Ecological importance of soil bacterivores for ecosystem functions

Plant and Soil

Volumn 398, Issue 1-2, 2016, Pages 1-24

  Trap, Jean ^a   Bonkowski, Michael ^b   Plassard, Claude ^c   Villenave, Cécile ^d   Blanchart, Eric ^a  

^a INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

^b UNIVERSITY OF COLOGNE   (Germany)

^c CEMAGREF   (France)

^d ELISOL Environnement   (France)

Author keywords

Bacterivores; Ecological stoichiometry; Meta analysis; Microbial loop; Nematodes; Plant growth; Plant nutrition; Protists

Indexed keywords

BACTERIVORY; BIODIVERSITY; ECOLOGICAL IMPACT; ECOSYSTEM FUNCTION; GLOBAL CHANGE; GROWTH RATE; IMMOBILIZATION; ISOTOPIC RATIO; META-ANALYSIS; MICROBIAL ECOLOGY; NEMATODE; NUTRIENT AVAILABILITY; PHYTOMASS; PRIMARY PRODUCTION; PROTIST; SOIL BIOTA; SOIL FERTILITY; STOICHIOMETRY;

BACTERIA (MICROORGANISMS); NEMATODA; PROTISTA;

EID: 84955179040     PISSN: 0032079X     EISSN: 15735036     Source Type: Journal    
DOI: 10.1007/s11104-015-2671-6     Document Type: Review

References (162)

