction, thiols and distribution of the heavy metal. New Phytologist, 125(4), 837–843.

    Article  CAS  Google Scholar 

  • Habig, W. H., Pabst, M. J., & Jakoby, W. B. (1974). Glutathione S-transferases the first enzymatic step in mercapturic acid formation. Journal of Biological Chemistry, 249(22), 7130–7139.

    CAS  Google Scholar 

  • Hartley, J., Cairney, J. W., Sanders, F. E., & Meharg, A. A. (1997). Toxic interactions of metal ions (Cd2+, Pb2+, Zn2+ and Sb3−) on in vitro biomass production of ectomycorrhizal fungi. New Phytologist, 137(3), 551–562.

    Article  CAS  Google Scholar 

  • Huang, Y., & Tao, S. (2001). Excessive Cu and Zn affecting on distribution of the metals and activities of glycolytic and nitrogen incorporating key enzymes in mycelia of ectomycorrhizal fungi Suillus bovinus. Journal of Environmental Sciences (China), 13(3), 337–341.

    CAS  Google Scholar 

  • Huang, Y., Tao, S., Jiang, X., & Liu, X. (2002). Influence of excesive copper on growth and accumulation of carbon and nitrogen in mycelia of four kinds of ectomycorrhizal fungi. Acta Microbiologica Sinica, 42(6), 737–744.

    CAS  Google Scholar 

  • Huang, Z., Huang, Y., & Peng, B. (2006). Influence of copper, cadmium on growth and cation exchange capacity of two kinds of ectomycorrhizal funguses. Acta Scientiae Circumstantiae, 27(8), 1654–1658.

    Google Scholar 

  • Huang, J., Nara, K., Zong, K., Wang, J., Xue, S., Peng, K., et al. (2014). Ectomycorrhizal fungal communities associated with Masson pine (Pinus massoniana) and white oak (Quercus fabri) in a manganese mining region in Hunan Province, China. Fungal Ecology, 9, 1–10.

    Article  Google Scholar 

  • Jacob, C., Courbot, M., Brun, A., Steinman, H. M., Jacquot, J. P., Botton, B., et al. (2001). Molecular cloning, characterization and regulation by cadmium of a superoxide dismutase from the ectomycorrhizal fungus Paxillus involutus. European Journal of Biochemistry, 268(11), 3223–3232.

    Article  CAS  Google Scholar 

  • Jentschke, G., & Godbold, D. (2000). Metal toxicity and ectomycorrhizas. Physiologia Plantarum, 109(2), 107–116.

    Article  CAS  Google Scholar 

  • Joselow, M. M., Tobias, E., Koehler, R., Coleman, S., Bogden, J., & Gause, D. (1978). Manganese pollution in the city environment and its relationship to traffic density. American Journal of Public Health, 68(6), 557–560.

    Article  CAS  Google Scholar 

  • Khan, A., Kuek, C., Chaudhry, T., Khoo, C., & Hayes, W. (2000). Role of plants, mycorrhizae and phytochelators in heavy metal contaminated land remediation. Chemosphere, 41(1), 197–207.

    Article  CAS  Google Scholar 

  • Landeweert, R., Hoffland, E., Finlay, R. D., Kuyper, T. W., & van Breemen, N. (2001). Linking plants to rocks: ectomycorrhizal fungi mobilize nutrients from minerals. Trends in Ecology & Evolution, 16(5), 248–254.

    Article  Google Scholar 

  • Leyval, C., Turnau, K., & Haselwandter, K. (1997). Effect of heavy metal pollution on mycorrhizal colonization and function: physiological, ecological and applied aspects. Mycorrhiza, 7(3), 139–153.

    Article  CAS  Google Scholar 

  • Meharg, A. A. (2003). The mechanistic basis of interactions between mycorrhizal associations and toxic metal cations. Mycological Research, 107(11), 1253–1265.

    Article  CAS  Google Scholar 

  • Mendez, M. O., & Maier, R. M. (2008). Phytoremediation of mine tailings in temperate and arid environments. Reviews in Environmental Science and Bio/Technology, 7(1), 47–59.

