Skip to main content
SpringerLink
Log in

Interactions Between Testate Amoebae and Saprotrophic Microfungi in a Scots Pine Litter Microcosm

  • Soil Microbiology
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

In all terrestrial ecosystems, testate amoebae (TA) encounter fungi. There are strong indications that both groups engage in multiple interactions, including mycophagy and decomposition of TA shells, processes which might be fundamental in nutrient cycling in certain ecosystems. Here, we present the results of an experiment focusing on interactions between TA and saprotrophic microfungi colonizing Scots pine (Pinus sylvestris L.) litter needles. The needles were collected from a temperate pine forest and cultivated in damp chambers. Over a few weeks, melanized mycelium of Anavirga laxa Sutton started to grow out of some needles; simultaneously, the common forest-soil TA Phryganella acropodia (Hertwig and Lesser) Hopkinson reproduced and spread around the mycelium. We investigated whether a potential relationship between TA and saprotrophic microfungi exists by comparing the composition of TA communities on and around the needles and testing the spatial relationship between the A. laxa mycelium and P. acropodia shells in the experimental microcosm. Additionally, we asked whether P. acropodia utilized the A. laxa mycelium as a nutrient source and screened whether P. acropodia shells were colonized by the microfungi inhabiting the experimental microcosm. Our results indicate that saprotrophic microfungi may affect the composition of TA communities and their mycelium may affect distribution of TA individuals in pine litter. Our observations suggest that P. acropodia did not graze directly on A. laxa mycelium, but rather fed on its exudates or bacteria associated with the exudates. The fungus Pochonia bulbillosa (Gams & Malla) Zare & Gams was often found parasitising encysted shells or decomposing already dead individuals of P. acropodia. TA and pine litter microfungi engage in various direct and indirect interactions which are still poorly understood and deserve further investigation. Their elucidation will improve our knowledge on fundamental processes influencing coexistence of soil microflora and microfauna.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5

Similar content being viewed by others

References

  1. 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 

  2. Balík V (1992) Testate amoebae fauna (Protozoa, Rhizopoda, Testacea) from the marsh habitats in the Krkonoše Mountains National Park (Czechoslovakia). Opera Corcontica 29:139–154

    Google Scholar 

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

    Google Scholar 

  4. Bamforth SS (1971) Numbers and proportions of Testacea and Ciliates in litters and soils. J Protozool 18:24–28

    Google Scholar 

  5. Bartoš E (1954) Koreňonožce radu Testacea. Vydavaťelstvo Slovenskej Akadémie Vied, Bratislava, pp 1–185

    Google Scholar 

  6. 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 

  7. Chakraborty S, Theodorou C, Bowen GD (1985) The reduction of root colonization by mycorrhizal fungi by mycophagous amebas. Can J Microbiol 31:295–297

    Article  Google Scholar 

  8. Coleman DC (2008) From peds to paradoxes: linkages between soil biota and their influences on ecological processes. Soil Biol Biochem 40:271–289

    Article  CAS  Google Scholar 

  9. Coûteaux MM (1975) Écologie des thécamoebiens de quelques humus bruts forestiers. Rev Écol Biol Sol 12:421–447

    Google Scholar 

  10. Coûteaux MM (1976) Dynamisme de l’equilibre des thécamoebiens dans quelques sols climaciques. Mem Mus Natl Hist Nat A Zool 96:1–183

    Google Scholar 

  11. Coûteaux MM, Dévaux J (1983) Effet d’un enrichissement en champignons sur la dynamique d’un peuplement thécamoebien d’un humus. Rev Écol Biol Sol 20:519–545

    Google Scholar 

  12. Coûteaux MM (1985) Relationships between testate amebas and fungi in humus microcosms. Soil Biol Biochem 17:339–345

    Article  Google Scholar 

  13. Couteaux MM, Darbyshire JF (1998) Functional diversity amongst soil protozoa. Appl Soil Ecol 10:229–237

    Article  Google Scholar 

  14. Couteaux MM (1992) Decomposition of cells and empty shells of testate amebas (Rhizopoda, Testacea) in an organic-acid soil sterilized by propylene-oxide fumigation, autoclaving, and gamma-ray irradiation. Biol Fert Soil 12:290–294

    Article  Google Scholar 

  15. Deflandre G (1929) Le genre Centropyxis Stein. Arch Protistenkd 67:322–375

    Google Scholar 

  16. Deflandre G (1936) Etude monographique sur le genre Nebela Leidy. Ann Protistologie 5:201–286

    Google Scholar 

  17. De Santo AV, Rutigliano FA, Berg B, Fioretto A, Puppi G, Alfani A (2002) Fungal mycelium and decomposition of needle litter in three contrasting coniferous forests. Acta Oecol 23:247–259

