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Biology and Fertility of Soils

, Volume 55, Issue 6, pp 617–627 | Cite as

Reduced catalytic activity of an exogenous extracellular β-D-glucosidase due to adsorption on a model humic-clay complex and different soils under wetting and drying cycles

  • Pierluigi MazzeiEmail author
  • Alessandro PiccoloEmail author
Original Paper
  • 107 Downloads

Abstract

To ascertain the role of extracellular enzymes in soil biochemical reactions, we followed the changes in catalytic activity of an exogenous β-glucosidase (GLU) enzyme after its adsorption on a synthetic model humic-clay complex, composed by a lignite humic acid coupled by Al bridges to a Ca-montmorillonite (HM), and on three sterilised soils (DS, ISC and IST) with different properties. Either HM or the selected soils enabled a stable GLU adsorption that induced a significant decrease of GLU activity. In the case of soils, both the largest GLU adsorption and reduction of catalytic activity was observed for the clayey and organic matter-rich ISC soil. When the GLU-soil adducts were subjected to wetting and drying (W/D) cycles for 3 and 6 weeks, the enzyme activity was further largely reduced after the first 3 weeks of W/D, while the decrease progressed more slowly during the following 3 weeks. This was attributed to the increasing modification of the enzyme conformational structure due to formation of dispersive and hydrogen bonds with the inorganic and organic components of HM and soils. Our results showed that an exogenous extracellular enzyme, such as GLU, is quantitatively immobilised on model and real soil aggregates, and that the catalytic activity is significantly and progressively reduced by soil physical-chemical changes, thereby implying that soil biochemical transformations are to be accounted more to intracellular than extracellular enzymes.

Keywords

Soil extracellular enzymes Exogeneous β-D-glucosidase Humic-clay complexes Soils Wetting/drying cycles Enzyme catalysis 

Notes

Acknowledgements

This research was conducted by the first author in partial fulfilment of PhD work at the Department of Agricultural Sciences of the University of Naples Federico II.

Supplementary material

374_2019_1376_MOESM1_ESM.docx (159 kb)
ESM 1 (DOCX 158 kb)