    Article  CAS  Google Scholar 

  • Ni, M., Dehesh, K., Tepperman, J. M., & Quail, P. H. (1996). GT-2: in vivo transcriptional activation activity and definition of novel twin DNA binding domains with reciprocal target sequence selectivity. The Plant Cell, 8(6), 1041–1059.

    Article  CAS  Google Scholar 

  • Ortiz, D., Kreppel, L., Speiser, D., Scheel, G., McDonald, G., & Ow, D. (1992). Heavy metal tolerance in the fission yeast requires an ATP-binding cassette-type vacuolar membrane transporter. The EMBO Journal, 11(10), 3491.

    CAS  Google Scholar 

  • Ortiz, D. F., Ruscitti, T., McCue, K. F., & Ow, D. W. (1995). Transport of metal-binding peptides by HMT1, a fission yeast ABC-type vacuolar membrane protein. Journal of Biological Chemistry, 270(9), 4721–4728.

    Article  CAS  Google Scholar 

  • Ott, T., Fritz, E., Polle, A., & Schützendübel, A. (2002). Characterisation of antioxidative systems in the ectomycorrhiza-building basidiomycete Paxillus involutus (Bartsch) Fr. and its reaction to cadmium. FEMS Microbiology Ecology, 42(3), 359–366.

    Article  CAS  Google Scholar 

  • Ouziad, F., Hildebrandt, U., Schmelzer, E., & Bothe, H. (2005). Differential gene expressions in arbuscular mycorrhizal-colonized tomato grown under heavy metal stress. Journal of Plant Physiology, 162(6), 634–649.

    Article  CAS  Google Scholar 

  • Ray, P., & Adholeya, A. (2009). Correlation between organic acid exudation and metal uptake by ectomycorrhizal fungi grown on pond ash in vitro. Biometals, 22(2), 275–281.

    Article  CAS  Google Scholar 

  • Roth, E. F., & Gilbert, H. S. (1984). The pyrogallol assay for superoxide dismutase: absence of a glutathione artifact. Analytical Biochemistry, 137(1), 50–53.

    Article  CAS  Google Scholar 

  • Roy, S., Khasa, D. P., & Greer, C. W. (2007). Combining alders, frankiae, and mycorrhizae for the revegetation and remediation of contaminated ecosystems. Botany, 85(3), 237–251.

    CAS  Google Scholar 

  • Sayer, J. A., & Gadd, G. M. (1997). Solubilization and transformation of insoluble inorganic metal compounds to insoluble metal oxalates by Aspergillus niger. Mycological Research, 101(06), 653–661.

    Article  CAS  Google Scholar 

  • Sharples, J., Meharg, A., Chambers, S., & Cairney, J. (2000). Evolution: symbiotic solution to arsenic contamination. Nature, 404(6781), 951–952.

    CAS  Google Scholar 

  • Thompson, G. W., & Medve, R. J. (1984). Effects of aluminum and manganese on the growth of ectomycorrhizal fungi. Applied and Environmental Microbiology, 48(3), 556–560.

    CAS  Google Scholar 

  • Wu, F., Liu, Y., Xia, Y., Shen, Z., & Chen, Y. (2011). Copper contamination of soils and vegetables in the vicinity of Jiuhuashan copper mine, China. Environmental Earth Sciences, 64(3), 761–769.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by the National Natural Science Foundation of China (31300525), the Doctoral Scientific Research Foundation (Z111021309) from Northwest A&F University to Dr. Jian Huang, and the Special Fund for Forestry Scientific Research in the Public Interest of China (201404302). We thank Dr. Nara Kazuhide and Dr. Chunlan Lian, the University of Tokyo, gifting the ectomycrrhizal fungal isolates.

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Qi, Y., Zhao, N., Liu, J. et al. Biochemical Responses of Ten Ectomycorrhizal Fungal Isolates to Manganese. Water Air Soil Pollut 227, 477 (2016). https://doi.org/10.1007/s11270-016-3183-6

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