1. Adl SM, Simpson AGB, Farmer MA, Andersen RA, Anderson OR, Barta JR, Bowser SS, Brugerolle G, Fensome RA, Fredericq S, James TY, Karpov S, Kugrens P, Krug J, Lane CE, Lewis LA, Lodge J, Lynn DH, Mann DG, McCourt RM, Mendoza L, Moestrup Ø, Mozley-Standridge SE, Nerad TA, Shearer CA, Smirnov AV, Spiegel FW, Taylor MFJR (2005) The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eucaryot Microbiol 52:399–451
2. Adl SM, Simpson AG, Lane CE, Lukeš J, Bass D, Bowser SS, Brown M, Burki F, Dunthorn M, Hampl V, Heiss A, Hoppenrath M, Lara E, leGall L, Lynn DH, McManus H, Mitchell EAD, Mozley-Stanridge SE, Wegener Parfrey L, Pawlowski J, Rueckert S, Shadwick L, Schoch C, Smirnov A, Spiegel FW (2012) The revised classification of eukaryotes. J Eucaryot Microbiol 59:429–514
3. Ågren GI (2004) The C:N:P stoichiomestry of autotrophs - theory and observations. Ecol Lett 7:185–191
4. Ågren GI (2008) Stoichiometry and nutrition of plant growth in natural communities. Annu Rev Ecol Syst 39:153–170
5. Alphei J, Bonkowski M, Scheu S (1996) Protozoa, Nematoda and Lumbricidae in the rhizosphere of Hordelymus europeaus (Poaceae): faunal interactions, response of microorganisms and effects on plant growth. Oecologia 106:111–126
6. Anderson RV, Coleman DC (1981) Population development and interactions between 2 species of bacteriophagic nematodes. Nematologica 27:6–19
7. Anderson RV, Elliott ET, McClellan JF, Coleman DC, Cole CV, Hunt HW (1978) Trophic interactions in soils as they affect energy and nutrient dynamics. 3. Biotic interactions of bacteria, amebas, and nematodes. Microb Ecol 4:361–371
8. Anderson R, Gould W, Woods L, Cambardella C, Ingham R, Coleman D (1983) Organic and inorganic nitrogenous losses by microbivorous nematodes in soil. Oikos 40:75–80
9. Baath E, Lohm U, Lundgren B, Rosswall T, Soderstrom B, Sohlenius B (1981) Impact of microbial-feeding animals on total soil activity and nitrogen dynamics: a soil microcosm experiment. Oikos 37:257–264
10. Bardgett RD, Cook R, Yeates GW, Denton CS (1999) The influence of nematodes on below-ground processes in grassland ecosystems. Plant Soil 212:23–33
11. Barrios E (2007) Soil biota, ecosystem services and land productivity. Ecol Econ 64:269–285
12. Benizri E, Dedourge O, Dibattista-Leboeuf C, Piutti S, Nguyen C, Guckert A (2002) Effect of maize rhizodeposits on soil microbial community structure. Appl Soil Ecol 21:261–265
13. Bjornlund L, Rønn R (2008) ‘David and Goliath’ of the soil food web - Flagellates that kill nematodes. Soil Biol Biochem 40:2032–2039
14. Bjornlund L, Liu MQ, Rønn R, Christensen S, Ekelund F (2012) Nematodes and protozoa affect plants differently, depending on soil nutrient status. Eur J Soil Biol 50:28–31
15. Blanc C, Sy M, Djigal D, Brauman A, Normand P, Villenave C (2006) Nutrition on bacteria by bacterial-feeding nematodes and consequences on the structure of soil bacterial community. Eur J Soil Biol 42:S70–S78
16. Bonkowski M (2004) Protozoa and plant growth: the microbial loop in soil revisited. New Phytol 162:617–631
17. Bonkowski M, Clarholm M (2012) Stimulation of plant growth through interactions of bacteria and protozoa: testing the auxiliary microbial loop hypothesis. Acta Protozool 51:237–247
18. Bonkowski M, Schaefer M (1997) Interactions between earthworms and soil protozoa: a trophic component in the soil food web. Soil Biol Biochem 29:499–502
19. Bonkowski M, Griffiths B, Scrimgeour C (2000) Substrate heterogeneity and microfauna in soil organic ‘hotspots’ as determinants of nitrogen capture and growth of ryegrass. Appl Soil 14:37–53
20. Bonkowski M, Geoghegan IE, Birch ANE, Griffiths BS (2001a) Effects of soil decomposer invertebrates (protozoa and earthworms) on an above-ground phytophagous insect (cereal aphid) mediated through changes in the host plant. Oikos 95:441–450
21. Bonkowski M, Jentschke G, Scheu S (2001b) 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 18:193–204
22. Bonkowski M, Villenave C, Griffiths B (2009) Rhizosphere fauna: the functional and structural diversity of intimate interactions of soil fauna with plant roots. Plant Soil 321:213–233
