The soil food web revisited: Diverse and widespread mycophagous soil protists

Soil Biology and Biochemistry

Volumn 94, Issue , 2016, Pages 10-18

  Geisen, Stefan ^a,e   Koller, Robert ^a,c   Hünninghaus, Maike ^a   Dumack, Kenneth ^a   Urich, Tim ^b,d   Bonkowski, Michael ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b UNIVERSITY OF VIENNA   (Austria)

^c FORSCHUNGSZENTRUM JÜLICH   (Germany)

^d UNIVERSITY OF GREIFSWALD   (Germany)

^e NETHERLANDS INSTITUTE OF ECOLOGY NIOO KNAW   (Netherlands)

Author keywords

Fungi; Microcosm studies; Soil food web; Soil metatranscriptomes; Soil protists; Trophic interactions

Indexed keywords

DATA MINING; ECOSYSTEMS; FUNGI; PROTOZOA; RNA;

FUNGAL COMMUNITY; MICROCOSM EXPERIMENTS; MICROCOSM STUDIES; RELATIVE ABUNDANCE; SOIL FOOD WEB; STRONG CORRELATION; TERRESTRIAL ECOSYSTEMS; TROPHIC INTERACTIONS;

SOILS;

COMMUNITY STRUCTURE; ENERGY BUDGET; FOOD WEB; FUNGUS; MICROCOSM; MYCOPHAGY; RELATIVE ABUNDANCE; SOIL BIOTA; SOIL ECOSYSTEM; SOIL MICROORGANISM; SPECIES DIVERSITY; TROPHIC INTERACTION;

ACANTHAMOEBA SP.; AMOEBA (GENUS); ARTHROPODA; BACTERIA (MICROORGANISMS); CERCOMONAS; CILIOPHORA; FUNGI; FUSARIUM; GROSSGLOCKNERIIDAE; LEPTOMYXA; MASTIGOPHORA (FLAGELLATES); MAYORELLA; NEMATODA; PROTISTA; THECAMOEBA; VAMPYRELLIDAE;

EID: 84960376353     PISSN: 00380717     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.soilbio.2015.11.010     Document Type: Article

References (84)

