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. Hoang
  • Johanna Pausch
  • Bahar S. Razavi
  • Irina Kuzyakova
  • Callum C. Banfield
  • Yakov Kuzyakov
Original Paper

Abstract

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.

Keywords

Earthworms Biopores Enzyme activities Catalytic efficiency Microbial activities Subsoil processes 

Notes

Acknowledgments

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)

References

  1. Aira M, Monroy F, Dominguez J (2003) Effects of two species of earthworms (Allolobophora sp.) on soil systems: a microfaunal and biochemical analysis. Pedobiologia 47:877–881Google Scholar
  2. Aira M, Monroy F, Domίnguez J (2007) Earthworms strongly modify microbial biomass and activity triggering enzymatic activities during vermicomposting independently of the application rates of pig slurry. Sci Total Environ 385:252–261CrossRefPubMedGoogle Scholar
  3. Allison SD (2005) Cheaters, diffusion and nutrients constrain decomposition by microbial enzymes in spatially structured environments. Ecology Letter 8:626–635CrossRefGoogle Scholar
  4. Allison SD, Vitousek PM (2005) Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biol Biochem 37:937–944CrossRefGoogle Scholar
  5. Anderson JPE, Domsch KH (1978) A physiological method for the quantitative measurement of microbial biomass in soils. Soil Biol Biochem 3:215–221CrossRefGoogle Scholar
  6. Anderson TH, Domsch KH (1989) Ratios of microbial biomass carbon to total organic carbon in arable soils. Soil Biol Biochem 21:471–479CrossRefGoogle Scholar
  7. Bamminger C, Zaiser N, Zinsser P, Lamers M, Kammann C, Marhan S (2014) Effects of biochar, earthworms, and litter addition on soil microbial activity and abundance in a temperate agricultural soil. Biol Fertil Soils 50:1189–1200CrossRefGoogle Scholar
  8. Barois I, Lavelle P (1986) Changes in respiration rate and some physicochemical properties of a tropical soil during transit through Pontoscolex core-thrurus (Glossoscolecidae, Oligochaeta). Soil Biol Biochem 18:539–541CrossRefGoogle Scholar
  9. Bastian F, Bouziri L, Nicolardot B, Ranjard L (2009) Impact of wheat straw decomposition on successional patterns of soil microbial community structure. Soil Biol Biochem 41:262–275CrossRefGoogle Scholar
  10. Bauhus J, Paré D, Côté L (1997) Effects of tree species, stand age and soil type on soil microbial biomass and its activity in a southern boreal forest. Soil Biol Biochem 30:1077–1089CrossRefGoogle Scholar
  11. Beck T (1984) Mikrobiologische und biochemische Charackterisierung landwirtschaftlich genutzter Böden II Mitteilung Beziehung zum Humusgehalt. Zeitschrift für Pflanzenernährung und Bodenkunde 147:467–475CrossRefGoogle Scholar
  12. Blagodatskaya EV, Anderson TH (1999) Adaptive responses of soil microbial communities under experimental acid stress in controlled laboratory studies. Appl Soil Ecol 11:207–216CrossRefGoogle Scholar
  13. Blagodatskaya E, Yuyukina T, Blagodatsky S, Kuzyakov Y (2011) Three-source-partitioning of microbial biomass and of CO2 efflux from soil to evaluate mechanisms of priming effects. Soil Biol Biochem 43:778–786CrossRefGoogle Scholar
  14. Blagodatsky SA, Yevdokimov IV, Larionova AA, Richter J (1998) Microbial growth in soil and nitrogen turnover: model calibration with laboratory data. Soil Biol Biochem 30:1757–1764CrossRefGoogle Scholar
  15. Brown GG, Barois I, Lavelle P (2000) Regulation of soil organic matter dynamics and microbial activity in the drilosphere and the role of interactions with other edaphic functional domains. Eur J Soil Biol 36:177–198CrossRefGoogle Scholar