23. Bonkowski M, Koller R, Jousset AJF (2011) How protozoa structure microbial communities in the rhizosphere of plants. J Phycol 47:S7
24. Borkott H (1989) Elementgehalte (C, N, P, K) wirbelloser Bodentiere. Z Pflanzenernähr Bodenkd 152:77–80
25. Bossio DA, Girvan MS, Verchot L, Bullimore J, Borelli T, Albrecht A, Scow KM, Ball AS, Pretty JN, Osborn AM (2005) Soil microbial community response to land use change in an agricultural landscape of western Kenya. Microb Ecol 49:50–62
26. Brown LK, George TS, Barrett GE, Hubbard SF, White PJ (2013) Interactions between root hair length and arbuscular mycorrhizal colonisation in phosphorus deficient barley (Hordeum vulgare). Plant Soil 372:195–205
27. Brussaard L (1997) Biodiversity and ecosystem functioning in soil. Ambio 26:563–570
28. Brussaard L, De Ruiter PC, Brown GG (2007) Soil biodiversity for agricultural sustainability. Agr Ecosyst Environ 121:233–244
29. Cappellazzo G, Lanfranco L, Fitz M, Wipf D, Bonfante P (2008) Characterization of an amino acid permease from the endomycorrhizal fungus Glomus mosseae. Plant Physiol 147:429–437
30. Chen X, Liu M, Hu F, Mao X, Li H (2007) Contributions of soil micro-fauna (protozoa and nematodes) to rhizosphere ecological functions. Acta Ecol Sin 27:3132–3143
31. Cheng YH, Jiang Y, Griffiths BS, Li DM, Hu F, Li HX (2011) Stimulatory effects of bacterial-feeding nematodes on plant growth vary with nematode species. Nematology 13:369–372
32. Clarholm M (1985a) Interactions of bacteria, protozoa and plants leading to mineralization of soil-nitrogen. Soil Biol Biochem 17:181–187
33. Clarholm M (1985b) Possible roles for roots, bacteria, protozoa, and fungi in supplying nitrogen to plants. In: Fitter AH (ed) Ecological interactions in soil. Blackwell Scient. Publ., pp 355–365
34. Cleveland CC, Liptzin D (2007) C: N: P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85:235–252
35. Cole CV, Elliott ET, Hunt HW, Coleman DC (1978) Trophic interactions in soils as they affect energy and nutrient dynamics. Phosphorus transformations. Microb Ecol 4:381–387
36. Coleman DC, Wall DH (2015) Soil fauna: occurrence, biodiversity, and roles in ecosystem function. In: Paul EA (ed) Soil Microbiology, Ecology and Biochemistry, 4th edn. Academic, Boston, pp 111–149
37. Coleman DC, Cole CV, Anderson RV, Blaha M, Campion MK, Clarholm M, Elliott ET, Hunt HW, Shaefer B, Sinclair J (1977) An analysis of rhizosphere-saprophage interactions in terrestrial ecosystems. Ecol Bull 25:299–309
38. Coleman DC, Anderson RV, Cole CV, Elliott ET, Woods L, Campion MK (1978) Trophic interactions in soils as they affect energy and nutrient dynamics. Flows of metabolic and biomass carbon. Microb Ecol 4:373–380
39. Courty PE, Pouysegur R, Buée M, Garbaye J (2006) Laccase and phosphatase activities of the dominant ectomycorrhizal types in a lowland oak forest. Soil Biol Biochem 38:1219–1222
40. Couteaux MM, Darbyshire JF (1998) Functional diversity amongst soil protozoa. Appl Soil 10:229–237
41. Cowling AJ (1994) Protozoa distribution and adaptation. In: Darbyshire JF (ed) Soil protozoa. CAB International, London, pp 5–42
42. Crotty FV, Adl SM, Blackshaw RP, Murray PJ (2013) Measuring soil protist respiration and ingestion rates using stable isotopes. Soil Biol Biochem 57:919–921
43. Darbyshire JF (1994) Soil protozoa. CAB International, London
44. Darbyshire JF, Davidson MS, Chapman SJ, Ritchie S (1994) Excretion of nitrogen and phosphorus by the soil Ciliate Colpoda steinii when fed the soil bacterium Arthrobacter sp. Soil Biol Biochem 26:1193–1199
45. De Ley P (1992) The nematode community of a marginal soil at Camberene, Senegal, with special attention to functional morphology and niche partitioning in the family Cephalobidae. Mededelingen van de Koninklijke. Academie voor Wetenschappen, Letteren en Schone Kunsten van België, Klasse der Wetenschappen 53:109–153
