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Testate Amoebae (Arcellinida and Euglyphida) vs. Ericoid Mycorrhizal and DSE Fungi: A Possible Novel Interaction in the Mycorrhizosphere of Ericaceous Plants?

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Abstract

Common occurrence of testate amoebae (TA) in the rhizosphere of mycorrhizal plants indicates existence of yet undocumented ecological interactions, involving three distinct groups of organisms: soil protists, mycorrhizal fungi, and their host plants. This tripartite relationship was to date investigated only to a limited extent, despite its probable importance for processes taking place in the mycorrhizosphere. In this study, we (1) explored spectra of different TA genera naturally associated with the rhizoplane of three autochthonous European Rhododendron species, (2) screened natural fungal colonization of the TA shells occupying the rhizoplane of selected rhododendrons, and (3) carried out two in vitro experiments addressing the question whether TA shells may serve as a nutrient source for ericoid mycorrhizal fungi (ErMF) and dark septate endophytes (DSE). Our field observations indicated that TA regularly associated with the rhizoplane of all screened rhododendrons and that ErMF and/or DSE associated with their roots possibly exploited the TA shells as a nutrient source. We were unable to detect any major differences among the TA spectra from the rhizoplanes with respect to the three Rhododendron species. The spectra were dominated by Diplochlamys, Centropyxis, Cyclopyxis, Euglypha, Trinema, and Assulina. Positive, neutral, and negative associations were found for various TA genera × Rhododendron species combinations. The highest fungal colonization was observed in Centropyxidae and Trigonopyxidae, reaching up to 45% of the shells in the case of Trigonopyxis. In the in vitro experiments, both ErMF Rhizoscyphus ericae and DSE Phialocephala fortinii regularly colonized TA shells, utilizing them as a source of nutrients. We hypothesize a complex relationship between ErMF–DSE and TA. If corroborated, it would represent an interesting nutrient loop in the mycorrhizosphere of ericaceous plants.

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References

  1. Alekperov I, Snegovaya N (2000) The fauna of testate amoebae (Rhizopoda, Testacea) in freshwater basins of Apsheron peninsula. Protistology 1:135–147

    Google Scholar 

  2. Aoki Y, Hoshino M, Matsubara T (2007) Silica and testate amoebae in a soil under pine-oak forest. Geoderma 142:29–35

    Article  CAS  Google Scholar 

  3. Bajwa R, Read DJ (1985) The biology of mycorrhiza in the Ericaceae: IX. Peptides as nitrogen sources for mycorrhizal and non-mycorrhizal plants. New Phytol 101:459–467

    Article  CAS  Google Scholar 

  4. Bajwa R, Abuarghub S, Read DJ (1985) The biology of mycorrhiza in the Ericaceae. X. The utilization of proteins and the production of proteolytic enzymes by mycorrhizal plants. New Phytol 101:469–486

    Article  CAS  Google Scholar 

  5. Baláž M, Vosátka M (2001) A novel inserted membrane technique for studies of mycorrhizal extraradical mycelium. Mycorrhiza 11:291–296

    Article  CAS  Google Scholar 

  6. Balík V (1990) Zur Kenntnis der Bodentestaceen (Rhizopoda: Testacea) Südböhmens. Act Mus Boh Meridion in Č. Budějovice 30:1–12 [in Czech with German summary]

    Google Scholar 

  7. Balík V (1992a) Krytenky (Rhizopoda, Testacea) z několika lokalit z chráněné krajinné oblasti Beskydy (Severní Morava, ČSFR). Čas Slez Muz Opava 41:31–40 [in Czech with English summary]

    Google Scholar 

  8. Balík V (1992b) Testate amoebae fauna (Protozoa, Rhizopoda, Testacea) from the marsh habitats in the Krkonoše Mountains National Park (Czechoslovakia). Opera Corcontica 29:139–154 [in Czech with English summary]

    Google Scholar 

  9. Balík V (1992c) Die Testaceen (Rhizopoda, Testacea) aus dem Naturschutzgebiet Trojmezná hora im Böhmerwald (Tschechoslowakei). Act Mus Boh Meridion in Č. Budějovice 32:69–78 [in Czech with German summary]

    Google Scholar 

  10. Balík V (1994) Testaceenfauna (Protozoa, Rhizopoda, Testacea) aus dem Naturschutzgebiet Žofínský prales (Novohradské hory Gebirge) in Südböhmen (Tschechische Republik). Act Mus Boh Meridion in Č. Budějovice 34:55–67 [in Czech with German summary]