    Article  Google Scholar 

  18. Ellis MB, Ellis JP (1997) Microfungi on land plants. Richmond Publishing, Slough

    Google Scholar 

  19. Fassatiová O, Lysek H (1982) Ovicidal fungi in soil ecological system. Acta Univ Carol Biol 9:297–334

    Google Scholar 

  20. Gilbert D, Amblard C, Bourdier G, Francez A-J (1998) 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 

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

    Article  Google Scholar 

  22. 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 

  23. Goreaud F, Pelissier R (2003) Avoiding misinterpretation of biotic interactions with the intertype K12-function: population independence vs. random labeling hypotheses. J Veget Sci 14:681–692

    Google Scholar 

  24. Hammer Ř, Harper DAT, Ryan PD (2001) PAST: palaeontological statistics software package for education and data analysis. Palaeontol Electronica 4:9

    Google Scholar 

  25. Han BP, Wang T, Lin QQ, Dumont HJ (2008) Carnivory and active hunting by the planktonic testate amoeba Difflugia tuberspinifera. Hydrobiologia 596:197–201

    Article  Google Scholar 

  26. Hayes AJ (1965) Some microfungi from Scots pine litter. Trans Br Mycol Soc 48:179–185

    Article  Google Scholar 

  27. Hogberg MN, Hogberg P (2002) Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved organic carbon in a forest soil. New Phytol 154:791–795

    Article  CAS  Google Scholar 

  28. Hasna I, Rämert L (2007) Food attraction and population growth of fungivorous nematodes with different fungi. Ann Appl Biol 151:175–182

    Article  Google Scholar 

  29. Illian J, Penttinen A, Stoyan H, Stoyan D (2008) Statistical analysis and modelling of spatial point patterns. Wiley-Interscience, Chichester

    Google Scholar 

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

    Article  Google Scholar 

  31. Koehn FE, Kirsch DR, Feng X, Janso J, Young Y (2008) A cell wall-active lipopeptide from the fungus Pochonia bulbillosa. J Nat Prod 71:2045–2048

    Article  PubMed  CAS  Google Scholar 

  32. Koukol O (2007) Effect of Pinus strobus L. invasion on the mycoflora of pine litter needles in the Bohemian Switzerland National Park (Czech Republic). In: Härtel H et al (eds) Sandstone landscapes. Academia, Praha, p 493

    Google Scholar 

  33. Krashevska V, Bonkowski M, Maraun M, Ruess L, Kandeler E, Scheu S (2008) Microorganisms as driving factors for the community structure of testate amoebae along an altitudinal transect in tropical mountain rain forests. Soil Biol Biochem 40:2427–2433

    Article  CAS  Google Scholar 

  34. Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, Högberg P, Stenlid J, Finlay R (2007) Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol 173:611–620

    Article  PubMed  CAS  Google Scholar 

  35. Lousier JD (1974) Effects of experimental soil-moisture fluctuations on turnover rates of Testacea. Soil Biol Biochem 6:19–26

    Article  Google Scholar 

  36. Lousier JD (1974) Response of soil Testacea to soil-moisture fluctuations. Soil Biol Biochem 6:235–239

    Article  Google Scholar 

  37. Lousier JD (1982) Colonization of decomposing deciduous leaf litter by Testacea (Protozoa, Rhizopoda)—species succession, abundance, and biomass. Oecologia 52:381–388

    Article  Google Scholar 

  38. Lousier JD, Parkinson D (1984) Annual population dynamics and production ecology of Testacea (Protozoa, Rhizopoda) in an aspen woodland soil. Soil Biol Biochem 16:103–114

    Article  Google Scholar 

  39. Miller RM, Reinhardt DR, Jastrow JD (1995) External hyphal production of vesicular-arbuscular mycorrhizal fungi in pasture and tallgrass prairie communities. Oecologia 103:17–23

    Article  Google Scholar 

  40. Mitchell CP, Millar CS, Minter DW (1978) Studies on decomposition of Scots pine needles. Trans Br Mycol Soc 71:343–348

    Article  Google Scholar 

  41. Moosavi M-R, Zare R, Zamanizadeh H-R, Fatemy S (2010) Pathogenicity of Pochonia species on eggs of Meloidogyne javanica. J Invertebr Pathol 104:125–133

    Article  PubMed  Google Scholar 

  42. Napolitano JJ, Flanagan VD (1981) Occurrence of amebas in and around the mushroom Laccaria trullisata. J Protozool 28:494–497

    Google Scholar 

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

    Google Scholar 

  44. Ogden CG, Pitta P (1990) Biology and ultrastructure of the mycophagus, soil testate ameba, Phryganella acropodia (Rhizopoda, Protozoa). Biol Fert Soils 9:101–109

    Article  Google Scholar 

  45. 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 

  46. Ponge JF (1991) Succession of fungi and fauna during decomposition of needles in a small area of Scots pine litter. Plant Soil 138:99–113