46. De Telegdy‐Kovats L (1932) The growth and respiration of bacteria in sand cultures in the presence and absence of protozoa. Ann Appl Biol 19:65–86
47. de Vries FT, Thebault E, Liiri M, Birkhofer K, Tsiafouli MA, Bjornlund L, Bracht Jørgensen H, Vincent Brady M, Christensen S, de Ruiter PC, d’Hertefeldt T, Frouz J, Hedlund K, Hemerik L, Gera Hol WH, Hotes S, Mortimer SR, Setala H, Sgardelis SP, Uteseny K, van der Putten WH, Wolters V, Bardgett RD (2013) Soil food web properties explain ecosystem services across European land use systems. Proc Natl Acad Sci U S A 110:14296–14301
48. Decaëns T (2010) Macroecological patterns in soil communities. Global Ecol Biogeogr 19:287–302
49. Djigal D, Brauman A, Diop TA, Chotte JL, Villenave C (2004) Influence of bacterial-feeding nematodes (Cephalobidae) on soil microbial communities during maize growth. Soil Biol Biochem 36:323–331
50. Djigal D, Baudoin E, Philippot L, Brauman A, Villenave C (2010) Shifts in size, genetic structure and activity of the soil denitrifier community by nematode grazing. Eur J Soil Biol 46:112–118
51. Drevon J-J, Hartwig UA (1997) Phosphorus deficiency increases the argon-induced decline of nodule nitrogenase activity in soybean and alfalfa. Planta 201:463–469
52. Dupouey J-L, Dambrine E, Laffite J-D, Moares C (2002) Irreversible impact of past land use on forest soils and biodiversity. Ecology 83:2978–2984
53. Ekelund F (1996) Growth kinetics of five common heterotrophic soil flagellates. Eur J Soil Biol 32:15–24
54. Ekelund F, Rønn R (1994) Notes on protozoa in agricultural soil with emphasis on heterotrophic flagellates and naked amebas and their ecology. FEMS Microbiol Rev 15:321–353
55. Ekelund F, Saj S, Vestergard M, Bertaux J, Mikola J (2009) The “soil microbial loop” is not always needed to explain protozoan stimulation of plants. Soil Biol Biochem 41:2336–2342
56. Elliott E, Cole C, Coleman D, Anderson R, Hunt H, McClellan J (1979) Amoebal growth in soil microcosms: a model system of C, N, and P. Trophic dynamics. Int J Environ Stud 13:169–174
57. Elliott ET, Anderson RV, Coleman DC, Cole CV (1980) Habitable pore-space and microbial trophic interactions. Oikos 35:327–335
58. Elser JJ, Urabe J (1999) The stoichiometry of consumer-driven nutrient recycling: theory, observations, and consequences. Ecology 80:735–751
59. Elser JJ, Sterner RW, Gorokhova E, Fagan WF, Markow TA, Cotner JB, Harrison JF, Hobbie SE, Odell GM, Weider LW (2000) Biological stoichiometry from genes to ecosystems. Ecol Lett 3:540–550
60. Elser JJ, Acharya K, Kyle M, Cotner J, Makino W, Markow T, Watts T, Hobbie S, Fagan W, Schade J, Hood J, Sterner RW (2003) Growth rate–stoichiometry couplings in diverse biota. Ecol Lett 6:936–943
61. Fanin N, Fromin N, Buatois B, Hattenschwiler S (2013) An experimental test of the hypothesis of non-homeostatic consumer stoichiometry in a plant litter-microbe system. Ecol Lett 16:764–772
62. Fenner M, Lee W (1989) Growth of seedlings of pasture grasses and legumes deprived of single mineral nutrients. J Appl Ecol 26:223–232
63. Ferris H, Venette RC, Lau SS (1997) Population energetics of bacterial-feeding nematodes: carbon and nitrogen budgets. Soil Biol Biochem 29:1183–1194
64. Ferris H, Venette RC, van der Meulen HR, Lau SS (1998) Nitrogen mineralization by bacterial-feeding nematodes: verification and measurement. Plant Soil 203:159–171
65. Finlay RD (2008) Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium. J Exp Bot 59:1115–1126
66. Foissner W (1999) Soil protozoa as bioindicators: pros and cons, methods, diversity, representative examples. Agric Ecosyst Environ 74:95–112
67. Foley JA, DeFries R, Asner GP, Barford C, Bonan G, Carpenter SR, Chapin FS, Coe MT, Daily GC, Gibbs HK, Helkowski JH, Holloway T, Howard EA, Kucharik CJ, Monfreda C, Patz JA, Prentice IC, Ramankutty N, Snyder PK (2005) Global consequences of land use. Science 309:570–574
68. Fürst von Lieven A (2003) Functional morphology and evolutionary origin of the three-part pharynx in nematodes. Zoology 106:183–201