References

  1. Ahmadi K, Razavi BS, Maharjan M, Kuzyakov Y, Kostka SJ, Carminati A, Zarebanadkouki M (2018) Effects of rhizosphere wettability on microbial biomass, enzyme activities and localization. Rhizosphere 7:35–42CrossRefGoogle Scholar
  2. Alarcón-Gutiérrez E, Floch C, Ziarelli F, Augur C, Criquet S (2010) Drying/rewetting cycles and γ-irradiation effects on enzyme activities of distinct layers from a Quercus ilex L. litter. Soil Biol Biochem 42:283–290Google Scholar
  3. Allison SD (2006) Soil minerals and humic acids alter enzyme stability: implications for ecosystem processes. Biogeochemistry 81:361–373CrossRefGoogle Scholar
  4. Bock K, Sigurskjold BW (1988) Mechanism and binding specificity of β-glucosidase-catalyzed hydrolysis of cellobiose analogues studied by competition enzyme kinetics monitored by H-NMR spectroscopy. Eur J Biochem 178:711–720CrossRefGoogle Scholar
  5. Borghetti C, Gioacchini P, Marzadori C (2003) Activity and stability of urease-hydroxyapatite and urease-hydroxyapatite-humic acid complexes. Biol Fertil Soils 38:96–101CrossRefGoogle Scholar
  6. Burns RG, DeForest JL, Marxsen J, Sinsabaugh RL, Stromberger ME, Wallenstein MD, Weintraub MN, Zoppini A (2013) Soil enzymes in a changing environment: current knowledge and future directions. Soil Biol Biochem 58:216–234CrossRefGoogle Scholar
  7. Busto MD, Perez-Mateos M (2000) Characterization of β-D glucosidase extracted from soil fractions. Eur J Soil Sci 51:193–200CrossRefGoogle Scholar
  8. Daou L, Perissol C, Luglia M, Calvert V, Criquet S (2016) Effects of drying/rewetting or freezing/thawing cycles on enzymatic activities of different Mediterranean soils. Soil Biol Biochem 93:142–149CrossRefGoogle Scholar
  9. Debosz K, Rasmussen PH, Pedersen AR (1999) Temporal variations in microbial biomass C and cellulolytic enzyme activity in arable soils: effects of organic matter input. Appl Soil Ecol 13:209–218CrossRefGoogle Scholar
  10. Dick RP (1994) Soil enzyme activity as an indicator of soil quality. In: Doran JW, Coleman DC, Bezdicek DF, Stewart BA (eds) Defining soil quality for a sustainable environment. SSSA Spec. Publ. 35. SSSA and ASA, Madison, pp 107–124Google Scholar
  11. Dick WA, Cheng L, Wang P (2000) Soil acid and alkaline phosphatase activity as pH adjustment indicators. Soil Biol Biochem 32:1915–1919CrossRefGoogle Scholar
  12. Drosos M, Piccolo A (2018) The molecular dynamics of soil humus as a function of tillage. Land Degrad Dev 29:1792–1805CrossRefGoogle Scholar
  13. Fierer N, Schimel JP, Holden PA (2003) Influence of drying–rewetting frequency on soil bacterial community structure. Microb Ecol 45:63–71CrossRefGoogle Scholar
  14. Gianfreda L, Rao M, Violante A (1991) Invertase (β-fructosidase): effects of montmorillonite, Al-hydroxide and Al(OH)-montmorillonite complex on activity and kinetic properties. Soil Biol Biochem 23:581–587CrossRefGoogle Scholar
  15. Gianfreda L, De Cristofaro A, Rao MA, Violante A (1995) Kinetic behavior of synthetic organo- and organo-mineral-urease complexes. Soil Sci Soc Am J 59:811–815CrossRefGoogle Scholar
  16. Goyal A, Ghosh B, Eveleigh D (1991) Characteristics of fungal cellulases. Bioresour Technol 36:37–50CrossRefGoogle Scholar
  17. Grover AK, Cushley RJ (1977) Studies on almond emulsion beta-D-glucosidase. II. Kinetic evidence for independent glucosidases and galactosidase sites. Biochim Biophys Acta 482:109–124CrossRefGoogle Scholar
  18. Grover AK, Macmurchie DD, Cushley RJ (1977) Studies on almond emulsion beta-D-glucosidase. I. Isolation and characterization of a bifunctional isozyme. Biochim Biophys Acta 482:98–108CrossRefGoogle Scholar
  19. Lammirato C, Miltner A, Wick LY, Kästner M (2010) Hydrolysis of cellobiose by b-glucosidase in the presence of soil minerals - interactions at solid-liquid interfaces and effects on enzyme activity levels. Soil Biol Biochem 42:2203–2210CrossRefGoogle Scholar
  20. Lawson SL, Antony R, Warren J, Withers SG (1998) Mechanistic consequences of replacing the active-site nucleophile Glu-358 in agrobacterium sp. β-glucosidase with a cysteine residue. Biochem J 330:203–209CrossRefGoogle Scholar
  21. Lehmann J, Kleber M (2015) The contentious nature of soil organic matter. Nature 528:60–68CrossRefGoogle Scholar
  22. Leprince F, Quiquampoix H (1996) Extracellular enzyme activity in soil: effect of pH and ionic strength on the interaction with montmorillonite of two acid phosphatases secreted by the ectomycorrhizal fungus Hebetomu cylindrospo rum. Eur J Soil Sci 47:511–522CrossRefGoogle Scholar
  23. Mazzei P, Piccolo A (2012) Quantitative evaluation of noncovalent interactions between glyphosate and dissolved humic substances by NMR spectroscopy. Environ Sci Technol 46:5939–5946CrossRefGoogle Scholar
  24. Mazzei P, Piccolo A (2013) Reduced activity of β-glucosidase resulting from host-guest interactions with dissolved fulvic acids as revealed by NMR spectroscopy. Eur J Soil Sci 64:508–515CrossRefGoogle Scholar
  25. Mazzei P, Piccolo A (2015) Interactions between natural organic matter and organic pollutants as revealed by NMR spectroscopy. Magn Reson Chem 53:667–678CrossRefGoogle Scholar
  26. Mazzei P, Oschkinat H, Piccolo A (2013) Reduced activity of alkaline phosphatase due to host–guest interactions with humic superstructures. Chemosphere 93:1972–1979CrossRefGoogle Scholar
  27. Morant AV, Jørgensen K, Jørgensen C, Paquette SM, Sánchez-Pérez R, Møller BL, Bak S (2008) β-Glucosidases as detonators of plant chemical defense. Phytochem 69:1795–1813CrossRefGoogle Scholar
  28. 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
