Arbuscular Mycorrhizal Fungal Communities Pushed Over the Edge – Lessons from Extreme Ecosystems

Conference paper
Part of the Sustainability in Plant and Crop Protection book series (SUPP)

Abstract

The diversity and structure of soil microbial communities are crucial elements in understanding the ecological impacts of rapidly changing environments. One important group of soil microbes is the ubiquitous plant symbiotic arbuscular mycorrhizal (AM) fungi. Their diverse communities are shaped by complex interactions of their abiotic and biotic environments. Locally extreme ecosystems have proven to be useful for natural long-term experiments in the ecology and evolution of AM fungi, giving an insight into much-needed processes of adaptation and acclimation of natural communities to abiotic stress. For example, data from natural CO2 springs (mofettes) show that when exposed to extreme long-term stress (soil hypoxia and elevated soil CO2 concentrations) specific and temporary stable AM fungal communities form with a high abundance of specialised, stress-tolerant taxa. Moreover, in both natural– and human-impacted ecosystems there are several such cases. This chapter covers a wide range of extremes (abiotic stresses) in the pedosphere, from high to low temperatures, drought and floods, hypoxia, salinity, and soil pollution. An overview of several specific stressed environments where AM fungal community ecology has been studied is presented. In some of these cases, locally extreme environments have already been used and could further serve as a powerful tool to study slow ecological and evolutionary processes that normally require long-term observations and experiments to study them.

Keywords

Abiotic stress Arbuscular mycorrhizal fungi Soil biodiversity Community ecology Extreme ecosystems Global change Glomeromycota Microbial ecology Mofettes 

References

  1. Al-Yahya’ei, M. N., Oehl, F., Vallino, M., Lumini, E., Redecker, D., Wiemken, A., & Bonfante, P. (2010). Unique arbuscular mycorrhizal fungal communities uncovered in date palm plantations and surrounding desert habitats of Southern Arabia. Mycorrhiza, 21, 195–209.CrossRefPubMedPubMedCentralGoogle Scholar
  2. Appoloni, S., Lekberg, Y., Tercek, M. T., Zabinski, C. A., & Redecker, D. (2008). Molecular community analysis of arbuscular mycorrhizal fungi in roots of geothermal soils in Yellowstone National Park (USA). Microbial Ecology, 56, 649–659.CrossRefPubMedGoogle Scholar
  3. Baar, J., Paradi, I., Lucassen, E. C. H. E. T., Hudson-Edwards, K. A., Redecker, D., Roelofs, J. G. M., & Smolders, A. J. P. (2011). Molecular analysis of AMF diversity in aquatic macrophytes: A comparison of oligotrophic and utra-oligotrophic lakes. Aquatic Botany, 94, 53–61.CrossRefGoogle Scholar
  4. Clapp, J. P., Young, J. P. W., Merryweather, J. W., & Fitter, A. H. (1995). Diversity of fungal symbionts in arbuscular mycorrhizas from a natural community. New Phytologist, 130, 259–265.CrossRefGoogle Scholar
  5. Daniell, T. J., Husband, R., Fitter, A. H., & Young, J. P. W. (2001). Molecular diversity of arbuscular mycorrhizal fungi colonizing arable crops. FEMS Microbiology Ecology, 36, 203–209.CrossRefPubMedGoogle Scholar
  6. del Val, C., Barea, J. M., & Azon-Aguilar, C. (1999). Diversity of arbuscular mycorrhizal fungus populations in heavy-metal-contaminated soils. Applied and Environmental Microbiology, 65, 718–723.PubMedPubMedCentralGoogle Scholar