    Google Scholar 

  11. Balík V (1997) Fauna krytenek (Protozoa, Testacea) západní části Tatranského Národního Parku (Slovenská Republika). Štúdie o Tatranskom Národnom Parku 2:103–122 [in Czech]

    Google Scholar 

  12. Bartoš E (1954) Koreňonožce radu Testacea. Vydavaťelstvo Slovenskej Akadémie Vied, Bratislava, pp 1–185 [in Slovak]

    Google Scholar 

  13. Bonkowski M (2004) Protozoa and plant growth: the microbial loop in soil revisited. New Phytol 162:617–631

    Article  Google Scholar 

  14. Bonkowski M, Cheng W, Griffiths BS, Alphei J, Scheu S (2000) Microbial–faunal interactions in the rhizosphere and effects on plant growth. Eur J Soil Biol 36:135–147

    Article  Google Scholar 

  15. Bonkowski M, Jentschke G, Scheu S (2001) Contrasting effects of microbial partners in the rhizosphere: interactions between Norway Spruce seedlings (Picea abies Karst.), mycorrhiza (Paxillus involutus (Batsch) Fr.) and naked amoebae (protozoa). Appl Soil Ecol 18:193–204

    Article  Google Scholar 

  16. Brundrett M, Bougher N, Dell B, Grove T, Malajczuk N (1996) Working with mycorrhizas in forestry and agriculture. ACIAR Monograph 32. ACIAR, Canberra, p 374

    Google Scholar 

  17. Cairney JWG, Meharg AA (2003) Ericoid mycorrhiza: a partnership that exploits harsh edaphic conditions. Eur J Soil Sci 54:735–740

    Article  Google Scholar 

  18. Coûteaux M-M (1985) Relationships between testate amoebae and fungi in humus microcosms. Soil Biol Biochem 17:339–345

    Article  Google Scholar 

  19. Coûteaux M-M, Darbyshire JF (1998) Functional diversity amongst soil protozoa. Appl Soil Ecol 10:229–237

    Article  Google Scholar 

  20. Cross JR (1975) Rhododendron ponticum L. J Ecol 63:345–364

    Article  Google Scholar 

  21. Deflandre G (1929) Le genre Centropyxis Stein. Archiv für Protistenkunde 67:322–375 [in French]

    Google Scholar 

  22. Deflandre G (1936) Etude monographique sur le genre Nebela Leidy. Annales de Protistologie 5:201–286 [in French]

    Google Scholar 

  23. Fitter AH, Garbaye J (1994) Interactions between mycorrhizal fungi and other soil organisms. Plant Soil 159:123–132

    Google Scholar 

  24. Foissner W (1987) Soil protozoa: fundamental problems, ecological significance, adaptations in Ciliates and Testaceans, bioindicators, and guide to the literature. Prog Protistol 2:69–212

    Google Scholar 

  25. Foissner W, Korganova GA (2000) The Centropyxis aerophila complex (Protozoa: Testacea). Acta Protozool 39:257–273

    Google Scholar 

  26. Gilbert D, Amblard C, Bourdier G, Francez A-J (1998a) The microbial loop at the surface of a peatland: structure, function, and impact of nutrient input. Microb Ecol 35:83–93

    Article  PubMed  CAS  Google Scholar 

  27. Gilbert D, Amblard C, Bourdier G, Francez A-J (1998b) Short-term effect of nitrogen enrichment on the microbial communities of a peatland. Hydrobiologia 373–374:111–119

    Article  Google Scholar 

  28. Gilbert D, Mitchell EAD, Amblard C, Bourdier G, Francez A-J (2003) Population dynamics and food preferences of the testate amoeba Nebela tincta major-bohemica-collaris complex (Protozoa) in a Sphagnum peatland. Acta Protozool 42:99–104

    Google Scholar 

  29. Grünig CR, McDonald BA, Sieber TN, Rogers SO, Holdenrieder O (2004) Evidence for subdivision of the root-endophyte Phialocephala fortinii into cryptic species and recombination within species. Fungal Genet Biol 41:676–687

    Article  PubMed  CAS  Google Scholar 

  30. Hammer R, Harper DAT, Ryan PD (2001) PAST: Palaeontological Statistics software package for education and data analysis. Palaeontol Electronica 4:9