  29. Nannipieri P, Kandeler E, Ruggiero P (2002) Enzyme activities and microbiological and biochemical processes in soil. In: Burns RG, Dick RP (eds) Enzymes in the environment. Activity, ecology and application. Marcel Dekker, Inc, New York, pp 1–33Google Scholar
  30. 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
  31. Nannipieri P, Trasar-Cepeda C, Dick RP (2018) Soil enzyme activity: a brief history and biochemistry as a basis for appropriate interpretations and meta-analysis. Biol Fertil Soils 54:11–19CrossRefGoogle Scholar
  32. Piccolo A (1996) Humus and soil conservation. In: Piccolo A (ed) Humic substances in terrestrial ecosystems. Elsevier, Amsterdam, pp 225–264CrossRefGoogle Scholar
  33. Piccolo A (2016) In memoriam of F. J. Stevenson and the question of humic substances. Chem Biol Technol Agric 3:23CrossRefGoogle Scholar
  34. Piccolo A, Spaccini R, Drosos M, Vinci G, Cozzolino V (2018) The molecular composition of humus carbon: recalcitrance and reactivity in soils. In: Garcia C, Nannipieri P, Hernandez T (eds) The future of soil carbon. Its Conservation and Formation. Elsevier, Amsterdam, pp 87–124CrossRefGoogle Scholar
  35. Quiquampoix H (1987a) A stepwise approach to the understanding of extracellular enzyme activity in soil. I. Effect of electrostatic interactions on the conformation of a beta-D-glucosidase adsorbed on different mineral surfaces. Biochimie 69:753–763CrossRefGoogle Scholar
  36. Quiquampoix H (1987b) A stepwise approach to the understanding of extracellular enzyme activity in soil II. Competitive effects on the adsorption of a beta-D-glucosidase in mixed mineral or organo-mineral systems. Biochimie 69:765–771CrossRefGoogle Scholar
  37. Quiquampoix H, Burns RG (2007) Interactions between proteins and soil mineral surfaces: environmental and health consequences. Elements 3:401–406CrossRefGoogle Scholar
  38. Quiquampoix H, Staunton S, Baron MH, Ratcliffe RG (1993) Interpretation of the pH dependence of protein adsorption on clay mineral surfaces and-its relevance to the understanding of extracellular enzyme activity in soil. Colloids Surf A Physicochem Eng Asp 75:85–93CrossRefGoogle Scholar
  39. Quiquampoix H, Abadie J, Baron MH, Leprince F, Matumoto-Pintro PT, Ratcliffe RG, Staunton S (1995) Mechanisms and consequences of protein adsorption on soil mineral surfaces. In: Horbett T, el a (eds) Proteins at interfaces II - ACS symposium series. American Chemical Society, Washington DC, pp 321–333CrossRefGoogle Scholar
  40. Quiquampoix H, Servagent-Noinville S, Baron MH (2002) Enzyme adsorption on soil mineral surfaces and consequences for the catalytic activity. In: Burns RG, Dick RP (eds) Enzymes in the environment: activity, ecology and applications. Marcel Dekker, New York, pp 285–306Google Scholar
  41. Rye CS, Withers SG (2000) Glycosidase mechanisms. Curr Opin Chem Biol 4:573–580CrossRefGoogle Scholar
  42. Saratchandra SU, Perrott KW (1984) Assay of β-glucosidase activity in soils. Soil Sci 138:15–19CrossRefGoogle Scholar
  43. Servagent-Noinville S, Revault M, Quiquampoix H, Baron MH (2000) Conformational changes of bovine serum albumin induced by adsorption on different clay surfaces: FTIR analysis. J Colloid Interface Sci 221:273–283CrossRefGoogle Scholar
  44. Shackle V, Freeman C, Reynolds B (2006) Exogenous enzyme supplements to promote treatment efficiency in constructed wetlands. Sci Total Environ 361:18–24CrossRefGoogle Scholar
  45. Schimel JP, Bennett J (2004) Nitrogen mineralization: Challenges of a changing paradigm. Ecology 85:591–602Google Scholar
  46. Sinsabaugh RL, Moorhead DL (1994) Resource allocation to extracellular enzyme production: a model for nitrogen and phosphorus control of litter decomposition. Soil Biol Biochem 26:1305–1311CrossRefGoogle Scholar
  47. Stotzky G (1986) Influence of soil mineral colloids and metabolic processes, growth adhesion, and ecology of microbes and viruses. In: Huang M, Schnitzer M (eds) Interactions of soil minerals and natural organics and nicrobes. Special publication, vol 17. Soil Science Society of America, Madison, pp 305–428Google Scholar
  48. Violante A, Arienzo M, Sannino F, Colombo C, Piccolo A, Gianfreda L (1999) Formation and characterization of OH-Al-humate-montmorillonite complexes. Org Geochem 30:461–468CrossRefGoogle Scholar
  49. Wells MJM, Stretz HA (2019) Supramolecular architectures of natural organic matter. Sci Total Environ 671:1125–1133CrossRefGoogle Scholar
  50. Xiang S, Doyle A, Holden PA, Schimel JP (2008) Drying and rewetting effects on C and N mineralization and microbial activity in surface and subsurface California grassland soils. Soil Biol Biochem 40:2281–2289CrossRefGoogle Scholar
  51. Xiao-Chang W, Qin L (2006) Beta-glucosidase activity in paddy soils of the Taihu Lake region, China. Pedosphere 16:118–124CrossRefGoogle Scholar
  52. Yan J, Pan G, Li L, Quan G, Ding C, Luo A (2010) Adsorption, immobilization, and activity of b-glucosidase on different soil colloids. J Colloid Interface Sci 348:565–570CrossRefGoogle Scholar
  53. Zornoza R, Guerrero C, Mataix-Solera J, Arcenegui V, Garcia-Orenes F, Mataix-Beneyto J (2006) Assessing air-drying and rewetting pre-treatment effect on some soil enzyme activities under Mediterranean conditions. Soil Biol Biochem 38:2125–2134Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Dipartimento di Farmacia (DIFARMA)Università di SalernoFiscianoItaly
  2. 2.Centro Interdipartimentale per la Risonanza Magnetica Nucleare per l’Ambiente, l’Agro-Alimentare ed i Nuovi Materiali (CERMANU)Università di Napoli Federico IIPorticiItaly
  3. 3.Dipartimento di AgrariaUniversità di Napoli Federico IIPorticiItaly

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