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The Effect of Ericoid Mycorrhizal and Ectomycorrhizal Plants on Soil Properties of Grass Meadow in Tundra of the Khibiny Mountains

  • SOIL CHEMISTRY
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Abstract

The study of the effect of plants with different type of mycorrhizal symbiosis on carbon, nitrogen, and phosphorus transformation in soils is important in view of the necessity to predict changes in nutrient cycles upon transformation of the structure of plant communities under changing environmental conditions. The impact of dwarf shrubs (Empetrum hermaphroditum, Vaccinium myrtillus, Vaccinium uliginosum, and Vaccinium vitis-idaea) with ericoid mycorrhiza (ERM) and shrub (Betula nana) with ectomycorrhiza (ECM) on the properties of Umbric Leptosol of grass meadow in tundra of the Khibiny Mountains has been studied. It is shown that the presence of plants with ERM and ECM causes an increase in the content of labile mineral and organic phosphorus and of extractable organic nitrogen in soil and in the C/N ratio in the microbial biomass and a decrease in the content of nitrates, N-mineralization and nitrification activity, and the C/N and C/P ratios in the extractable organic matter. The increased activity of glucosidase, chitinase, and phosphatase testifies to high activity of exoenzymes of ERM fungi even in soil with high availability of inorganic nitrogen and phosphorus.

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REFERENCES

  1. N. D. Ananyeva, E. V. Blagodatskaya, and T. S. Demkina, “Temporal and spatial variability of the microbial metabolic quotient in soils,” Eurasian Soil Sci. 35, 1092–1099 (2002).

    Google Scholar 

  2. N. D. Ananyeva, E. A. Susyan, I. M. Ryzhova, E. O. Bocharnikova, and E. V. Stolnikova, “Microbial biomass carbon and the microbial carbon dioxide production by soddy-podzolic soils in postagrogenic biogeocenoses and in native spruce forests of the southern taiga (Kostroma oblast),” Eurasian Soil Sci. 42, 1029–1037 (2009).

    Article  Google Scholar 

  3. I. S. Buzin, M. I. Makarov, T. I. Malysheva, M. S. Kadulin, N. E. Koroleva, and M. N. Maslov, “Transformation of nitrogen compounds in soils of mountain tundra ecosystems in the Khibiny,” Eurasian Soil Sci. 52, 518–525 (2019). https://doi.org/10.1134/S1064229319030025

    Article  Google Scholar 

  4. M. I. Makarov, “The role of mycorrhiza in nitrogen nutrition of plants: a review,” Eurasian Soil Sci. 52, 193–205 (2019). https://doi.org/10.1134/S1064229319020108

    Article  Google Scholar 

  5. M. I. Makarov, I. S. Buzin, A. V. Tiunov, T. I. Malysheva, M. S. Kadulin, and N. E. Koroleva, “Nitrogen isotopes in soils and plants of tundra ecosystems in the Khibiny Mountains,” Eurasian Soil Sci. 52, 1194–1206 (2019). https://doi.org/10.1134/S1064229319100077

    Article  Google Scholar 

  6. M. I. Makarov, A. V. Volkov, T. I. Malysheva, and V. G. Onipchenko, “Phosphorus, nitrogen, and carbon in the soils of subalpine and alpine altitudinal belts of the Teberda Nature Reserve,” Eurasian Soil Sci. 34, 52–60 (2001).

    Google Scholar 

  7. M. I. Makarov, M. S. Kadulin, S. R. Turchin, T. I. Malysheva, A. A. Aksenova, V. G. Onipchenko, and O. V. Menyailo, “The effect of Vaccinium vitis-idaea on properties of mountain-meadow soil under alpine lichen heath,” Russ. J. Ecol. 50, 337–342 (2019). https://doi.org/10.1134/S1067413619040118

    Article  Google Scholar 

  8. M. I. Makarov, N. A. Leoshkina, A. A. Ermak, and T. I. Malysheva, “Seasonal dynamics of the mineral nitrogen forms in mountain-meadow alpine soils,” Eurasian Soil Sci. 43, 905–913 (2010).