    Google Scholar 

  31. Hedley RH (1963) Cement and iron in the arenaceous foraminifera. Micropaleontology 9:433–441

    Article  CAS  Google Scholar 

  32. Ingham ER, Massicotte HB (1994) Protozoan communities around conifer roots colonized by ectomycorrhizal fungi. Mycorrhiza 5:53–61

    Article  Google Scholar 

  33. Jaccard P (1908) Nouvelles recherches sur la distribution florale. Bull Soc Vaud Sci Nat 44:223–270 [in French]

    Google Scholar 

  34. Joyon L, Charret R (1962) Sur l’ultrastructure du Thécamoebien Hyalosphenia papilo (Leidy). C R Acad Sci 255:2661–2663 [in French]

    Google Scholar 

  35. Jumpponen A (2001) Dark septate endophytes—are they mycorrhizal? Mycorrhiza 11:207–211

    Article  Google Scholar 

  36. Jumpponen A, Trappe JM (1998) Dark septate endophytes: a review of facultative biotrophic root-colonizing fungi. New Phytol 140:295–310

    Article  Google Scholar 

  37. Kerley SJ, Read DJ (1995) The biology of mycorrhiza in the Ericaceae. XVIII. Chitin degradation by Hymenoscyphus ericae and transfer of chitin–nitrogen to the host plant. New Phytol 131:369–375

    Article  CAS  Google Scholar 

  38. Kerley SJ, Read DJ (1997) The biology of mycorrhiza in the Ericaceae. XIX. Fungal mycelium as a nitrogen source for the ericoid mycorrhizal fungus Hymenoscyphus ericae and its host plant. New Phytol 136:691–701

    Article  Google Scholar 

  39. Kerley SJ, Read DJ (1998) The biology of mycorrhiza in the Ericaceae. XX. Plant and mycorrhizal necromass as nitrogenous substrates for ericoid mycorrhizal fungus Hymenoscyphus ericae and its host. New Phytol 139:353–360

    Article  Google Scholar 

  40. Klironomos JN, Hart MM (2001) Animal nitrogen swap for plant carbon. Nature 410:651–652

    Article  PubMed  CAS  Google Scholar 

  41. Mandyam K, Jumpponen A (2005) Seeking the elusive function of the root-colonising dark septate endophytic fungi. Stud Mycol 53:173–189

    Article  Google Scholar 

  42. Mitchell EAD, Charman DJ, Warner BG (2008) Testate amoebae analysis in ecological and paleoecological studies of wetlands: past, present and future. Biodivers Conserv doi:10.1007/s10531-007-9221-3

  43. Morcazewski J (1961) Testacea du littoral peu profound du lac Kisajno (Region des lacs de Mazurie). Polskie Archiwum Hydrobiol 9:175–194 [in Polish and French]

    Google Scholar 

  44. Morisita M (1959) Measuring the dispersion of individuals and analysis of the distributional patterns. Mem Fac Sci Kyushu Univ Ser E (Biol) 2:215–233

    Google Scholar 

  45. Nilsen ET, Walker JF, Miller OK, Semones SW, Lei TT, Clinton BD (1999) Inhibition of seedling survival under Rhododendron maximum (Ericaceae): could allelopathy be a cause? Am J Bot 86:1597–1605

    Article  PubMed  Google Scholar 

  46. Ogden CG, Hedley RH (1980) An atlas of freshwater testate amoebae. Oxford University Press, Oxford, p 222

    Google Scholar 

  47. Patterson RT, Dalby A, Kumar A, Henderson LA, Boudreau EA (2002) Arcellaceans (thecamoebians) as indicators of land-use change: settlement history of the Swan Lake area, Ontario as a case study. J Paleolimn 28:297–316

    Article  Google Scholar 

  48. Pearson V, Read DJ (1973) The biology of mycorrhiza in the Ericaceae. I. The isolation of the endophyte and synthesis of mycorrhiza in aseptic culture. New Phytol 72:371–379

    Article  Google Scholar 

  49. Read DJ (1996) The structure and function of the ericoid mycorrhizal root. Ann Bot 77:365–374

    Article  CAS  Google Scholar 

  50. Read DJ, Perez-Moreno J (2003) Mycorrhizas and nutrient cycling in ecosystems—a journey towards relevance? New Phytol 157:475–492

    Article  Google Scholar 

  51. Read DJ, Leake JR, Perez-Moreno J (2004) Mycorrhizal fungi as drivers of ecosystem processes in heathland and boreal forest biomes. Can J Bot 82:1243–1263

