Abstract
Background and aims
The rhizosphere priming effect (RPE) is the stimulation or suppression of soil organic matter decomposition by living roots and associated rhizosphere organisms. The RPE is pivotal in regulating biogeochemical cycles in terrestrial ecosystems. However, biological mechanisms, especially soil micro-food web interactions, behind the RPE remain largely unknown.
Methods
We quantified the RPE of soybean and cottonwood at three growth stages using a natural 13C tracer method, measured soil microbial and nematode community composition, and investigated their relations with the RPE.
Results
The magnitude of the RPE varied widely at different growth stages. Soybean produced a greater cumulative RPE than cottonwood. The plant species effect was also observed in the bacterial PLFA with higher values found in the soybean treatment. Mantel test analysis suggested that the variations in microbial community were closely related with the RPE, soil and plant characteristics. The nematode community affected the RPE indirectly through altering the structure of the microbial community.
Conclusions
We demonstrated that the RPE was connected with interactions of soil micro-food webs. This connection indicates that soil micro-food web interactions in the rhizosphere may either regulate microbial turnover and/or microbial community composition, subsequently modulating the RPE.
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Abbreviations
- RPE:
-
Rhizosphere priming effect
- SOM:
-
Soil organic matter
- SOC:
-
Soil organic carbon
- PVC:
-
Polyvinyl chloride
- MBC:
-
Microbial biomass carbon
- MBN:
-
Microbial biomass nitrogen
- PLFA:
-
Phospholipid fatty acid
- DOC:
-
Dissolved organic carbon
- DTN:
-
Dissolved total nitrogen
References
Alphei J, Bonkowski M, Scheu S (1996) Protozoa, nematoda and Lumbricidae in the rhizosphere of Hordelymus europaeus (Poaceae): faunal interactions, response of microorganisms and effects on plant growth. Oecologia 106:111–126
Arbuckle JL (2006) Amos (Version 7.0) [Computer Program]. SPSS, Chicago
Bird JA, Herman DJ, Firestone MK (2011) Rhizosphere priming of soil organic matter by bacterial groups in a grassland soil. Soil Biol Biochem 43:718–725
Blagodatskaya ЕV, Kuzyakov Y (2008) Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review. Biol Fertil Soils 45:115–131
Blagodatskaya EV, Blagodatsky SA, Anderson TH, Kuzyakov Y (2007) Priming effects in Chernozem induced by glucose and N in relation to microbial growth strategies. Appl Soil Ecol 37:95–105
Blagodatsky S, Blagodatskaya E, Yuyukina T, Kuzyakov Y (2010) Model of apparent and real priming effects: Linking microbial activity with soil organic matter decomposition. Soil Biology and Biochemistry 42(8):1275-1283
Bongers T (1990) The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83:14–19
Bongers T (1994) De Nematoden van Nederland. In: Vormgeving en technische realisatie. Uitgeverij Pirola, Schoorl, Netherlands
Bongers T, Bongers M, (1998) Functional diversity of nematodes. Applied Soil Ecology 10(3):239-251
Bossio DA, Scow KM, Gunapala N, Graham KJ (1998) Determinants of soil microbial communities: effects of agricultural management, season, and soil type on phospholipid fatty acid profiles. Microb Ecol 36:1–12
Bossuyt H, Denef H, Six J, Frey SD, Merckx R, Paustian K (2001) Influence of microbial populations and residue quality on aggregate stability. Appl Soil Ecol 16:195–208
Briar SS, Fonte SJ, Park I, Six J, Scow K, Ferris H (2011) The distribution of nematodes and soil microbial communities across soil aggregate fractions and farm management systems. Soil Biol Biochem 43:905–914
Cheng W (2009) Rhizosphere priming effect: its functional relationships with microbial turnover, evapotranspiration, and C-N budgets. Soil Biol Biochem 41:1795–1801
Cheng W, Coleman DC (1990) Effect of living roots on soil organic matter decomposition. Soil Biol Biochem 22:781–787
Cheng W, Kuzyakov Y (2005) Root effects on soil organic matter decomposition. In: Zobel RW, Wright SF (eds). Roots and soil management: interactions between roots and the soil. Agronomy monograph no 48. Madison, WI, USA: Am Soc of Agron/Crop Sci Soc Am/Soil Sci Soc Am J: 119–143
Cheng W, Johnson DW, Fu S (2003) Rhizosphere effects on decomposition: controls of plant species, phenology, and fertilization. Soil Sci Soc Am J 67:1418–1427
Cheng W, Parton WJ, Gonzalez-Meler MA, Phillips R, Asao S, Mcnickle GG, Brzostek E, Jastrow JD (2014) Synthesis and modeling perspectives of rhizosphere priming. New Phytol 201:31–44
Danso SKA, Kapuya J, Hardarson G (1990) Nitrogen fixation and growth of soybean as influenced by varying the methods of inoculation with Bradyrhizobium japonicum. Plant Soil 125:81–86
Dijkstra FA, Carrillo Y, Pendall E, Morgan JA (2013) Rhizosphere priming: a nutrient perspective. Front Microbiol 4:216
Djigal D, Brauman A, Diop T, Chotte JL, Villenave C (2004) Influence of bacterial-feeding nematodes (Cephalobidae) on soil microbial communities during maize growth. Soil Biol Biochem 36:323–331
Ferris H, Bongers T, de Goede RGM (2001) A framework for soil food web diagnostics: extension of the nematode faunal analysis concept. Applied Soil Ecology 18(1):13-29