1. Adl S.M., Simpson A.G.B., Lane C.E., Lukeš J., Bass D., Bowser S.S., Brown M.W., Burki F., Dunthorn M., Hampl V., Heiss A., Hoppenrath M., Lara E., le Gall L., Lynn D.H., McManus H., Mitchell E.A.D., Mozley-Stanridge S.E., Parfrey L.W., Pawlowski J., Rueckert S., Shadwick L., Schoch C.L., Smirnov A., Spiegel F.W. The revised classification of eukaryotes. Journal of Eukaryotic Microbiology 2012, 59:429-514.
2. Allen P.G., Dawidowicz E.A. Phagocytosis in Acanthamoeba: I. A mannose receptor is responsible for the binding and phagocytosis of yeast. Journal of Cellular Physiology 1990, 145:508-513.
3. Anderson I.J., Watkins R.F., Samuelson J., Spencer D.F., Majoros W.H., Gray M.W., Loftus B.J. Gene discovery in the Acanthamoeba castellanii genome. Protist 2005, 156:203-214.
4. Bamforth S.S. Interactions between protozoa and other organisms. Agriculture, Ecosystems & Environment 1988, 24:229-234.
5. Bamforth S.S. Water film fauna of microbiotic crusts of a warm desert. Journal of Arid Environments 2004, 56:413-423.
6. Bates S.T., Clemente J.C., Flores G.E., Walters W.A., Parfrey L.W., Knight R., Fierer N. Global biogeography of highly diverse protistan communities in soil. ISME Journal 2013, 7:652-659.
7. Berney C., Pawlowski J. A molecular time-scale for eukaryote evolution recalibrated with the continuous microfossil record. Proceedings of the Royal Society B 2006, 273:1867-1872.
8. Berney C., Romac S., Mahé F., Santini S., Siano R., Bass D. Vampires in the oceans: predatory cercozoan amoebae in marine habitats. ISME Journal 2013, 7:2387-2399.
9. Berthold A., Palzenberger M. Comparison between direct counts of active soil ciliates (Protozoa) and most probable number estimates obtained by Singh's dilution culture method. Biology and Fertility of Soils 1995, 19:348-356.
10. Böhme A., Risse-Buhl U., Küsel K. Protists with different feeding modes change biofilm morphology. FEMS Microbiology Ecology 2009, 69:158-169.
11. Bonkowski M. Protozoa and plant growth: the microbial loop in soil revisited. New Phytologist 2004, 162:617-631.
12. Bonkowski M., Brandt F. Do soil protozoa enhance plant growth by hormonal effects?. Soil Biology & Biochemistry 2002, 34:1709-1715.
13. Bowers B., Korn E.D. Cytochemical identification of phosphatase activity in the contractile vacuole of Acanthamoeba castellanii. Journal of Cell Biology 1973, 59:784-791.
14. Brüssow H. Bacteria between protists and phages: from antipredation strategies to the evolution of pathogenicity. Molecular Microbiology 2007, 65:583-589.
15. Bunting L.A., Neilson J.B., Bulmer G.S. Cryptococcus neoformans: gastronomic delight of a soil ameba. Sabouraudia 1979, 17:225-232.
16. Chakraborty S., Old K. Mycophagous soil amoeba: interactions with three plant pathogenic fungi. Soil Biology & Biochemistry 1982, 14:247-255.
17. Chakraborty S., Old K.M., Warcup J.H. Amoebae from a take-all suppressive soil which feed on Gaeumannomyces graminis tritici and other soil fungi. Soil Biology & Biochemistry 1983, 15:17-24.
18. Chou H.-H., Holmes M.H. DNA sequence quality trimming and vector removal. Bioinformatics 2001, 17:1093-1104.
19. Clarke M., Lohan A., Liu B., Lagkouvardos I., Roy S., Zafar N., Bertelli C., Schilde C., Kianianmomeni A., Burglin T., Frech C., Turcotte B., Kopec K., Synnott J., Choo C., Paponov I., Finkler A., Heng Tan C., Hutchins A., Weinmeier T., Rattei T., Chu J., Gimenez G., Irimia M., Rigden D., Fitzpatrick D., Lorenzo-Morales J., Bateman A., Chiu C.-H., Tang P. Genome of Acanthamoeba castellanii highlights extensive lateral gene transfer and early evolution of tyrosine kinase signaling. Genome Biology 2013, 14:R11.
20. Corsaro D., Venditti D. Phylogenetic evidence for a new genotype of Acanthamoeba (Amoebozoa, Acanthamoebida). Parasitology Research 2010, 107:233-238.
21. CoÛteaux M.M., Darbyshire J.F. Functional diversity amongst soil protozoa. Applied Soil Ecology 1998, 10:229-237.