69. Gallet-Budynek A, Brzostek E, Rodgers VL, Talbot JM, Hyzy S, Finzi AC (2009) Intact amino acid uptake by northern hardwood and conifer trees. Oecologia 160:129–138
70. Gardi C, Jeffery S, Saltelli A (2013) An estimate of potential threats levels to soil biodiversity in EU. Glob Change Biol 19:1538–1548
71. Geisen S, Fiore-Donno AM, Walochnik J, Bonkowski M (2014) Acanthamoeba everywhere: high diversity of Acanthamoeba in soils. Parasitol Res 113:3151–3158
72. Geisen S, Tveit AT, Clark IM, Richter A, Svenning MM, Bonkowski M, Urich T (2015) Metatranscriptomic census of active protists in soils. ISME J. doi:10.1038/ismej.2015.30
73. Glücksman E, Bell T, Griffiths RI, Bass D (2010) Closely related protist strains have different grazing impacts on natural bacterial communities. Environ Microbiol 12:3105–3113
74. Gould WD, Coleman DC, Rubink AJ (1979) Effect of bacteria and amoebae on rhizosphere phosphatase activity. Appl Environ Microb 37:943–946
75. Griffiths BS (1994) Soil nutrient flow. In: Darbyshire JF (ed) Soil protozoa. CAB International, Oxford, pp 65–92
76. Griffiths BS, Ritz K (1988) A technique to extract, enumerate and measure protozoa from mineral soils. Soil Biol Biochem 20:163–173
77. Griffiths BS, Bonkowski M, Dobson G, Caul S (1999) Changes in soil microbial community structure in the presence of microbial-feeding nematodes and protozoa. Pedobiologia 43:297–304
78. Griffiths BS, Spilles A, Bonkowski M (2012) C: N: P stoichiometry and nutrient limitation of the soil microbial biomass in a grazed grassland site under experimental P limitation or excess. Ecol Process 1:1–11
79. Gusewell S (2004) N: P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266
80. Hanley M, Fenner M (1997) Seedling growth of four fire‐following Mediterranean plant species deprived of single mineral nutrients. Funct Ecol 11:398–405
81. Hedges LV, Gurevitch J, Curtis PS (1999) The meta-analysis of response ratios in experimental ecology. Ecology 80:1150–1156
82. Herdler S, Kreuzer K, Scheu S, Bonkowski M (2008) Interactions between arbuscular mycorrhizal fungi (Glomus intraradices, Glomeromycota) and amoebae (Acanthamoeba castellanii, Protozoa) in the rhizosphere of rice (Oryza sativa). Soil Biol Biochem 40:660–668
83. Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil 237:173–195
84. Hinsinger P, Brauman A, Devau N, Gerard F, Jourdan C, Laclau JP, Le Cadre E, Jaillard B, Plassard C (2011) Acquisition of phosphorus and other poorly mobile nutrients by roots. Where do plant nutrition models fail? Plant Soil 348:29–61
85. Hodge A, Robinson D, Fitter A (2000) Are microorganisms more effective than plants at competing for nitrogen? Trends Plant Sci 5:304–308
86. Horiuchi J-i, Prithiviraj B, Bais HP, Kimball BA, Vivanco JM (2005) Soil nematodes mediate positive interactions between legume plants and rhizobium bacteria. Planta 222:848–857
87. Ingham RE, Trofymow J, Ingham ER, Coleman DC (1985) Interactions of bacteria, fungi, and their nematode grazers: effects on nutrient cycling and plant growth. Ecol Monogr 55:119–140
88. Irshad U, Villenave C, Brauman A, Plassard C (2011) Grazing by nematodes on rhizosphere bacteria enhances nitrate and phosphorus availability to Pinus pinaster seedlings. Soil Biol Biochem 43:2121–2126
89. Irshad U, Brauman A, Villenave C, Plassard C (2012) Phosphorus acquisition from phytate depends on efficient bacterial grazing, irrespective of the mycorrhizal status of Pinus pinaster. Plant Soil 358:148–161
90. Jentschke G, Bonkowski M, Godbold DL, Scheu S (1995) Soil protozoa and forest tree growth - Non-nutritional effects and interaction with mycorrhizae. Biol Fert Soils 20:263–269
91. Jones DL, Nguyen C, Finlay RD (2009) Carbon flow in the rhizosphere: carbon trading at the soil-root interface. Plant Soil 321:5–33
92. Jousset A (2011) Ecological and evolutive implications of bacterial defences against predators. Environ Microbiol 14:1830–1843
93. Jousset A, Lara E, Wall LG, Valverde C (2006) Secondary metabolites help biocontrol strain Pseudomonas fluorescens CHA0 to escape protozoan grazing. Appl Environ Microb 72:7083–7090