  16. Buck C, Langmaack M, Schrader S (1999) Nutrient content of earthworm casts influenced by different mulch types. Eur J Soil Biol 35:23–30CrossRefGoogle Scholar
  17. Buttigieg PL, Ramette A (2014) A guide to statistical analysis in microbial ecology: a community-focused, living review of multivariate data analyses. FEMS Microbiol Ecol 90:543–550.CrossRefPubMedGoogle Scholar
  18. Capowiez Y, Bottinelli N, Sammartino S, Michel E, Jouquet P (2015) Morphological and functional characterisation of the burrow systems of six earthworm species (Lumbricidae). Biol Fertil Soils 51:869–877CrossRefGoogle Scholar
  19. Chenu C, Stotzky G (2002) Interactions between microorganisms and soil particles: an overview. In: Huang PM, Bollag J-M, Senesi N (eds) Interaction between soil particles and microorganisms. John Wiley and Sons, Ltd, West Sussex, pp 4–40Google Scholar
  20. Creamer RE, Schulte RPO, Stone D, Gal A, Krogh PH, Papa GL, Murray PJ, Pérès G, Foerster B, Rutgers M, Sousa JP, Winding A (2014) Measuring soil respiration across Europe: do incubation temperature and incubation period matter? Ecol Indic 36:409–418CrossRefGoogle Scholar
  21. Dippold MA, Kuzyakov Y (2013) Biogeochemical transformations of amino acids in soil assessed by position-specific labelling. Plant Soil 373:385–401CrossRefGoogle Scholar
  22. Don A, Steinberg B, Schöning I, Pritsch K, Joschoko M, Gleixner G, Schulze ED (2008) Organic carbon sequestration in earthworm burrows. Soil Biol Biochem 40:1803–1812CrossRefGoogle Scholar
  23. Eivazi F, Tabatabai MA (1977) Phosphatases in soils. Soil Biol Biochem 09:167–172CrossRefGoogle Scholar
  24. Farrell RE, Gupta VVSR, Germida JJ (1994) Effects of cultivation on the activity and kinetics of Arylsulfatase in Saskatchewan soils. Soil Biol Biochem 26:1033–1040CrossRefGoogle Scholar
  25. Flegel M, Schrader S (2000) Importance of food quality on selected enzyme activities in earthworm casts (Dendrobaena octaedra, Lumbricidae). Soil Biol Biochem 32:1191–1196CrossRefGoogle Scholar
  26. German DP, Chacon SS, Allison SD (2011) Substrate concentration and enzyme allocation can affect rates of microbial decomposition. Ecology 92:1471–1480CrossRefPubMedGoogle Scholar
  27. Gill RA, Burke IC (2002) Influence of soil depth on the decomposition of Bouteloua gracilis roots in the shortgrass steppe. Plant Soil 241:233–242CrossRefGoogle Scholar
  28. Gilot C (1997) Effects of a tropical geophageous earthworm, M. anomala (Megascolecidae), on soil characteristics and production of a yam crop in Ivory Coast. Soil Biol Biochem 29:353–359CrossRefGoogle Scholar
  29. Goberna M, Insam H, Klammer S, Pascual JA, Sanchez J (2005) Microbial community structure at different depths in disturbed and undisturbed semiarid mediterranean forest soils. Microb Ecol 50:315–326CrossRefPubMedGoogle Scholar
  30. Hamid R, Khan MA, Ahmad M, Ahmad MM, Abdin MZ, Musarrat J, Javed S (2013) Chitinases: an update. J Pharm Bioallied Sci 5:21–29PubMedPubMedCentralGoogle Scholar
  31. Hoang TTD, Razavi BS, Kuzyakov Y, Blagodatskaya E (2016) Earthworm burrows: kinetics and spatial distribution of enzymes of C-, N- and P- cycles. Soil Biol Biochem 99:94–103CrossRefGoogle Scholar
  32. Hodge A, Robinson D, Filter A (2000) Are microorganisms more effective than plants at competing for nitrogen? Trends Plant Sci 5:304–308CrossRefPubMedGoogle Scholar
  33. Jégou D, Schrader S, Diestel H, Cluzeau D (2001) Morphological, physical and biochemical characteristics of burrow walls formed by earthworms. Appl Soil Ecol 17:165–174CrossRefGoogle Scholar