22. Crotty F., Adl S., Blackshaw R., Murray P. Protozoan pulses unveil their pivotal position within the soil food web. Microbial Ecology 2012, 63:905-918.
23. de Ruiter P.C., Neutel A.M., Moore J.C. Energetics, patterns of interaction strengths, and stability in real ecosystems. Science 1995, 269:1257-1260.
24. Dunthorn M., Foissner W., Katz L.A. Molecular phylogenetic analysis of class Colpodea (phylum Ciliophora) using broad taxon sampling. Molecular Phylogenetics and Evolution 2008, 46:316-327.
25. Ekelund F. Enumeration and abundance of mycophagous protozoa in soil, with special emphasis on heterotrophic flagellates. Soil Biology & Biochemistry 1998, 30:1343-1347.
26. Flavin M., O'Kelly C.J., Nerad T.A., Wilkinson G. Cholamonas cyrtodiopsidis gen. n., sp. n. (Cercomonadida), an endocommensal, mycophagous heterotrophic flagellate with a doubled kinetid. Acta Protozoologica 2000, 39:51-60.
27. Foissner W. Colpodide Ciliaten (Protozoa: Ciliophora) aus alpinen Böden. Zoologische Jahrbücher Systematik 1980, 107:391-432.
28. Foissner W. An updated compilation of world soil ciliates (Protozoa, Ciliophora), with ecological notes, new records, and descriptions of new species. European Journal of Protistology 1998, 34:195-235.
29. Foissner W. Description of two new, mycophagous soil ciliates (Ciliophora, Colpodea): Fungiphrya strobli n. g., n. sp. and Grossglockneria ovata n. sp. Journal of Eukaryotic Microbiology 1999, 46:34-42.
30. Foissner W. Soil protozoa as bioindicators: pros and cons, methods, diversity, representative examples. Agriculture, Ecosystems & Environment 1999, 74:95-112.
31. Foissner W., Didier P. Nahrungsaufnahme, Lebenszyklus und Morphogenese von Pseudoplatyophrya nana (KAHL, 1926) (Ciliophora, Colpodida). Protistologica 1983, 19:103-109.
32. Fouque E., Trouilhe M.C., Thomas V., Hartemann P., Rodier M.H., Héchard Y. Cellular, biochemical, and molecular changes during encystment of free-living amoebae. Eukaryotic Cell 2012, 11:382-387.
33. Galagan J.E., Calvo S.E., Borkovich K.A., Selker E.U., Read N.D., Jaffe D., FitzHugh W., Ma L.-J., Smirnov S., Purcell S. The genome sequence of the filamentous fungus Neurospora crassa. Nature 2003, 422:859-868.
34. Gast R.J. Development of an Acanthamoeba-specific reverse dot-blot and the discovery of a new ribotype. Journal of Eukaryotic Microbiology 2001, 48:609-615.
35. Gast R.J., Ledee D.R., Fuerst P.A., Byers T.J. Subgenus systematics of Acanthamoeba: four nuclear 18S rDNA sequence types. Journal of Eukaryotic Microbiology 1996, 43:498-504.
36. Geisen S., Fiore-Donno A.M., Walochnik J., Bonkowski M. Acanthamoeba everywhere: high diversity of Acanthamoeba in soils. Parasitology Research 2014, 113:3151-3158.
37. Geisen S., Rosengarten J., Koller R., Mulder C., Urich T., Bonkowski M. Pack hunting by a common soil amoeba on nematodes. Environmental Microbiology 2015.
38. Geisen S., Tveit A.T., Clark I.M., Richter A., Svenning M.M., Bonkowski M., Urich T. Metatranscriptomic census of active protists in soils. ISME Journal 2015, 9:2178-2190.
39. Glücksman E., Bell T., Griffiths R.I., Bass D. Closely related protist strains have different grazing impacts on natural bacterial communities. Environmental Microbiology 2010, 12:3105-3113.
40. Heal O.W. Soil fungi as food for amoebae. Soil Organisms 1963, 289-297. North-Holland Publishing Company, Amsterdam. J. Doeksen, J. Van der Drift (Eds.).
41. Hekman W.E., van den Boogert P.J.H.F., Zwart K.B. The physiology and ecology of a novel, obligate mycophagous flagellate. FEMS Microbiology Ecology 1992, 86:255-265.
42. Herdler S., Kreuzer K., Scheu S., Bonkowski M. Interactions between arbuscular mycorrhizal fungi (Glomus intraradices, Glomeromycota) and amoebae (Acanthamoeba castellanii, Protozoa) in the rhizosphere of rice (Oryza sativa). Soil Biology & Biochemistry 2008, 40:660-668.