Ferris H, Sánchez-Moreno S, Brennan EB (2012) Structure, functions and interguild relationships of the soil nematode assemblage in organic vegetable production. Appl Soil Ecol 61:16–25
Fonseca CR, John JL (1996) Connectance, a role for community allometry. Oikos 77:353–358
Fontaine S, Mariotti A, Abbadie L (2003) The priming effect of organic matter: a question of microbial competition? Soil Biol Biochem 35:837–843
Fontaine S, Barot S, Barre P, Bdioui N, Mary B, Rumpel C (2007) Stability of soil carbon in deep soil layers controlled by fresh carbon supply. Nature 450:277–280
Fu X, Guo D, Wang H, Dai X, Li M, Chen F (2017) Differentiating between root- and leaf-litter controls on the structure and stability of soil micro-food webs. Soil Biol Biochem 113:192–200
Grace JB (2006) Structural equation modeling and natural systems. Cambridge University Press, Cambridge, pp 1–365
Ingham RE, Trofymow JA, 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
Kuzyakov Y (2002) Review: factors affecting rhizosphere priming effects. J Plant Nutr Soil Sci 4:66–70
Kuzyakov Y (2010) Priming effects: interactions between living and dead organic matter. Soil Biol Biochem 42:1363–1371
Kuzyakov Y, Cheng W (2001) Photosynthesis controls of rhizosphere respiration and organic matter decomposition. Soil Biol Biochem 33:1915–1925
Li Q, Liang WJ, Zhang XK, Mohammad M (2017) Soil nematodes of grasslands in northern China. Zhejiang University Press, China
Liang W, Lou Y, Li Q, Zhong S, Zhang X, Wang J (2009) Nematode faunal response to long-term application of nitrogen fertilizer and organic manure in Northeast China. Soil Biol Biochem 41:883–890
Liang C, Schimel JP, Jastrow JD (2017) The importance of anabolism in microbial control over soil carbon storage. Nat Microbiol 2:17105
Lundquist E, Jackson L, Scow K, Hsu C (1999) Changes in microbial biomass and community composition, and soil carbon and nitrogen pools after incorporation of rye into three California agricultural soils. Soil Biol Biochem 31:221–236
McGill WB, Figueiredo CT (1993) Total nitrogen. In: Carter MR (ed) Soil sampling and methods of analysis. Lewis Publishers, Boca Raton, pp 201–211
Moore-Kucera J, Dick RP (2008) Application of 13C-labeled litter and root materials for in situ decomposition studies using phospholipid fatty acids. Soil Biol Biochem 40:2485–2493
Nobili M, Contin M, Mondini C, Brookes PC (2001) Soil microbial biomass is triggered into activity by trace amounts of substrate. Soil Biol Biochem 33:1163–1170
Nottingham AT, Griffiths H, Chamberlain PM, Stott AW, Tanner EVJ (2009) Soil priming by sugar and leaf-litter substrates: a link to microbial groups. Appl Soil Ecol 42:183–190
Otten W, Hall D, Harris K, Ritz K, Young IM, Gilligan CA (2001) Soil physics, fungal epidemiology and the spread of Rhizoctonia solani. New Phytol 151:459–468
Paterson E, Gebbing T, Abel C, Sim A, Telfer G (2007) Rhizodeposition shapes rhizosphere microbial community structure in organic soil. New Phytol 173:600–610
Pimm SL (1984) The complexity and stability of ecosystems. Nature 307:321–326
Rowell DL (1994) Soil science: methods and applications. Harlow, Longman, pp 1–350
Sánchez-Moreno S, Ferris H, Young-Mathews A, Culman SW, Jackson LE (2011) Abundance, diversity and connectance of soil food web channels along environmental gradients in an agricultural landscape. Soil Biol Biochem 43:2374–2383
Shahzad T, Chenu C, Genet P, Barot S, Perveen N, Mougin C, Fontaine S (2015) Contribution of exudates, arbuscular mycorrhizal fungi and litter depositions to the rhizosphere priming effect induced by grassland species. Soil Biol Biochem 80:146–155
Su T, Dijkstra FA, Wang P, Cheng W (2017) Rhizosphere priming effects of soybean and cottonwood: do they vary with latitude? Plant Soil 420:1–12
Vance ED, Brooks PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707
Warembourg FR, Estelrich HD (2001) Plant phenology and soil fertility effects on below-ground carbon allocation for an annual (Bromus madritensis) and a perennial (Bromus erectus) grass species. Soil Biol Biochem 10:1291–1303
Yeates GW (2003) Nematodes as soil indicators: functional and biodiversity aspects. Biol Fertil Soils 37:199–210
Zhang S, Li Q, Lü Y, Zhang X, Liang W (2013) Contributions of soil biota to C sequestration varied with aggregate fractions under different tillage systems. Soil Biol Biochem 62:147–156
Zhu B, Cheng W (2011) 13C isotope fractionation during rhizosphere respiration of C3 and C4 plants. Plant Soil 342:277–287
Zhu B, Cheng WX (2013) Impacts of drying-wetting cycles on rhizosphere respiration and soil organic matter decomposition. Soil Biol Biochem 63:89–96
Acknowledgements
This research was supported by the National Key Research and Development Plan of China (2017YFD0200602).
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Kou, X., Su, T., Ma, N. et al. Soil micro-food web interactions and rhizosphere priming effect. Plant Soil 432, 129–142 (2018). https://doi.org/10.1007/s11104-018-3782-7
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DOI: https://doi.org/10.1007/s11104-018-3782-7
Keywords
- Soil micro-food web
- Rhizosphere priming effect
- Microbial PLFA
- Nematode community