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Soil peroxidase regulates organic matter decomposition through improving the accessibility of reducing sugars and amino acids

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Abstract

Peroxidase activity can be an important soil property for predicting soil organic matter dynamics, but peroxidase control on organic matter degradation has not yet been fully understood. We hypothesized that peroxidase could enhance soil C and N mineralization via improving the bioavailability of reducing sugars and amino acids. First, an arable soil (~13 g dry weight equivalent) was amended with horseradish peroxidase at 0, 0.1, and 0.2 activity units g−1 soil, and then examined for peroxidase and hydrolase activities, water-extractable phenolic content, and soil C and N mineralization over a 21-day incubation. Soil C mineralization was enhanced by peroxidase addition, but it was not correlated with the concentration of water extractable phenolics or hydrolase activity. Exoglucanase and β-glucosidase activities were significantly lower in soil amended with peroxidase at 0.2 units than at 0.1 units. Second, peroxidase, cellulase, protease or their combinations were added into sterile soils to examine enzyme-catalyzed productions of soluble reducing sugars and amino acids. Reducing sugar concentration was increased after peroxidase addition and this effect was more pronounced when both peroxidase and hydrolases were added. Thus-produced reducing sugars and amino acids were significantly correlated with soil C and N mineralization (Pearson’s correlation coefficient, r = 0.65 and r = 0.63, P < 0.01), respectively. Our results indicated that the effects of peroxidase on organic matter degradation were not through the production of soluble phenolics or the enhancement of hydrolase activity. Instead, by oxidizing phenolics soil peroxidase liberated carbohydrates and proteins that were otherwise encapsulated in soil humus and thus inaccessible to soil hydrolases and microbes.

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References

  • Allison S (2006) Soil minerals and humic acids alter enzyme stability: implications for ecosystem processes. Biogeochemistry 81:361–373

    Article  CAS  Google Scholar 

  • Appel HM (1993) Phenolics in ecological interactions: the importance of oxidation. J Chem Ecol 19:1521–1552

    Article  CAS  PubMed  Google Scholar 

  • Bergbauer MS, Newell Y (1992) Contribution to lignocellulose degradation and DOC formation from a salt marsh macrophyte by the ascomycete Phaeosphaeria spartinicola. FEMS Microbiol Ecol 86:341–348

    Article  CAS  Google Scholar 

  • Blum U (1998) Effects of microbial utilization of phenolic acids and their phenolic breakdown products on allelopathic interactions. J Chem Ecol 24:685–708

    Article  CAS  Google Scholar 

  • Blum U, Shafer SR (1988) Microbial populations and phenolic-acids in soil. Soil Biol Biochem 20:793–800

    Article  CAS  Google Scholar 

  • Bugg TDH, Ahmad M, Hardiman E, Singh R (2011) The emerging role for bacteria in lignin degradation and bio-product formation. Curr Opin Biotechnol 22:394–400

    Article  CAS  PubMed  Google Scholar 

  • Burns RG (1982) Enzyme activity in soil: location and a possible role in microbial ecology. Soil Biol Biochem 14:42–427

    Article  Google Scholar 

  • Carreiro MM, Sinsabaugh RL, Repert DA, Parkhurst DF (2000) Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology 81:2359–2365

    Article  Google Scholar 

  • Ceccanti B, Doni S, Macci C, Cercignani G, Masciandaro G (2008) Characterization of stable humic–enzyme complexes of different soil ecosystem through analytical isoelectric focusing technique (IEF). Soil Biol Biochem 40:2174–2177

    Article  CAS  Google Scholar 

  • Dari K, Béchet M, Blondeau R (1995) Isolation of soil Streptomyces strains capable of degrading humic acids and analysis of their peroxidase activity. FEMS Microbiol Ecol 16:115–122

    Article  CAS  Google Scholar 

  • DeForest JL, Zak DR, Pregitzer KS, Burton AJ (2004) Anthropogenic NO3 − deposition alters microbial community function in northern hardwood forests. Soil Sci Soc Am J 68:132–138

    Article  CAS  Google Scholar 

  • DeForest JL, Zak DR, Pregitzer KS, Burton AJ (2005) Atmosphere nitrate deposition and enhanced dissolved organic carbon leaching: test of a potential mechanism. Soil Sci Soc Am J 69:1233–1237