  34. Jenkinson DS, Ladd JN (1981) Microbial biomass in soil: measurement and turnover. In: Paul EA, Ladd JN (eds) Soil biochemistry, vol 5. Dekker, New York, pp 415–471Google Scholar
  35. Kautz T (2014) Research on subsoil biopores and their functions in organically managed soils: a review. Renew Agr Food Syst 30:318–327CrossRefGoogle Scholar
  36. Kautz T, Amelung W, Ewert F, Gaiser T, Horn R, Jahn R, Javaux M, Kemna A, Kuzyakov Y, Munch JC, Pätzold S, Peth S, Scherer HW, Schloter M, Schneider H, Vanderborght J, Vetterlein D, Walter A, Wiesenberg GLB, Köpke U (2013) Nutrient acquisition from arable subsoils in temperate climates: a review. Soil Biol Biochem 57:1003–1022CrossRefGoogle Scholar
  37. Kautz T, Lüsebrink M, Pätzold S, Vetterlein D, Pude R, Athmann M, Küpper PM, Perkons U, Köpke U (2014) Contribution of anecic earthworms to biopore formation during cultivation of perennial ley crops. Pedobiologia 57:47–52CrossRefGoogle Scholar
  38. Kibblewhite MG, Ritz K, Swift MJ (2007) Soil health in agricultural systems. Philos Trans R Soc B 363:685–701CrossRefGoogle Scholar
  39. Koch AL (1985) The macroeconomics of bacterial growth. In: Fletcher M, Floodgate GD (eds) Bacteria in their natural environments. Academic, London, pp 1–42Google Scholar
  40. Koch O, Tscherko G, Kandeler E (2007) Temperature sensitivity of microbial respiration, nitrogen mineralization, and potential soil enzyme activities in organic alpine soils. Global Biogeochem Cy 21:1–11CrossRefGoogle Scholar
  41. Kögel-Knabner I (2002) The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biol Biochem 34:139–162CrossRefGoogle Scholar
  42. Kuzyakov Y (2010) Priming effects: interactions between living and dead organic matter. Soil Biol Biochem 42:1363–1371CrossRefGoogle Scholar
  43. Kuzyakov Y, Blagodatskaya E (2015) Microbial hotspots and hot moments in soil: concept and review. Soil Biol Biochem 83:184–199CrossRefGoogle Scholar
  44. Lavelle P, Martin A (1992) Small-scale and large-scale effects of endogeic earthworm on soil organic matter dynamics in soils of the humid tropics. Soil Biol Biochem 24:1491–1498CrossRefGoogle Scholar
  45. Le Bayon RC, Binet F (2006) Earthworms change the distribution and availability of phosphorous in organic substrates. Soil Biol Biochem 38:235–246CrossRefGoogle Scholar
  46. Lin Q, Brookes PC (1999) An evaluation of the substrate-induced respiration method. Soil Biol Biochem 31:1969–1983CrossRefGoogle Scholar
  47. Lopez-Hernandez D, Lavelle P, Niño M (1993) Phosphorus transformations in two P-sorption contrasting tropical soils during transit through Pontoscolex corethrurus (Glossoscolecidae: Oligochaeta). Soil Biol Biochem 25:789–792CrossRefGoogle Scholar
  48. MacKay AD, Syers JK, Springett JA, Gregg PEH (1982) Plant availability of phosphorus in superphosphate and a phosphate rock as influenced by earthworms. Soil Biol Biochem 14:281–287CrossRefGoogle Scholar
  49. Malcolm RE (1983) Assessment of phosphatase activity in soils. Soil Biol Biochem 15:403–408CrossRefGoogle Scholar
  50. Marinissen JCY, de Ruiter PC (1993) Contribution of earthworm to carbon and nitrogen cycling in agro-ecosystems. Agric Ecosyst Environ 47:59–74CrossRefGoogle Scholar
  51. Martin A (1991) Short- and long-term effects of the endogeic earthworm Millsonia anomala (Omodeo) (Megascolecidæ, Oligochæta) of tropical savannas, on soil organic matter. Biol Fert Soils 11:234–238CrossRefGoogle Scholar
  52. Marx MC, Kandeler E, Wood M, Wermbter N, Jarvis SC (2005) Exploring the enzymatic landscape: distribution and kinetics of hydrolytic enzymes in soil particale-size fractions. Soil Biol Biochem 37:35–48CrossRefGoogle Scholar