94. Jousset A, Scheu S, Bonkowski M (2008) Secondary metabolite production facilitates establishment of rhizobacteria by reducing both protozoan predation and the competitive effects of indigenous bacteria. Funct Ecol 22:714–719
95. Jousset A, Rochat L, Péchy-Tarr M, Keel C, Scheu S, Bonkowski M (2009) Predators promote defence of rhizosphere bacterial populations by selective feeding on non-toxic cheaters. ISME J 3:666–674
96. Jousset A, Rochat L, Scheu S, Bonkowski M, Keel C (2010) Predator–prey chemical warfare determines the expression of biocontrol genes by rhizosphere-associated Pseudomonas fluorescens. Appl Environ Microb 76:5263–5268
97. Kibblewhite MG (2012) Definition of priority areas for soil protection at a continental scale. Soil Use Manage 28:128–133
98. Kibblewhite MG, Ritz K, Swift MJ (2008) Soil health in agricultural systems. Philos T Roy Soc B 363:685–701
99. Koller R, Robin C, Bonkowski M, Ruess L, Scheu S (2013a) Litter quality as driving factor for plant nutrition via grazing of protozoa on soil microorganisms. FEMS Microbiol Ecol 85:241–250
100. Koller R, Rodriguez A, Robin C, Scheu S, Bonkowski M (2013b) Protozoa enhance foraging efficiency of arbuscular mycorrhizal fungi for mineral nitrogen from organic matter in soil to the benefit of host plants. New Phytol 199:203–211
101. Koller R, Scheu S, Bonkowski M, Robin C (2013c) Protozoa stimulate N uptake and growth of arbuscular mycorrhizal plants. Soil Biol Biochem 65:204–210
102. Kreuzer K, Adamczyk J, Iijima M, Wagner M, Scheu S, Bonkowski M (2006) Grazing of a common species of soil protozoa (Acanthamoeba castellanii) affects rhizosphere bacterial community composition and root architecture of rice (Oryza sativa L.). Soil Biol Biochem 38:1665–1672
103. Krome K, Rosenberg K, Bonkowski M, Scheu S (2009a) Grazing of protozoa on rhizosphere bacteria alters growth and reproduction of Arabidopsis thaliana. Soil Biol Biochem 41:1866–1873
104. Krome K et al (2009b) Soil bacteria and protozoa affect root branching via effects on the auxin and cytokinin balance in plants. Plant Soil 328:191–201
105. Kuikman PJ, Van Veen JA (1989) The impact of protozoa on the availability of bacterial nitrogen to plants. Biol Fert Sci 8:13–18
106. Kuikman PJ, Jansen AG, Van Veen JA, Zehnder AJB (1990) Protozoan predation and the turnover of soil organic-carbon and nitrogen in the presence of plants. Biol Fert Sci 10:22–28
107. Kuikman PJ, Jansen AG, Van Veen JA (1991) N-15-nitrogen mineralization from bacteria by protozoan grazing at different soil-moisture regimes. Soil Biol Biochem 23:193–200
108. Kuzyakov Y, Xu X (2013) Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytol 198:656–669
109. Lambshead P (1993) Recent developments in marine benthic biodiversity research. Oceanis 19:5
110. Lambshead P, Chen Z, Chen W, Chen S, Dickson S (2004) Marine nematode biodiversity. In: Chen ZX et al. (ed) Nematology: Advances and Perspectives. CAB International, pp 436–467
111. Lavelle P, Spain AV (2001) Soil Ecology. Kluwer, Dordrecht
112. Leake JR, Johnson D, Donnelly DP, Muckle GE, Boddy L, Read DJ (2004) Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Can J Bot-Rev Can Bot 82:1016–1045
113. Lennox LB, Alexander M (1981) Fungicide enhancement of nitrogen fixation and colonization of Phaseolus vulgaris by Rhizobium phaseoli. Appl Environ Microb 41:404–411
114. Levrat P, Pussard M, Alabouvette C (1992) Enhanced bacterial metabolism of a Pseudomonas strain in response to the addition of culture filtrate of a bacteriophagous amoeba. Eur J Protistol 28:79–84
115. Louche J, Ali MA, Cloutier-Hurteau B, Sauvage F-X, Quiquampoix H, Plassard C (2010) Efficiency of acid phosphatases secreted from the ectomycorrhizal fungus Hebeloma cylindrosporum to hydrolyse organic phosphorus in podzols. FEMS Microbiol Ecol 73:323–335
116. Manzoni S, Taylor P, Richter A, Porporato A, Ågren GI (2012) Environmental and stoichiometric controls on microbial carbon‐use efficiency in soils. New Phytol 196:79–91
