Skip to main content

Soil micro-food web interactions and rhizosphere priming effect

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.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

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

    Article  Google Scholar 

  • Arbuckle JL (2006) Amos (Version 7.0) [Computer Program]. SPSS, Chicago

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Bongers T (1990) The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83:14–19

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Cheng W (2009) Rhizosphere priming effect: its functional relationships with microbial turnover, evapotranspiration, and C-N budgets. Soil Biol Biochem 41:1795–1801

    Article  CAS  Google Scholar 

  • Cheng W, Coleman DC (1990) Effect of living roots on soil organic matter decomposition. Soil Biol Biochem 22:781–787

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Dijkstra FA, Carrillo Y, Pendall E, Morgan JA (2013) Rhizosphere priming: a nutrient perspective. Front Microbiol 4:216

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Fonseca CR, John JL (1996) Connectance, a role for community allometry. Oikos 77:353–358

    Article  Google Scholar 

  • Fontaine S, Mariotti A, Abbadie L (2003) The priming effect of organic matter: a question of microbial competition? Soil Biol Biochem 35:837–843

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Grace JB (2006) Structural equation modeling and natural systems. Cambridge University Press, Cambridge, pp 1–365

    Book  Google Scholar 

  • 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

    Article  Google Scholar 

  • Kuzyakov Y (2002) Review: factors affecting rhizosphere priming effects. J Plant Nutr Soil Sci 4:66–70

    Google Scholar 

  • Kuzyakov Y (2010) Priming effects: interactions between living and dead organic matter. Soil Biol Biochem 42:1363–1371

    Article  CAS  Google Scholar 

  • Kuzyakov Y, Cheng W (2001) Photosynthesis controls of rhizosphere respiration and organic matter decomposition. Soil Biol Biochem 33:1915–1925

    Article  CAS  Google Scholar 

  • Li Q, Liang WJ, Zhang XK, Mohammad M (2017) Soil nematodes of grasslands in northern China. Zhejiang University Press, China

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Liang C, Schimel JP, Jastrow JD (2017) The importance of anabolism in microbial control over soil carbon storage. Nat Microbiol 2:17105

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • McGill WB, Figueiredo CT (1993) Total nitrogen. In: Carter MR (ed) Soil sampling and methods of analysis. Lewis Publishers, Boca Raton, pp 201–211

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Pimm SL (1984) The complexity and stability of ecosystems. Nature 307:321–326

    Article  Google Scholar 

  • Rowell DL (1994) Soil science: methods and applications. Harlow, Longman, pp 1–350

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Vance ED, Brooks PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Yeates GW (2003) Nematodes as soil indicators: functional and biodiversity aspects. Biol Fertil Soils 37:199–210

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Zhu B, Cheng W (2011) 13C isotope fractionation during rhizosphere respiration of C3 and C4 plants. Plant Soil 342:277–287

    Article  CAS  Google Scholar 

  • Zhu B, Cheng WX (2013) Impacts of drying-wetting cycles on rhizosphere respiration and soil organic matter decomposition. Soil Biol Biochem 63:89–96

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by the National Key Research and Development Plan of China (2017YFD0200602).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Qi Li or Peng Wang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Responsible Editor: Eric Paterson

Electronic supplementary material

ESM 1

(DOCX 14 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-018-3782-7

Keywords

  • Soil micro-food web
  • Rhizosphere priming effect
  • Microbial PLFA
  • Nematode community