43. Hess S., Sausen N., Melkonian M. Shedding light on vampires: the phylogeny of vampyrellid amoebae revisited. PLoS ONE 2012, 7:e31165.
44. Holtkamp R., van der Wal A., Kardol P., van der Putten W.H., de Ruiter P.C., Dekker S.C. Modelling C and N mineralisation in soil food webs during secondary succession on ex-arable land. Soil Biology & Biochemistry 2011, 43:251-260.
45. Hunt H.W., Coleman D.C., Ingham E.R., Ingham R.E., Elliott E.T., Moore J.C., Rose S.L., Reid C.P.P., Morley C.R. The detrital food web in a shortgrass prairie. Biology and Fertility of Soils 1987, 3:57-68.
46. Jousset A. Ecological and evolutive implications of bacterial defences against predators. Environmental Microbiology 2012, 14:1830-1843.
47. Jousset A., Lara E., Wall L., Valverde C. Secondary metabolites help biocontrol strain Pseudomonas fluorescens CHA0 to escape protozoan grazing. Applied and Environmental Microbiology 2006, 72:7083.
48. Jousset A., Rochat L., Pechy-Tarr M., Keel C., Scheu S., Bonkowski M. Predators promote defence of rhizosphere bacterial populations by selective feeding on non-toxic cheaters. ISME Journal 2009, 3:666-674.
49. Kamono A., Meyer M., Cavalier-Smith T., Fukui M., Fiore-Donno A.M. Exploring slime mould diversity in high-altitude forests and grasslands by environmental RNA analysis. FEMS Microbiology Ecology 2013, 84:98-109.
50. Khan N.A. Acanthamoeba: Biology and Pathogenesis 2009, Caister Academic Press, Norfolk, United Kingdom.
51. Koller R., Robin C., Bonkowski M., Ruess L., Scheu S. Litter quality as driving factor for plant nutrition via grazing of protozoa on soil microorganisms. FEMS Microbiology Ecology 2013, 85:241-250.
52. Koller R., Rodriguez A., Robin C., Scheu S., Bonkowski M. Protozoa enhance foraging efficiency of arbuscular mycorrhizal fungi for mineral nitrogen from organic matter in soil to the benefit of host plants. New Phytologist 2013, 199:203-211.
53. Kreuzer K., Adamczyk J., Iijima M., Wagner M., Scheu S., Bonkowski M. Grazing of a common species of soil protozoa (Acanthamoeba castellanii) affects rhizosphere bacterial community composition and root architecture of rice (Oryza sativa L.). Soil Biology & Biochemistry 2006, 38:1665-1672.
54. Krishna Murti C.R., Shukla O.P. Differentiation of pathogenic amoebae: encystation and excystation of Acanthamoeba culbertsoni - a model. Journal of Biosciences 1984, 6:475-489.
55. Lanzén A., Jørgensen S.L., Bengtsson M.M., Jonassen I., Øvreås L., Urich T. Exploring the composition and diversity of microbial communities at the Jan Mayen hydrothermal vent field using RNA and DNA. FEMS Microbiology Ecology 2011, 77:577-589.
56. Lanzén A., Jørgensen S.L., Huson D.H., Gorfer M., Grindhaug S.H., Jonassen I., Øvreås L., Urich T. CREST - classification resources for environmental sequence tags. PLoS ONE 2012, 7:e49334.
57. Laybourn-Parry J. A Functional Biology of Free-living Protozoa 1984, Univ of California Press.
58. Lynn D.H., Wright A.D., Schlegel M., Foissner W. Phylogenetic relationships of orders within the class Colpodea (phylum Ciliophora) inferred from small subunit rRNA gene sequences. Journal of Molecular Evolution 1999, 48:605-614.
59. Matz C., Kjelleberg S. Off the hook - how bacteria survive protozoan grazing. Trends in Microbiology 2005, 13:302-307.
60. Mitchell E.A.D., Charman D.J., Warner B.G. Testate amoebae analysis in ecological and paleoecological studies of wetlands: past, present and future. Biodiversity & Conservation 2008, 17:2115-2137.
61. Moore J.C., Hunt H.W. Resource compartmentation and the stability of real ecosystems. Nature 1988, 333:261-263.
62. Neidig N., Jousset A., Nunes F., Bonkowski M., Paul R.J., Scheu S. Interference between bacterial feeding nematodes and amoebae relies on innate and inducible mutual toxicity. Functional Ecology 2010, 24:1133-1138.