117. Marmeisse R, Guidot A, Gay G, Lambilliotte R, Sentenac H, Combier JP, Melayah D, Fraissinet-Tachet L, Debaud JC (2004) Hebeloma cylindrosporum - a model species to study ectomycorrhizal symbiosis from gene to ecosystem. New Phytol 163:481–498
118. Matz C, Kjelleberg S (2005) Off the hook–how bacteria survive protozoan grazing. Trends Microbiol 13:302–307
119. Mazzola M, de Bruijn I, Cohen MF, Raaijmakers JM (2009) Protozoan-induced regulation of cyclic lipopeptide biosynthesis is an effective predation defense mechanism for Pseudomonas fluorescens. Appl Environ Microb 75:6804–6811
120. Meier IC, Avis PG, Phillips RP (2013) Fungal communities influence root exudation rates in pine seedlings. FEMS Microbiol Ecol 83:585–595
121. Mooshammer M, Wanek W, Hämmerle I, Fuchslueger L, Hofhansl F, Knoltsch A, Schnecker J, Takriti M, Watzka M, Wild B, Keiblinger KM, Zechmeister-Boltenstern S, Richter A (2014a) Adjustment of microbial nitrogen use efficiency to carbon: nitrogen imbalances regulates soil nitrogen cycling. Nat Commun 5:1–7
122. Mooshammer M, Wanek W, Zechmeister-Boltenstern S, Richter A (2014b) Stoichiometric imbalances between terrestrial decomposer communities and their resources: mechanisms and implications of microbial adaptations to their resources. Front Microbiol 5:1–10
123. Nasholm T, Kielland K, Ganeteg U (2009) Uptake of organic nitrogen by plants. New Phytol 182:31–48
124. Neff JC, Chapin FS III, Vitousek PM (2003) Breaks in the cycle: dissolved organic nitrogen in terrestrial ecosystems. Front Ecol Environ 1:205–211
125. Neidig N, Jousset A, Nunes F, Bonkowski M, Paul RJ, Scheu S (2010) Interference between bacterial feeding nematodes and amoebae relies on innate and inducible mutual toxicity. Funct Ecol 24:1133–1138
126. Olsson PA, Baath E, Jakobsen I, Söderstrom B (1996) Soil bacteria respond to presence of roots but not to mycelium of arbuscular mycorrhizal fungi. Soil Biol Biochem 28:463–470
127. Parry JD (2004) Protozoan grazing of freshwater biofilms. Adv Appl Microbiol 54:167–196
128. Peters JL, Sutton AJ, Jones DR, Abrams KR, Rushton L (2006) Comparison of two methods to detect publication bias in meta-analysis. Jama-J Am Med Assoc 295:676–680
129. Pimentel D (2006) Soil erosion: a food and environmental threat. Environ Dev Sust 8:119–137
130. Plassard C, Dell B (2010) Phosphorus nutrition of mycorrhizal trees. Tree Physiol 30:1129–1139
131. Plassard C, Bonafos B, Touraine B (2000) Differential effects of mineral and organic N sources, and of ectomycorrhizal infection by Hebeloma cylindrosporum, on growth and N utilization in Pinus pinaster. Plant Cell Environ 23:1195–1205
132. Plassard C, Louche J, Ali MA, Duchemin M, Legname E, Cloutier-Hurteau B (2011) Diversity in phosphorus mobilisation and uptake in ectomycorrhizal fungi. Ann For Sci 68:33–43
133. Postma-Blaauw M, de Vries FT, De Goede R, Bloem J, Faber J, Brussaard L (2005) Within-trophic group interactions of bacterivorous nematode species and their effects on the bacterial community and nitrogen mineralization. Oecologia 142:428–439
134. Puglisi E, Pascazio S, Suciu N, Cattani I, Fait G, Spaccini R, Crecchio C, Piccolo A, Trevisan M (2013) Rhizosphere microbial diversity as influenced by humic substance amendments and chemical composition of rhizodeposits. J Geochem Explor 129:82–94
135. Pussard M, Alabouvette C, Levrat P (1994) Protozoan interactions with the soil microflora and possibilities for biocontrol of plant pathogens. In: Darbyshire JF (ed) Soil Protozoa. CAB International, Oxford, pp 123–146
136. Ramirez C, Alexander M (1980) Evidence suggesting protozoan predation on Rhizobium associated with germinating seeds and in the rhizosphere of beans (Phaseolus vulgaris L.). Appl Environ Microb 40:492–499
137. Rønn R, McCaig AE, Griffiths BS, Prosser JI (2002) Impact of protozoan grazing on bacterial community structure in soil microcosms. Appl Environ Microb 68:6094–6105
138. Rønn R, Vestergard M, Ekelund F (2012) Interactions between bacteria, protozoa and nematodes in soil. Acta Protozool 51:223–235