  7. Dumbrell, A. J., Nelson, M., Helgason, T., Dytham, C., Fitter, A. H., Nelson, H., Dytham, C., & Fitter, A. H. (2010). Relative roles of niche and neutral processes in structuring a soil microbial community. The ISME Journal, 4, 337–345.CrossRefPubMedGoogle Scholar
  8. Dumbrell, A. J., Ashton, P. D., Aziz, N., Feng, G., Nelson, M., Dytham, C., Fitter, A. H., & Helgason, T. (2011). Distinct seasonal assemblages of arbuscular mycorrhizal fungi revealed by massively parallel pyrosequencing. New Phytologist, 190, 794–804.CrossRefPubMedGoogle Scholar
  9. Dumbrell, A. J., Ferguson, R. M. W., & Clark, D. R. (2016). Microbial community analysis by single-amplicon high-throughput next generation sequencing: Data analysis – From raw output to ecology. In T. J. McGenity, K. N. Timmis, & B. Nogales (Eds.), Hydrocarbon and lipid microbiology protocols, Springer protocols handbooks. Heidelberg: Springer.Google Scholar
  10. Estrada, B., Beltran-Hermoso, M., Palenzuela, J., Iwase, K., Ruiz-Lozano, J. M., Barea, J. M., & Oehl, F. (2013). Diversity of arbuscular mycorrhizal fungi in the rhizosphere of Asteriscus maritimus (L.) Less., a representative plant species in arid and saline Mediterranean ecosystems. Journal of Arid Environments, 97, 170–175.CrossRefGoogle Scholar
  11. European Environment Agency. (2007). State of the environment No 1/2007 Chapter 2. Office for official publications of the European communities.Google Scholar
  12. European Science Foundation. (2007). Annual report. Available at http://www.esf.org/fileadmin/Public_documents/Publications/AnnualReport2007.pdf
  13. Fitter, A. H. (2005). Darkness visible: Reflections on underground ecology. Journal of Ecology, 93, 231–243.CrossRefGoogle Scholar
  14. Fitter, A. H., & Moyersoen, B. (1996). Evolutionary trends in root–microbe symbioses. Philosophical Transactions of the Royal Society B: Biological Sciences, 351, 1367–1375.CrossRefGoogle Scholar
  15. Francini, G., Männistö, M., Alaoja, V., & Kytöviita, M. M. (2014). Arbuscular mycorrhizal fungal community divergence within a common host plant in two different soils in a subarctic Aeolian sand area. Mycorrhiza, 24, 539–550.CrossRefPubMedGoogle Scholar
  16. Gostinčar, C., Grube, M., de Hoog, S., Zalar, P., & Gunde-Cimerman, N. (2010). Extremotolerance in fungi: evolution on the edge. Mini review. FEMS Microbiology Ecology, 71, 2–11.CrossRefPubMedGoogle Scholar
  17. Griffioen, W. A. J. (1994). Characterization of a heavy metal-tolerant endomycorrhizal fungus from the surroundings of a zinc refinery. Mycorrhiza, 4, 197–200.CrossRefGoogle Scholar
  18. Hanson, P. J., & Weltzin, J. F. (2000). Drought disturbance from climate change: Response of United States forests. Science of the Total Environment, 262, 205–220.CrossRefPubMedGoogle Scholar
  19. Harikumar, V. S., Blaszkowski, J., Medhanie, G., Kanagaraj, M. K., & Samuel, V. D. (2015). Arbuscular mycorrhizal fungi colonizing the plant communities in Eritrea, Northeast Africa. Applied Ecology and Environmental Research, 13, 193–203.Google Scholar
  20. Hassan, S. E. D., Boon, E., St-Arnaud, M., & Hijri, M. (2011). Molecular biodiversity of arbuscular mycorrhizal fungi in trace metal-polluted soils. Molecular Ecology, 20, 3469–3483.CrossRefGoogle Scholar
  21. Helgason, T., Daniell, T. J., Husband, R., Fitter, A. H., & Young, J. P. W. (1998). Ploughing up the wood-wide web? Nature, 394, 431.CrossRefPubMedGoogle Scholar