    Article  Google Scholar 

  9. M. N. Maslov and M. I. Makarov, “Organic matter of the soil of the mountain tundra in North Fennoscandia,” Moscow Univ. Soil Sci. Bull. 68, 99–103 (2013).

    Article  Google Scholar 

  10. M. N. Maslov and M. I. Makarov, “Transformation of nitrogen compounds in the tundra soils of Northern Fennoscandia,” Eurasian Soil Sci. 49, 757-764 (2016). https://doi.org/10.1134/S1064229316070073

    Article  Google Scholar 

  11. E. V. Stolnikova, N. D. Ananyeva, and O. V. Chernova, “The microbial biomass and its activity and structure in the soils of old forests in the European Russia,” Eurasian Soil Sci. 44, 453–463 (2011).

    Article  Google Scholar 

  12. E. A. Susyan, N. D. Ananyeva, E. G. Gavrilenko, O. V. Chernova, and M. V. Bobrovskii, “Microbial biomass carbon in the profiles of forest soils of the southern taiga zone,” Eurasian Soil Sci. 42, 1148–1155 (2009).

    Article  Google Scholar 

  13. E. Bååth and T. H. Anderson, “Comparison of soil fungal/bacterial ratios in a pH gradient using physiological and PLFA based techniques,” Soil Biol. Biochem. 35, 955–963 (2003).

    Article  Google Scholar 

  14. J. B. Brant, E. W. Sulzman, and D. D. Myrold, “Microbial community utilization of added carbon substrates in response to long-term carbon input manipulation,” Soil Biol. Biochem. 38, 2219–2232 (2006).

    Article  Google Scholar 

  15. P. C. Brooks, A. Landman, G. Pruden, and D. S. Jenkinson, “Chloroform fumigation and release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen,” Soil Biol. Biochem. 17, 837–842 (1985).

    Article  Google Scholar 

  16. E. R. Brzostek, D. Dradoni, Z. A. Brown, and R. P. Phillips, “Mycorrhizal type determines the magnitude and direction of root-induced changes in decomposition in a temperate forest,” New Phytol. 206, 1274–1282 (2015).

    Article  Google Scholar 

  17. P.-L. Chagnon, F. Rineau, and C. Kaiser, “Mycorrhizas across scales: a journey between genomics, global patterns of biodiversity and biogeochemistry,” New Phytol. 209, 913–916 (2016).

    Article  Google Scholar 

  18. K. E. Clemmensen, R. D. Finlay, A. Dahlberg, J. Stenlid, D. A. Wardle, and B. D. Lindahl, “Carbon sequestration is related to mycorrhizal fungal community shifts during long-term succession in boreal forests,” New Phytol. 205, 1525–1536 (2015).

    Article  Google Scholar 

  19. F. A. Collier and M. I. Bidartondo, “Waiting for fungi: the ectomycorrhizal invasion of lowland heathlands,” J. Ecol. 97, 950–963 (2009).

    Google Scholar 

  20. J. V. Colpaert and A. van Laere, “A comparison of the extracellular enzyme activities of two ectomycorrhizal and a leaf-saprotrophic basidiomycete colonizing beech leaf litter,” New Phytol. 134, 133–141 (1996).

    Article  Google Scholar 

  21. P. E. Courty, M. Buée, A. G. Diedhiou, P. Frey-Klett, F. Le Tacon, F. Rineau, M.-P. Turpault, S. Uroz, and J. Garbaye, “The role of ectomycorrhizal communities in forest ecosystem processes: new perspectives and emerging concepts,” Soil Biol. Biochem. 42, 679–698 (2010).

    Article  Google Scholar 

  22. A. Frostegard, E. Bååth, and A. Tunlid, “Shifts in the structure of soil microbial communities in limed forests as revealed by phospholipid fatty-acid analysis,” Soil Biol. Biochem. 25, 723–730 (1993).

    Article  Google Scholar 

  23. M. Hallinger, M. Manthey, and M. Wilmking, “Establishing a missing link: Warm summers and winter snow cover promote shrub expansion into alpine tundra in Scandinavia,” New Phytol. 186, 890–899 (2010).