63. Old K.M., Darbyshire J.F. Soil fungi as food for giant amoebae. Soil Biology & Biochemistry 1978, 10:93-100.
64. Old K.M., Oros J.M. Mycophagous amoebae in Australian forest soils. Soil Biology & Biochemistry 1980, 12:169-175.
65. Page F.C. A New Key to Freshwater and Soil Gymnamoebae with Instructions for Culture 1988, Freshwater Biological Association, Ambleside, Cumbria.
66. Petz W., Foissner W., Adam H. Culture, food selection and growth rate in the mycophagous ciliate Grossglockneria acuta Foissner, 1980: first evidence of autochthonous soil ciliates. Soil Biology & Biochemistry 1985, 17:871-875.
67. Petz W., Foissner W., Wirnsberger E., Krautgartner W.D., Adam H. Mycophagy, a new feeding strategy in autochthonous soil ciliates. Naturwissenschaften 1986, 73:560-562.
68. Qvarnstrom Y., Nerad T.A., Visvesvara G.S. Characterization of a new pathogenic Acanthamoeba species, A. byersi n. sp., isolated from a human with fatal amoebic encephalitis. Journal of Eukaryotic Microbiology 2013, 60:626-633.
69. Rodríguez-Zaragoza S. Ecology of free-living amoebae. Critical Reviews in Microbiology 1994, 20:225-241.
70. Rønn R., McCaig A.E., Griffiths B.S., Prosser J.I. Impact of protozoan grazing on bacterial community structure in soil microcosms. Applied and Environmental Microbiology 2002, 68:6094-6105.
71. Rosenberg K., Bertaux J., Krome K., Hartmann A., Scheu S., Bonkowski M. Soil amoebae rapidly change bacterial community composition in the rhizosphere of Arabidopsis thaliana. ISME Journal 2009, 3:675-684.
72. Saleem M., Fetzer I., Dormann C.F., Harms H., Chatzinotas A. Predator richness increases the effect of prey diversity on prey yield. Nature Communications 2012, 3:1305.
73. Sawyer T.K., Griffin J.L. A proposed new family, Acanthamoebidae n. fam. (Order Amoebida), for certain cyst-forming filose amoebae. Transactions of the American Microscopical Society 1975, 94:93-98.
74. Scherm B., Balmas V., Spanu F., Pani G., Delogu G., Pasquali M., Migheli Q. Fusarium culmorum: causal agent of foot and root rot and head blight on wheat. Molecular Plant Pathology 2013, 14:323-341.
75. Smirnov A.V., Chao E., Nassonova E.S., Cavalier-Smith T. A revised classification of naked lobose amoebae (Amoebozoa: Lobosa). Protist 2011, 162:545-570.
76. Stephenson S.L., Feest A. Ecology of soil eumycetozoans. Acta Protozoologica 2012, 51:201-208.
77. Stotefeld L., Scheu S., Rohlfs M. Fungal chemical defence alters density-dependent foraging behaviour and success in a fungivorous soil arthropod. Ecological Entomology 2012, 37:323-329.
78. Stothard D.R., Schroeder-Diedrich J.M., Awwad M.H., Gast R.J., Ledee D.R., Rodriguez-Zaragoza S., Dean C.L., Fuerst P.A., Byers T.J. The evolutionary history of the genus Acanthamoeba and the identification of eight new 18S rRNA gene sequence types. Journal of Eukaryotic Microbiology 1998, 45:45-54.
79. Tapilskaja N. Amoeba albida Nägler und ihre Beziehungen zu dem Pilz Verticillium dahliae Kleb, dem Erreger der Welkekrankheit von Baumwollpflanzen. Pedobiologia 1967, 7:156-165.
80. Tracey M.V. Cellulase and chitinase in soil amoebae. Nature 1955, 175:815.
81. Trap J., Bonkowski M., Plassard C., Villenave C., Blanchart E. Ecological importance of soil bacterivores for ecosystem functions. Plant and Soil 2015, 1-24.
82. Weekers P.H.H., Bodelier P.L.E., Wijen J.P.H., Vogels G.D. Effects of grazing by the free-living soil amoebae Acanthamoeba castellanii, Acanthamoeba polyphaga, and Hartmannella vermiformis on various bacteria. Applied and Environmental Microbiology 1993, 59:2317-2319.
83. Wilkinson D.M. Testate amoebae and nutrient cycling: peering into the black box of soil ecology. Trends in Ecology & Evolution 2008, 23:596-599.
84. Wilkinson D.M., Mitchell E.A.D. Testate amoebae and nutrient cycling with particular reference to soils. Geomicrobiology Journal 2010, 27:520-533.