  22. Helgason, T., Merryweather, J. W., Denison, J., Wilson, P., Young, J. P. W., & Fitter, A. H. (2002). Selectivity and functional diversity in arbuscular mycorrhizas of co-occurring fungi and plants from a temperate deciduous woodland. Journal of Ecology, 90, 371–384.CrossRefGoogle Scholar
  23. Helgason, T., Merryweather, J. W., Young, J. P. W., & Fitter, A. H. (2007). Specificity and resilience in the arbuscular mycorrhizal fungi of a natural woodland community. Journal of Ecology, 95, 623–630.CrossRefGoogle Scholar
  24. Hirabayashi, Y., Mahendran, R., Koirala, S., Konoshima, L., Yamazaki, D., et al. (2013). Global flood risk under climate change. Nature Climate Change, 3, 816–821.CrossRefGoogle Scholar
  25. Hohberg, K., Schulz, H. J., Balkenhol, B., Pilz, M., Thomalla, A., et al. (2015). Soil faunal communities from mofette fields: Effects of high geogenic carbon dioxide concentration. Soil Biology Biochemistry, 88, 420–429.CrossRefGoogle Scholar
  26. Jansa, J., Mozafar, A., Kuhn, G., Anken, T., Ruh, R., et al. (2003). Soil tillage affects the community structure of mycorrhizal fungi in maize roots. Ecological Applications, 13, 1164–1176.CrossRefGoogle Scholar
  27. Kohout, P., Sýkorová, Z., Ctvrtlíková, M., Rydlová, J., Suda, J., et al. (2012). Surprising spectra of root-associated fungi in submerged aquatic plants. FEMS Microbiology Ecology, 80, 216–235.CrossRefPubMedGoogle Scholar
  28. Krishnamoorthy, R., Kim, K., Kim, C., & Sa, T. (2014). Changes of arbuscular mycorrhizal traits and community structure with respect to soil salinity in a coastal reclamation land. Soil Biology Biochemistry, 72, 1–10.CrossRefGoogle Scholar
  29. Lekberg, Y., Meadow, J., Rohr, J. R., Redecker, D., & Zabinski, C. A. (2011). Importance of dispersal and thermal environment for mycorrhizal communities: Lessons from Yellowstone National Park. Ecology, 92, 1292–1302.CrossRefPubMedGoogle Scholar
  30. Lemos, L. N., Fulthorpe, R. R., Triplett, E. W., & Roesch, L. F. W. (2011). Rethinking microbial diversity analysis in the high throughput sequencing era. Journal of Microbiological Methods, 86, 42–51.CrossRefPubMedGoogle Scholar
  31. Leyval, C., Turnau, K., & Haselwandter, K. (1997). Effect of heavy metal pollution on mycorrhizal colonization and function: Physiological, ecological and applied aspects. Mycorrhiza, 7, 139–153.CrossRefGoogle Scholar
  32. Maček, I. (2013). A decade of research in mofette areas has given us new insights into adaptation of soil microorganisms to abiotic stress. Acta Agriculturae Slovenica, 101, 209–217.Google Scholar
  33. Maček, I. (2017). Arbuscular mycorrhizal fungi in hypoxic environments. In A. Varma et al. (Eds.), Mycorrhiza – Function, diversity, state of art. Cham: Springer. doi:10.1007/978-3-319-53064-2_16.Google Scholar
  34. Maček, I., Dumbrell, A. J., Nelson, M., Fitter, A. H., Vodnik, D., & Helgason, T. (2011). Local adaptation to soil hypoxia determines the structure of an arbuscular mycorrhizal fungal community in roots from natural CO2 springs. Applied and Environmental Microbiology, 77, 4770–4777.CrossRefPubMedPubMedCentralGoogle Scholar
  35. Maček, I., Kastelec, D., & Vodnik, D. (2012). Root colonization with arbuscular mycorrhizal fungi and glomalin-related soil protein (GRSP) concentration in hypoxic soils from natural CO2 springs. Agricultural and Food Science, 21, 62–71.Google Scholar