    Article  CAS  Google Scholar 

  52. Real R, Vargas JM (1996) The probabilistic basis of Jaccard’s index of similarity. Syst Biol 45:380–385

    Article  Google Scholar 

  53. Rydlová J, Vosátka M (2000) Sporulation of symbiotic arbuscular mycorrhizal fungi inside dead seeds of a non-host plant. Symbiosis 29:231–248

    Google Scholar 

  54. Rydlová J, Batkhuugyin E, Vosátka M (2004) Sporulation of four arbuscular mycorrhizal fungi isolates inside dead seed cavities and glass capillaries. Symbiosis 36:269–284

    Google Scholar 

  55. Schröter D, Brussaard L, De Deyn G, Poveda K, Brown VK, Berg MP, Wardle DA, Moore J, Wall DH (2004) Trophic interactions in a changing world: modelling aboveground–belowground interactions. Basic Appl Ecol 5:515–528

    Article  Google Scholar 

  56. Smith SE, Read DJ (1997) Mycorrhizal Symbiosis, 2nd edn. Academic, London, pp 323–345

    Google Scholar 

  57. Sutton CA, Wilkinson DM (2007) The effects of Rhododendron on testate amoebae communities in woodland soils in North West England. Acta Protozool 46:333–338

    Google Scholar 

  58. Vargas R (1990) Avances en microbiologia de suelos: los protozoarios y su importancia en la mineralizacion del nitrogeno. Agronomía Costarricense 14(1):121–134 [in Spanish]

    Google Scholar 

  59. Vohník M, Lukančič S, Bahor E, Regvar M, Vosátka M, Vodnik D (2003) Inoculation of Rhododendron cv. Belle-Heller with two strains of Phialocephala fortinii in two different substrates. Folia Geobotanica 38:191–200

    Article  Google Scholar 

  60. Vohník M, Albrechtová J, Vosátka M (2005) The inoculation with Oidiodendron maius and Phialocephala fortinii alters phosphorus and nitrogen uptake, foliar C:N ratio and root biomass distribution in Rhododendron cv. Azurro. Symbiosis 40:87–96

    Google Scholar 

  61. Vohník M, Fendrych M, Albrechtová J, Vosátka M (2007) Intracellular colonization of Rhododendron and Vaccinium roots by Cenococcum geophilum, Geomyces pannorum and Meliniomyces variabilis. Folia Microbiologica 52:407–414

    Article  PubMed  Google Scholar 

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Acknowledgments

This study was supported by the Academy of Sciences of the Czech Republic (research projects AV0Z60050516 and AV0Z50110509) and Ministry of Education, Youth, and Sports of the Czech Republic (research program LC06063). M. Vohník was financially supported by the Grant Agency of the Czech Republic (GACR 206/03/H137). The authors thank Dominik Vodnik, Simon Lukančič, and Matyáš Fendrych for help with collection of the environmental samples, Vladimír Balík and Alena Kubátová for useful information at the beginning of the work and Edward A. D. Mitchell, David M. Wilkinson, and anonymous reviewers for valuable comments on earlier versions of the manuscript.

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Authors and Affiliations

  1. Department of Mycorrhizal Symbioses, Institute of Botany, Academy of Sciences of the Czech Republic (ASCR), Lesní 323, Průhonice, 252 43, Czech Republic

    M. Vohník, J. Albrechtová & M. Vosátka

  2. Department of Plant Physiology, Faculty of Science, Charles University in Prague, Viničná 5, 128 44, Prague, Czech Republic

    M. Vohník & J. Albrechtová

  3. Department of Paleontology, Faculty of Science, Charles University in Prague, Albertov 6, 128 44, Prague, Czech Republic

    Z. Burdíková

  4. Department of Biomathematics, Institute of Physiology, Academy of Sciences of the Czech Republic (ASCR), Vídeňská 1083, 142 20, Prague, Czech Republic

    Z. Burdíková

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  1. M. Vohník
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Vohník, M., Burdíková, Z., Albrechtová, J. et al. Testate Amoebae (Arcellinida and Euglyphida) vs. Ericoid Mycorrhizal and DSE Fungi: A Possible Novel Interaction in the Mycorrhizosphere of Ericaceous Plants?. Microb Ecol 57, 203–214 (2009). https://doi.org/10.1007/s00248-008-9402-y

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