Biology and Fertility of Soils

, Volume 52, Issue 8, pp 1105–1119 | Cite as

Hotspots of microbial activity induced by earthworm burrows, old root channels, and their combination in subsoil

  • Duyen T. T. HoangEmail author
  • Johanna Pausch
  • Bahar S. Razavi
  • Irina Kuzyakova
  • Callum C. Banfield
  • Yakov Kuzyakov
Original Paper


Biopores are pores or voids in soil produced by roots, by earthworms, or by the occupation of earthworms in root pores, which are considered important microbial hotspots, especially in subsoil. We hypothesized that earthworms (Lumbricus terrestris L.) exert stronger effects on microbial activities than decaying plant roots (of Cichorium intybus L.) in the subsoil because of the addition of pre-digested organic material. We tested this hypothesis by analyzing microbial biomass (Cmic), total organic C (Corg), and activities of eight enzymes (cellobiohydrolase, β-glucosidase, xylanase, acid phosphomonoesterase, leucine aminopeptidase, tyrosine aminopeptidase, chitotriosidase, and n-acetylglucosaminidase) down to 105-cm depth. The Cmic increase was associated with a two- to threefold increase of Corg content in biopores as compared to bulk soil. The highest percentage of Cmic-to-Corg (3.7 to 7.3 %) in the drilosphere demonstrated the enhancement of microbial efficiency for organic matter decomposition by earthworms. The availability of organic matter in biopores increased the activities of C- and N-targeting enzymes by 1.2–11.3 times, but reduced acid phosphomonoesterase activity by 10–40 % in biopores versus bulk soil. Introducing earthworms in root biopores caused 1.5–1.8 times higher microbial biomass and 1.2–1.9 times increased enzyme activities compared to the sole effect of earthworms. Soil depth showed a strong effect on the drilosphere, but only slight effects on the biochemical properties of root biopores and bulk soil. In conclusion, biopores are important microbial hotspots of C, N, and P transformations in subsoil. Earthworms exerted stronger effects on biochemical properties of biopores than decaying roots.


Earthworms Biopores Enzyme activities Catalytic efficiency Microbial activities Subsoil processes 



We thank Dr. Timo Kautz for the field experiment setup, Dr. Evgenia Blagodatskaya for the fruitful suggestions on the experimental setup, Dr. Norman Loftfield for the support in laboratory, and the Centre for Stable Isotope Research and Analysis—KOSI (Göttingen, Germany) for the TOC measurement. We gratefully acknowledge the Vietnamese government for supporting DH, and DAAD for supporting BSR. The study was supported by the German Research Foundation in the framework of the project PAK 888.1.

Supplementary material

374_2016_1148_MOESM1_ESM.pdf (199 kb)
ESM 1 Supplementary S1 Relationship between Cmic and Ka. (PDF 91 kb)


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Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Duyen T. T. Hoang
    • 1
    • 4
    Email author
  • Johanna Pausch
    • 1
  • Bahar S. Razavi
    • 2
  • Irina Kuzyakova
    • 3
  • Callum C. Banfield
    • 1
  • Yakov Kuzyakov
    • 1
    • 2
  1. 1.Department of Soil Science of Temperate EcosystemsGeorg-August University of GöttingenGöttingenGermany
  2. 2.Department of Agricultural Soil ScienceGeorg-August University of GöttingenGöttingenGermany
  3. 3.Department of Ecoinformatics, Biometrics and Forest GrowthGeorg-August University of GöttingenGöttingenGermany
  4. 4.Department of Soil ScienceForestry UniversityHanoiVietnam

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