  36. Maček, I., Vodnik, D., Pfanz, H., Low-Décarie, E., Dumbrell, A.J. (2016a). Locally extreme environments as natural long-term experiments in ecology. In: A. J. Dumbrell, R. Kordas, & G. Woodward (Eds), Advances in ecological research, large scale ecology: Model systems to global perspectives (Vol. 55). Elsevier Ltd.Google Scholar
  37. Maček, I., Šibanc, N., Kavšček, M., & Leštan, D. (2016b). Diversity of arbuscular mycorrhizal fungi in metal polluted and EDTA washed garden soils before and after soil revitalization with commercial and indigenous fungal inoculum. Ecological Engineering, 95, 330–339.CrossRefGoogle Scholar
  38. Merryweather, J. W., & Fitter, A. H. (1998). The arbuscular mycorrhizal fungi of Hyacinthoides non-scripta I. Diversity of fungal taxa. New Phytologist, 138, 117–129.CrossRefGoogle Scholar
  39. Millar, N., & Bennett, A. E. (2016). Stressed out symbiotes: Hypotheses for the influence of abiotic stress on arbuscular mycorrhizal fungi. Oecologia, doi:10.1007/s00442-016-3673-7.Google Scholar
  40. Moora, M., Öpik, M., Davison, J., Jairus, T., Vasar, M., et al. (2016). AM fungal communities inhabiting the roots of submerged aquatic plant Lobelia dortmanna are diverse and include a high proportion of novel taxa. Mycorrhiza, 26, 735–745.CrossRefPubMedGoogle Scholar
  41. Oehl, F., & Körner, C. (2014). Multiple mycorrhization at the coldest place known for Angiosperm plant life. Alpine Botany, 124, 193–198.CrossRefGoogle Scholar
  42. Oehl, F., Sieverding, E., Palenzuela, J., Ineichen, K., & da Silva, G. A. (2011). Advances in Glomeromycota taxonomy and classification. IMA Fungus, 2, 191–199.CrossRefPubMedPubMedCentralGoogle Scholar
  43. Oehl, F., Palenzuela, J., Sanchez-Castro, I., Kuss, P., Sieverding, E., & da Silva, G. A. (2012). Acaulospora nivalis, a new fungus in the Glomeromycetes, characteristic for high alpine and nival altitudes of the Swiss Alps. Nova Hedwigia, 95, 105–122.CrossRefGoogle Scholar
  44. Öpik, M., & Davison, J. (2016). Uniting species – And community-oriented approaches to understand arbuscular mycorrhizal fungal diversity. Fungal Ecology. doi:10.1016/j.funeco.2016.07.005.
  45. Öpik, M., Metsis, M., Daniell, T. J., Zobel, M., & Moora, M. (2009). Large-scale parallel 454 sequencing reveals host ecological group specificity of arbuscular mycorrhizal fungi in a boreonemoral forest. New Phytologist, 184, 424–437.CrossRefPubMedGoogle Scholar
  46. Öpik, M., Zobel, M., Cantero, J. J., Davison, J., Facelli, J. M., et al. (2013). Global sampling of plant roots expands the described molecular diversity of arbuscular mycorrhizal fungi. Mycorrhiza, 23, 411–430.CrossRefPubMedGoogle Scholar
  47. Öpik, M., Davison, J., Moora, M., & Zobel, M. (2014). DNA-based detection and identification of Glomeromycota: The virtual taxonomy of environmental sequences. The Botanical Review, 147, 135–147.Google Scholar
  48. Pawlowska, T. E., Blaszkowski, J., & Rühling, A. (1996). The mycorrhizal status of plants colonizing a calamine spoil mound in southern Poland. Mycorrhiza, 6, 499–505.CrossRefGoogle Scholar
  49. Read, D. J. (1991). Mycorrhizas in ecosystems. Experientia, 47, 376–391.CrossRefGoogle Scholar
  50. Redecker, D., Kodner, R., & Graham, L. E. (2002). Palaeoglonius grayi from the Ordovician. Mycotaxon, 84, 33–37.Google Scholar
  51. Renker, C., Blanke, V., & Buscot, F. (2005). Diversity of arbuscular mycorrhizal fungi in grassland spontaneously developed on area polluted by a fertilizer plant. Environmental Pollution, 135, 255–266.CrossRefPubMedGoogle Scholar