  53. Matson PA, Parton W, Power A, Swift M (1997) Agricultural intensification and ecosystem properties. Science 277:504–509CrossRefPubMedGoogle Scholar
  54. Mcgill MB, Cannon KR, Robertson JA, Cook FD (1986) Dynamics of soil microbial biomass and water-soluble organic C in Breton L after 50 years of cropping to two rotations. Can J Soil Sci 66:1–19CrossRefGoogle Scholar
  55. Menichetti L, Ekblad A, Kätterer T (2014) Contribution of roots and amendments to soil carbon accumulation within the soil profile in a long-term field experiment in Sweden. Agric Ecosyst Environ 200:79–87CrossRefGoogle Scholar
  56. Mganga KZ, Razavi BS, Kuzyakov Y (2015) Microbial and enzymes response to nutrient additions in soils of Mt. Kilimanjaro region depending on land use. Eur J Soil Biol 69:33–40CrossRefGoogle Scholar
  57. Miller M, Dick RP (1995) Dynamics of soil C and microbial biomass in whole soil and aggregates in two cropping systems. Appl Soil Ecol 2:253–261CrossRefGoogle Scholar
  58. Nakamoto T (2000) The distribution of wheat and maize roots as influenced by biopores in a subsoil of the Kanto loam type. Plant Prod Sci 3:140–144CrossRefGoogle Scholar
  59. Nannipieri P, Gianfreda L (1998). Kinetics of enzyme reactions in soil environments. In: Huang PM, Senesi N, Buffle J (eds) Environmental particles-structure and surface reactions of soil particles. J. Wiley and Sons, pp 449–479Google Scholar
  60. Nannipieri P, Ceccanti B, Bianchi D (1988) Characterization of humus-phosphatase complexes extracted from soil. Soil Biol Biochem 20:683–691CrossRefGoogle Scholar
  61. Nannipieri P, Sequi P, Fusi P (1996) Humus and enzyme activity. In: Piccolo A (ed) Humic substances in terrestrial ecosystems. Elsevier, Amsterdam, pp 293–328CrossRefGoogle Scholar
  62. Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670CrossRefGoogle Scholar
  63. Nannipieri P, Giagnoni L, Landi L, Renella G (2011) Role of phosphatase enzymes in soil. In: Bunemann EK, Obreson A, Frossard E (eds) Phosphorus in action. Springer, Berlin, pp 215–243CrossRefGoogle Scholar
  64. Nannipieri P, Giagnoni L, Renella G, Puglisi E, Ceccanti B, Masciandaro G, Fornasier F, Moscatelli MC, Marinari S (2012) Soil enzymology: classical and molecular approaches. Biol Fertil Soils 48:743–762CrossRefGoogle Scholar
  65. Orchard VA, Cook FJ (1983) The relationship between soil respiration and soil moisture. Soil Biol Biochem 15:447–453CrossRefGoogle Scholar
  66. Pathan SI, Ceccherini MT, Pietramellara G, Puschenreiter M, Giagnoni L, Arenella M, Varanini Z, Nannpieri P, Renella G (2015) Enzyme activitiy and microbial community structure in the rhizosphere of two maize lines differing in N use efficiency. Plant Soil 387:413–424CrossRefGoogle Scholar
  67. Perkons U, Kautz T, Uteau D, Peth S, Geier V, Thomas K, Holz KL, Athmann M, Pude R, Köpke U (2014) Root-length densities of various annual crops following crops with contrasting root systems. Soil Till Res 137:50–57CrossRefGoogle Scholar
  68. Poll C, Marhan S, Ingwersen J, Kandeler E (2008) Dynamics of litter carbon turnover and microbial abundance in a rye detritusphere. Soil Biol Biochem 40:1306–1321CrossRefGoogle Scholar
  69. Rawlings ND, Morton FR, Barrett AT (2006) MEROPS: the peptidase database. Nucleic Acids Res 32:D160–D164CrossRefGoogle Scholar
  70. Razavi BS, Blagodatskaya E, Kuzyakov Y (2015) Nonlinear temperature sensitivity of enzyme kinetics explains canceling effect: a case study on loamy haplic Luvisol. Front Microbiol 6:1126CrossRefPubMedPubMedCentralGoogle Scholar