    Article  Google Scholar 

  47. Ponge JF (1991) Food resources and diets of soil animals in a small area of Scots pine litter. Geoderma 49:33–62

    Article  Google Scholar 

  48. Schönborn W (1986) Population dynamics and production biology of testate amebas (Rhizopoda, Testacea) in raw humus of 2 coniferous forest soils. Arch Protistenkd 132:325–342

    Google Scholar 

  49. Schönborn W (1992) Comparative studies on the production biology of protozoan communities in freshwater and soil ecosystems. Arch Protistenkd 141:187–214

    Google Scholar 

  50. 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 

  51. Sutton BC (1975) Hyphomycetes on cupules of Castanea sativa. Trans Br Mycol Soc 64:405–426

    Article  Google Scholar 

  52. Timonen S, Christensen S, Ekelund F (2004) Distribution of protozoa in Scots pine mycorrhizospheres. Soil Biol Biochem 36:1087–1093

    Article  CAS  Google Scholar 

  53. Todorov M (2001) Testate amoebae (Protozoa: Rhizopoda) in soil and litter of beech forests (Fagus sylvatica L.) from Bulgaria. Act Zool Bulg 53:19–36

    Google Scholar 

  54. Tokumasu S, Aoki T, Oberwinkler F (1994) Fungal succession on pine needles in Germany. Mycoscience 35:29–37

    Article  Google Scholar 

  55. van Maanen A, Gourbière F (1997) Host and geographical distribution of Verticicladium trifidum, Thysanophora penicillioides, and similar fungi on decaying coniferous needles. Can J Bot 75:699–710

    Google Scholar 

  56. Vohník M, Burdíková Z, Albrechtová J, Vosátka M (2009) 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

    Article  PubMed  Google Scholar 

  57. White JF, Bacon CW, Hywel-Jones NL, Spatafora JW (2003) Clavicipitalean fungi: evolutionary biology, chemistry, biocontrol, and cultural impacts. CRC Press, Boca Raton, p 575

    Book  Google Scholar 

  58. Wilkinson DM (2008) Testate amoebae and nutrient cycling: peering into the black box of soil ecology. Trend Ecol Evol 23:596–599

    Article  Google Scholar 

  59. Wilkinson DM, Mitchell EAD (2010) Testate amoebae and nutrient cycling with particular reference to soils. Geomicrobiol J 27:520–533

    Article  Google Scholar 

  60. Yeates GW, Foissner W (1995) Testate amebas as predators of nematodes. Biol Fert Soils 20:1–7

    Article  Google Scholar 

  61. Zare R, Gams W, Evans HC (2001) A revision of Verticillium section Prostrata. V. The genus Pochonia, with notes on Rotiferophthora. Nova Hedwig 73:51–86

    Google Scholar 

  62. Zucconi L, Pasqualetti M (2007) Microfungal assemblage on Quercus ilex leaf litter in Tuscany, central Italy. Plant Biosyst 141:305–313

    Google Scholar 

Download references

Acknowledgement

This study was supported by the Academy of Sciences of the Czech Republic (research projects AV0Z60050516 and AV0Z50110509), Ministry of Education, Youth and Sports (research program LC06063) and Grant Agency of the Czech Republic (206/09/P295 and 204/09/H084). The authors thank David M. Wilkinson and Humphrey G. Smith for valuable comments on the results of the experiment, four anonymous reviewers for their valuable effort, and Jesse J. Sadowsky for a stylistic revision. MV thanks the foundation “Nadání Josefa, Marie a Zdenky Hlávkových” for funding his stay at Liverpool John Moores University, Liverpool, UK.

Author information

Authors and Affiliations

  1. Department of Mycorrhizal Symbioses, Institute of Botany ASCR, Průhonice, CZ-25243, Czech Republic

    Martin Vohník

  2. Department of Plant Experimental Biology, Faculty of Science, Charles University in Prague, Prague, CZ-12843, Czech Republic

    Martin Vohník

  3. Department of Paleontology, Faculty of Science, Charles University in Prague, Prague, CZ-12844, Czech Republic

    Zuzana Burdíková

  4. Department of Biomathematics, Institute of Physiology ASCR, Prague, CZ-14220, Czech Republic

    Zuzana Burdíková & Aleš Vyhnal

  5. Department of Botany, Faculty of Science, Charles University in Prague, Prague, CZ-112843, Czech Republic

    Ondřej Koukol

Authors
  1. Martin Vohník
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zuzana Burdíková
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aleš Vyhnal
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ondřej Koukol
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Martin Vohník.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vohník, M., Burdíková, Z., Vyhnal, A. et al. Interactions Between Testate Amoebae and Saprotrophic Microfungi in a Scots Pine Litter Microcosm. Microb Ecol 61, 660–668 (2011). https://doi.org/10.1007/s00248-010-9777-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-010-9777-4

Keywords

Search

Navigation