  52. Roesch, L. F. W., Fulthorpe, R. R., Riva, A., Casella, G., Hadwin, A. K. M., et al. (2007). Pyrosequencing enumerates and contrasts soil microbial diversity. The ISME Journal, 1, 283–290.PubMedPubMedCentralGoogle Scholar
  53. Rosendahl, S. (2008). The first glance into the Glomus genome: An ancient asexual scandal with meiosis? New Phytologist, 193, 546–548.CrossRefGoogle Scholar
  54. Schloss, P. D. (2009). A high-throughput DNA sequence aligner for microbial ecology studies. PloS One, 4, e8230.CrossRefPubMedPubMedCentralGoogle Scholar
  55. Schulz, H. J., & Potapov, M. B. (2010). A new species of Folsomia from mofette fields of the Northwest Czechia (Collembola, Isotomidae). Zootaxa, 2553, 60–64.Google Scholar
  56. Schüßler, A. (2008). Glomeromycota species list. Available at: http://schuessler.userweb.mwn.de/amphylo/
  57. Schüßler, A., & Walker, C. (2010). The Glomeromycota: A species list with new families and new genera. The Royal Botanic Garden Edinburgh (UK), The Royal Botanic Garden, Kew (UK), Botanische Staatssammlung Munich (DE), and Oregon State University, Gloucester (USA). Available online at http://www.amf-phylogeny.com
  58. Šibanc, N., Dumbrell, A. J., Mandić-Mulec, I., & Maček, I. (2014). Impacts of naturally elevated soil CO2 concentrations on communities of soil archaea and bacteria. Soil Biology Biochemistry, 68, 348–356.CrossRefGoogle Scholar
  59. Smith, S. E., & Read, D. J. (2008). Mycorrhizal symbiosis (3rd ed.787 pp). Academic: London.Google Scholar
  60. Smolders, A. J. P., Lucassen, E., & Roelofs, J. G. M. (2002). The isoetid environment: biogeochemistry and threats. Aquatic Botany, 73, 325–350.CrossRefGoogle Scholar
  61. Sonjak, S., Beguiristain, T., Leyval, C., & Regvar, M. (2009). Temporal temperature gradient gel electrophoresis (TTGE) analysis of arbuscular mycorrhizal fungi associated with selected plants from saline and metal polluted environments. Plant and Soil, 314, 25–34.CrossRefGoogle Scholar
  62. Sudová, R., Sýkorová, Z., Rydlová, J., Čtvrtlíková, M., & Oehl, F. (2015). Rhizoglomus melanum, a new arbuscular mycorrhizal fungal species associated with submerged plants in freshwater lake Avsjøen in Norway. Mycological Progress, 14, 1–9.CrossRefGoogle Scholar
  63. Symanczik, S., Blaszkowski, J., Koegel, S., Boller, T., Wiemken, A., & Al-Yahya’ei, M. (2014a). Isolation and identification of desert habituated arbuscular mycorrhizal fungi newly reported from the Arabian Peninsula. Journal of Arid Land, 6, 488–497.CrossRefGoogle Scholar
  64. Symanczik, S., Blaszkowski, J., Chwat, G., Boller, T., Wiemken, A., & Al-Yahya’ei, M. N. (2014b). Three new species of arbuscular mycorrhizal fungi discovered at one location in a desert of Oman: Diversispara omaniana, Septoglomus nakheelum and Rhizophagus arabicus. Mycologia, 106, 243–259.CrossRefPubMedGoogle Scholar
  65. Tedersoo, L., Pärtel, K., Jairus, T., Gates, G., Põldmaa, K., & Tamm, H. (2009). Ascomycetes associated with ectomycorrhizas: molecular diversity and ecology with particular reference to the Helotiales. Environmental Microbiology, 11, 3166–3178.CrossRefPubMedGoogle Scholar
  66. Tedersoo, L., Bahram, M., Ryberg, M., Otsing, E., Kõljalg, U., & Abarenkov, K. (2014). Global biogeography of the ectomycorrhizal/sebacina lineage (Fungi, Sebacinales) as revealed from comparative phylogenetic analyses. Molecular Ecology, 23, 4168–4183.CrossRefPubMedGoogle Scholar