  71. Ritz K, Wheatley RE (1989) Effects of water amendment on basal and substrate-induced respiration rates of mineral soils. Biol Fert Soils 8:242–246Google Scholar
  72. Rodríguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotech Adv 17:319–339CrossRefGoogle Scholar
  73. Salomé C, Nunan N, Pouteau V, Lerch TZ, Chenu C (2010) Carbon dynamics in topsoil and in subsoil may be controlled by different regulatory mechanisms. Glob Chang Biol 16:416–426CrossRefGoogle Scholar
  74. Sanaullah M, Chabbi A, Leifeld J, Bardoux G, Billou D, Rumpel C (2011) Decomposition and stabilization of root litter in top- and subsoil horizons: what is the difference? Plant Soil 338:127–141CrossRefGoogle Scholar
  75. Satchell JE, Martin K (1984) Phosphatase activity in earthworm faeces. Soil Biol Biochem 16:191–194CrossRefGoogle Scholar
  76. Schimel JP, Weintraub MN (2003) The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem 35:549–563CrossRefGoogle Scholar
  77. Silver WL, Miya RK (2001) Global patterns in root decomposition: comparision of climate and litter quality effects. Oecologia 129:407–419CrossRefGoogle Scholar
  78. Spohn M, Kuzyakov Y (2014) Spatial and temporal dynamics of hotspots of enzyme activity in soil as affected by living and dead roots: a soil zymography analysis. Plant Soil 379:67–77CrossRefGoogle Scholar
  79. Stehouwer RC, Dick WA, Traina SJ (1993) Characteristics of earthworm burrow lining affecting atrazine sorption. J Environ Qual 22:181–185CrossRefGoogle Scholar
  80. Svensson K, Friberg H (2007) Changes in active microbial biomass by earthworms and grass amendments in agricultural soil. Biol Fert Soils 44:223–228CrossRefGoogle Scholar
  81. Tabatabai MA, Garcίa-Manzanedo AM, Acosta-Martίnez V (2002) Substrate specificity of arylamidase in soils. Soil Biol Biochem 34:103–110CrossRefGoogle Scholar
  82. Thielemann U (1986) The octet-method for sampling earthworm populations. Pedobiologia 29:296–302Google Scholar
  83. Tiunov AV, Scheu S (2000) Microfungal communities in soil, litter and casts of Lumbricus terrestris L. (Lumbricidae): a laboratory experiment. Appl Soil Ecol 14:17–26CrossRefGoogle Scholar
  84. Uksa M, Schloter M, Kautz T, Athmann M, Köpke U, Fischer D (2015) Spartial variability of hydrolytic and oxidative potential enzyme activities in different subsoil compartments. Biol Fertil Soils 51:517–521CrossRefGoogle Scholar
  85. Uteau D, Pagenkemper SK, Peth S, Horn R (2013) Root and time dependent soil structure formation and its influence on gas transport in the subsoil. Soil Till Res 132:69–76CrossRefGoogle Scholar
  86. Van Bruggen AHC, Semenov AM (2000) In search of biological indicators for soil health and disease suppression. Appl Soil Ecol 15:13–24CrossRefGoogle Scholar
  87. Van Der Waerden BL (1952) On the method of saddle points. Appl Sci Res B 2:33–45CrossRefGoogle Scholar
  88. Vetterlein D, Kühn T, Kaiser K, Jahn R (2013) Illite transformation and potasium release upon changes in composition of the rhizosphere soil solution. Plant Soil 371:267–279CrossRefGoogle Scholar
  89. Wan JHC, Wong MH (2004) Effects of earthworm activity and P-solubilizing bacteria on P availability in soil. J Soil Sci Plant Nutr 167:209–213CrossRefGoogle Scholar
  90. West AW, Sparling GP (1986) Modification to the substrate-induced respiration method to permit measurement of microbial biomass in soils of differing water contents. J Microbiol Meth 3:177–189CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Duyen T. T. Hoang
    • 1
    • 4
  • 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

Personalised recommendations