    Article  Google Scholar 

  24. M. G. A. van der Heijden, F. M. Martin, M. A. Selosse, and I. R. Sanders, “Mycorrhizal ecology and evolution: the past, the present, and the future,” New Phytol. 205, 1406–1423 (2015).

    Article  Google Scholar 

  25. S. N. Kivlin, S. M. Emery, and J. A. Rudgers, “Fungal symbionts alter plant responses to global change,” Am. J. Bot. 100, 1445–1457 (2013).

    Article  Google Scholar 

  26. T. E. C. Kraus, R. A. Dahlgren, and R. J. Zasoski, “Tannins in nutrient dynamics of forest ecosystems—a review,” Plant Soil. 256, 41–66 (2003).

    Article  Google Scholar 

  27. R. Liese, T. Lübbe, N. W. Albers, and I. C. Meier, “The mycorrhizal type governs root exudation and N uptake of temperate tree species,” Tree Physiol. 38, 83–95 (2018).

    Article  Google Scholar 

  28. G. Lin, M. L. McCormack, C. Ma, and D. Guo, “Similar below-ground carbon cycling dynamics but contrasting modes of nitrogen cycling between arbuscular mycorrhizal and ectomycorrhizal forests,” New Phytol. 213, 1440–1451 (2017).

    Article  Google Scholar 

  29. Q. Lin and P. C. Brookes, “Comparison of selective inhibition and biovolume measurements of microbial biomass and its community structure in unamended, ryegrass-amended, fumigated and pesticide-treated soils,” Soil Biol. Biochem. 31, 1999–2014 (1999).

    Article  Google Scholar 

  30. A. U. Mallik, “Conifer regeneration problems in boreal and temperate forests with ericaceous understories: role of disturbance, seedbed limitation, and keystone species change,” Crit. Rev. Plant Sci. 22, 341–366 (2003).

    Article  Google Scholar 

  31. M.-C. Marx, M. Wood, and S. C. Jarvis, “A microplate fluorometric assay for the study of enzyme diversity in soils,” Soil Biol. Biochem. 33, 1633–1640 (2001).

    Article  Google Scholar 

  32. W. B. McGill and C. V. Cole, “Comparative aspects of cycling of organic C, N, S and P through soil organic matter,” Geoderma 26, 267–286 (1981).

    Article  Google Scholar 

  33. Molecular Mycorrhizal Symbiosis, Ed. by F. Martin (Wiley, Chichester, 2016).

    Google Scholar 

  34. V. G. Onipchenko, M. I. Makarov, and E. van der Maarel, “Influence of alpine plants on soil nutrient concentrations in a monoculture experiment,” Folia Geobot. 36, 225–241 (2001).

    Article  Google Scholar 

  35. K. H. Orwin, M. U. F. Kirschbaum, M. G. St John, and I. A. Dickie, “Organic nutrient uptake by mycorrhizal fungi enhances ecosystem carbon storage: a model-based assessment,” Ecol. Lett. 14, 493–502 (2011).

    Article  Google Scholar 

  36. R. L. Phillips, D. R. Zak, W. E. Holmes, and D. C. White, “Microbial community composition and function beneath temperate trees exposed to elevated atmospheric carbon dioxide and ozone,” Oecologia 131, 236–244 (2002).

    Article  Google Scholar 

  37. R. P. Phillips, E. Brzostek, and M. G. Midgley, “The mycorrhizal-associated nutrient economy: a new framework for predicting carbon-nutrient couplings in temperate forests,” New Phytol. 199, 41–51 (2013).

    Article  Google Scholar 

  38. E. Post, M. C. Forchhammer, M. S. Bret-Harte, T. V. Callaghan, T. R. Christensen, B. Elberling, A. D. Fox, et al., “Ecological dynamics across the Arctic associated with recent climate change,” Science 325, 1355–1358 (2009).

    Article  Google Scholar 

  39. D. J. Read, J. R. Leake, and J. Perez-Moreno, “Mycorrhizal fungi as drivers of ecosystem processes in heathland and boreal forest biomes,” Can. J. Bot. 82, 1243–1263 (2004).