  67. Toju, H., Tanabe, A. S., & Ishii, H. S. (2016). Ericaceous plant-fungus network in a harsh alpine-subalpine environment. Molecular Ecology, 25, 3242–3257.CrossRefPubMedGoogle Scholar
  68. Vallino, M., Massa, N., Lumini, E., Bianciotto, V., Berta, G., & Bonfante, P. (2006). Assessment of arbuscular mycorrhizal fungal diversity in roots of Solidago gigantea growing in a polluted soil in Northern Italy. Environmental Microbiology, 8, 971–983.CrossRefPubMedGoogle Scholar
  69. van der Heijden, M. G. A., Martin, F. M., Selosse, M., & Sanders, I. R. (2015). Mycorrhizal ecology and evolution: The past, the present, and the future. New Phytologist, 205, 1406–1423.CrossRefPubMedGoogle Scholar
  70. Varga, S., Finozzi, C., Vestberg, M., & Kytöviita, M. (2015). Arctic arbuscular mycorrhizal spore community and viability after storage in cold conditions. Mycorrhiza, 25, 335–343.CrossRefPubMedGoogle Scholar
  71. Vodnik, D., Kastelec, D., Pfanz, H., Maček, I., & Turk, B. (2006). Small-scale spatial variation in soil CO2 concentration in a natural carbon dioxide spring and some related plant responses. Geoderma, 133, 309–319.CrossRefGoogle Scholar
  72. Vodnik, D., Videmšek, U., Pintar, M., Maček, I., & Pfanz, H. (2009). The characteristics of soil CO2 fluxes at a site with natural CO2 enrichment. Geoderma, 150, 32–37.CrossRefGoogle Scholar
  73. Walker, C., & Trappe, J. M. (1993). Names and epithets in the Glomales and Endogonales. Mycological Research, 97, 339–344.CrossRefGoogle Scholar
  74. Whitfield, L., Richards, A. J., & Rimmer, D. L. (2004). Relationships between soil heavy metal concentration and mycorrhizal colonization in Thymus polytrichus in northern England. Mycorrhiza, 14, 55–62.CrossRefPubMedGoogle Scholar
  75. Wigand, C., Andersen, F. O., Christensen, K. K., Holmer, M., & Jensen, H. S. (1998). Endomycorrhizae of isoetids along a biogeochemical gradient. Limnology and Oceanography, 43, 508–515.CrossRefGoogle Scholar
  76. Wilde, P., Manal, A., Stodden, M., Sieverding, E., Hildebrandt, U., & Bothe, H. (2009). Biodiversity of arbuscular mycorrhizal fungi in roots and soils of two salt marshes. Environmental Microbiology, 11, 1548–1561.CrossRefPubMedGoogle Scholar
  77. Yamato, M., Ikeda, S., & Iwase, K. (2008). Community of arbuscular mycorrhizal fungi in a coastal vegetation on Okinawa island and effect of the isolated fungi on growth of sorghum under salt-treated conditions. Mycorrhiza, 18, 241–249.CrossRefPubMedGoogle Scholar
  78. Yamato, M., Yagame, T., Yoshimura, Y., & Iwase, K. (2012). Effect of environmental gradient in coastal vegetation on communities of arbuscular mycorrhizal fungi associated with Ixeris repens (Asteraceae). Mycorrhiza, 22, 623–630.CrossRefPubMedGoogle Scholar
  79. Zarei, M., König, S., Hempel, S., Nekouei, M. K., Savaghebi, G., & Buscot, F. (2008). Community structure of arbuscular mycorrhizal fungi associated to Veronica rechingeri at the Anguran zinc and lead mining region. Environmental Pollution, 156, 1277–1283.CrossRefPubMedGoogle Scholar
  80. Zarei, M., Hempel, S., Wubet, T., Schäfer, T., Savaghebi, G., et al. (2010). Molecular diversity of arbuscular mycorrhizal fungi in relation to soil chemical properties and heavy metal contamination. Environmental Pollution, 158, 2757–2765.CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Biotechnical FacultyUniversity of LjubljanaLjubljanaSlovenia
  2. 2.Faculty of Mathematics, Natural Sciences and Information Technologies (FAMNIT)University of PrimorskaKoperSlovenia

Personalised recommendations