139. Rosenberg K, Bertaux J, Krome K, Hartmann A, Scheu S, Bonkowski M (2009) Soil amoebae rapidly change bacterial community composition in the rhizosphere of Arabidopsis thaliana. ISME J 3:675–684
140. Saleem M, Fetzer I, Dormann CF, Harms H, Chatzinotas A (2012) Predator richness increases the effect of prey diversity on prey yield. Nat Commun 3:1305
141. Sardans J, Rivas-Ubach A, Penuelas J (2012) The elemental stoichiometry of aquatic and terrestrial ecosystems and its relationships with organismic lifestyle and ecosystem structure and function: a review and perspectives. Biogeochemistry 111:1–39
142. Schlaghamersky J, Eisenhauer N, Frelichc LE (2014) Earthworm invasion alters enchytraeid community composition and individual biomass in northern hardwood forests of North America. Appl Soil 83:159–169
143. Sinsabaugh RL, Manzoni S, Moorhead DL, Richter A (2013) Carbon use efficiency of microbial communities: stoichiometry, methodology and modelling. Ecol Lett 16:930–939
144. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, London
145. Somasundaram S, Bonkowski M, Iijima M (2008) Functional role of mucilage-border cells: a complex facilitating protozoan effects on plant growth. Plant Prod Sci 11:344–351
146. Sundin P, Valeur A, Olsson S, Odham G (1990) Interactions between bacteria-feeding nematodes and bacteria in the rape rhizosphere - Effects on root exudation and distribution of bacteria. FEMS Microbiol Ecol 73:13–22
147. Tao J, Chen X, Liu M, Hu F, Griffiths B, Li H (2009) Earthworms change the abundance and community structure of nematodes and protozoa in a maize residue amended rice-wheat rotation agro-ecosystem. Soil Biol Biochem 41:898–904
148. Tibbett M, Sanders FE (2002) Ectomycorrhizal symbiosis can enhance plant nutrition through improved access to discrete organic nutrient patches of high resource quality. Ann Bot-London 89:783–789
149. Venette RC, Ferris H (1998) Influence of bacterial type and density on population growth of bacterial-feeding nematodes. Soil Biol Biochem 30:949–960
150. Vitousek PM et al (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57:1–45
151. Wagg C, Bender SF, Widmer F, van der Heijden MGA (2014) Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proc Natl Acad Sci U S A 111:5266–5270
152. Wall DH, Bardgett RD, Kelly EF (2010) Biodiversity in the dark. Nat Geosci 3:297–298
153. Wallenda T, Read DJ (1999) Kinetics of amino acid uptake by ectomycorrhizal roots. Plant Cell Environ 22:179–187
154. Weekers PH, Bodelier PL, Wijen JP, Vogels GD (1993) Effects of grazing by the free-living soil amoebae Acanthamoeba castellanii, Acanthamoeba polyphaga, and Hartmannella vermiformis on various bacteria. Appl Environ Microb 59:2317–2319
155. Weisse T (2002) The significance of inter- and intraspecific variation in bacterivorous and herbivorous protists. Anton Leeuw Int J G 81:327–341
156. Wright DJ (1975) Elimination of nitrogenous compounds by Panagrellus redivivus, Goodey, 1945 (Nematoda: Cephalobidae). Comp Biochem Phys B 52:247–253
157. Xiao HF, Griffiths B, Chen XY, Liu MQ, Jiao JG, Hu F, Li HX (2010) Influence of bacterial-feeding nematodes on nitrification and the ammonia-oxidizing bacteria (AOB) community composition. Appl Soil 45:131–137
158. Xu X, Thornton PE, Post WM (2013) A global analysis of soil microbial biomass carbon, nitrogen and phosphorus in terrestrial ecosystems. Global Ecol Biogeogr 22:737–749
159. Yeates GW (2003) Nematodes as soil indicators: functional and biodiversity aspects. Biol Fert Sci 37:199–210
160. Yeates G (2007) Abundance, diversity, and resilience of nematode assemblages in forest soils. Can J Forest Res 37:216–225
161. Zechmeister-Boltenstern S, Keiblinger KM, Mooshammer M, Peñuelas J, Richter A, Sardans J, Wanek W (2015) The application of ecological stoichiometry to plant–microbial–soil organic matter transformations. Ecol Monogr 85:133–155
162. Zwart KB, Darbyshire JF (1992) Growth and nitrogenous excretion of a common soil flagellate Spumella sp. - a laboratory experiment. J Soil Sci 43:145–157