    Article  Google Scholar 

  40. N. V. Shekhovtsova, O. A. Marakaev, K. A. Pervushina, and G. A. Osipov, “The underground organ microbial complexes of moorland spotted orchid Dactylorhiza maculate (L.) Soó (Orchidaceae),” Adv. Biosci. Biotechnol. 4, 35–42 (2013).

    Article  Google Scholar 

  41. N. Soudzilovskaia, M. G. A. van der Heijden, J. H. C. Cornelissen, M. I. Makarov, V.G. Onipchenko, M. N. Maslov, A. A. Akhmetzanova, and P. M. van Bodegom, “Quantitative assessment of the differential impacts of arbuscular and ectomycorrhiza on soil carbon cycling,” New Phytol. 208, 280–293 (2015).

    Article  Google Scholar 

  42. M. V. Sørensen, R. Strimbeck, K. O. Nystuen, R. E. Kapas, B. Enquist, and B. J. Graae, “Draining the pool? Carbon storage and fluxes in three alpine plant communities,” Ecosystems 21, 316–330 (2018).

    Article  Google Scholar 

  43. B. N. Sulman, E. Shevliakova, E. R. Brzostek, S. N. Kivlin, S. Malyshev, D. N. L. Menge, and X. Zhang, “Diverse mycorrhizal associations enhance terrestrial C storage in a global model,” Global Biogeochem. Cycles 33, 501–523 (2019).

    Article  Google Scholar 

  44. L. L. Taylor, J. R. Leake, J. Quirk, K. Hardy, S. A. Banwart, and D. J. Beerling, “Biological weathering and the long-term carbon cycle: integrating mycorrhizal evolution and function into the current paradigm,” Geobiology 7, 171–191 (2009).

    Article  Google Scholar 

  45. M. K. Taylor, R. A. Lankau, and N. Wurzburger, “Mycorrhizal associations of trees have different indirect effects on organic matter decomposition,” J. Ecol. 104, 1576–1584 (2016).

    Article  Google Scholar 

  46. L. Tedersoo and M. Bahram, “Mycorrhizal types differ in ecophysiology and alter plant nutrition and soil processes,” Biol. Rev. 94, 1857–1880 (2019).

    Article  Google Scholar 

  47. E. D. Vance, P. C. Brookes, and D. S. Jenkinson, “An extraction method for measuring soil microbial biomass C,” Soil Biol. Biochem. 19, 703–707 (1987).

    Article  Google Scholar 

  48. D. C. White and D. B. Ringelberg, “Signature biolipid biomarker analysis,” in Techniques in Microbial Ecology, Ed. by R. S. Burlage, (Oxford University Press, Oxford, 1998), pp. 255–272.

    Google Scholar 

  49. N. Wurzburger and R. L. Hendrick, “Rhododendron thickets alter N cycling and soil extracellular enzyme activities in southern Appalachian hardwood forests,” Pedobiologia 50, 563–576 (2007).

    Article  Google Scholar 

  50. N. Wurzburger and R. L. Hendrick, “Plant litter chemistry and mycorrhizal roots promote a nitrogen feedback in a temperate forest,” J. Ecol. 97, 528–536 (2009).

    Article  Google Scholar 

  51. H. Yin, E. Wheeler, and R. P. Phillips, “Root-induced changes in nutrient cycling in forests depend on exudation rates,” Soil Biol. Biochem. 78, 213–221 (2014).

    Article  Google Scholar 

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Funding

This study was supported by the Russian Science Foundation, project no. 16-14-10208.

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Correspondence to M. I. Makarov.

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Translated by I. Bel’chenko

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Makarov, M.I., Malysheva, T.I., Kadulin, M.S. et al. The Effect of Ericoid Mycorrhizal and Ectomycorrhizal Plants on Soil Properties of Grass Meadow in Tundra of the Khibiny Mountains. Eurasian Soil Sc. 53, 569–579 (2020). https://doi.org/10.1134/S1064229320050087

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