    Article  CAS  Google Scholar 

  • Fan TWM, Lane AN, Chekmenev E, Wittebort RJ, Higashi RM (2004) Synthesis and physico-chemical properties of peptides in soil humic substances. J Peptide Res 63:253–264

    Article  CAS  Google Scholar 

  • Fenner N, Freeman C, Reynolds B (2005) Observations of a seasonally shifting thermal optimum in peatland carbon-cycling processes; implications for the global carbon cycle and soil enzyme methodologies. Soil Biol Biochem 37:1814–1821

    Article  CAS  Google Scholar 

  • Fierer N, Schimel JP, Cates RG, Zou J (2001) Influence of balsam poplar tannin fractions on carbon and nitrogen dynamics in Alaskan taiga floodplain soils. Soil Biol Biochem 33:1827–1839

    Article  CAS  Google Scholar 

  • Freeman C, Lock MA, Marxsen J, Jones SE (1990) Inhibitory effects of high molecular weight dissolved organic matter upon the metabolic processes in biofilms from contrasting rivers and streams. Freshw Biol 24:159–166

    Article  CAS  Google Scholar 

  • Freeman C, Ostle N, Kang H (2001) An enzymic ‘latch’ on a global carbon store. Nature 409:149

    Article  CAS  PubMed  Google Scholar 

  • Gianfreda L, Bollag JM (1996) Influence of natural and anthropogenic factors on enzyme activity in soil. In: Stotsky G, Bollag JM (eds) Soil biochemistry. Marcel Dekker, New York, pp 123–193

    Google Scholar 

  • Gramss G, Ziegenhagen D, Sorge S (1998) Degradation of soil humic extract by wood- and soil-associated fungi, bacteria, and commercial enzymes. Microb Ecol 37:140–151

    Article  Google Scholar 

  • Gramss G, Voigt KD, Kirsche B (1999) Oxidoreductase enzymes liberated by plant roots and their effects on soil humic material. Chemosphere 38:1481–1494

    Article  CAS  Google Scholar 

  • Haslam E (1998) Practical polyphenolics – from structure to molecular recognition and physiological action. Cambridge University Press, Cambridge

    Google Scholar 

  • Hayes MHB, Malcolm RL (2001) Considerations of the compositions and aspects of the structures of humic substances. In: Clapp CE, Hayes MHB, Senesi N, Bloom PR, Jardine PM (eds) Humic substances and chemical contaminants. Soil Science Society of America, Madison, WI, pp 3–39

    Google Scholar 

  • Hofman J, Dušek L (2003) Biochemical analysis of soil organic matter and microbial biomass composition – a pilot study. Eur J Soil Biol 39:217–224

    Article  CAS  Google Scholar 

  • Howard RL, Abotsi E, van Rensburg JEL, Howard S (2003) Lignocellulose biotechnology: issues of bioconversion and enzyme production. Afr J Biotechnol 2:602–619

    CAS  Google Scholar 

  • Joanisse GD, Bradley RL, Preston CM, Munson AD (2007) Soil enzyme inhibition by condensed litter tannins may drive ecosystem structure and processes: the case of Kalmia angustifolia. New Phytol 175:535–546

    Article  CAS  PubMed  Google Scholar 

  • Johnsen AR, Jacobsen OS (2008) A quick and sensitive method for the quantification of peroxidase activity of organic surface soil from forests. Soil Biol Biochem 40:814–821

    Article  CAS  Google Scholar 

  • Knicker H, Hatcher PG (1997) Survival of protein in an organic-rich sediment: possible protection by encapsulation in organic matter. Naturwissenschaften 84:231–234

    Article  CAS  Google Scholar 

  • Krull E, Baldock J, Skjemstad J (2001) Soil texture effects on decomposition and soil carbon storage. Net Ecosystem Exchange CRC Workshop Proceedings, pp 103–110.

  • Kurek B, Monties B (1994) Oxidation of spruce lignin by fungal lignin peroxidase and horseradish peroxidase: comparison of their actions on molecular structure of the polymer in colloidal solution. Enzyme Microb Technol 16:125–130

    Article  CAS  Google Scholar 

  • Ladd JN, Butler JHA (1972) Short-term assays of soil proteolytic enzyme activities using proteins and dipeptide derivatives as substrates. Soil Biol Biochem 4:19–30

    Article  CAS  Google Scholar 

  • Lichtfouse E, Wehrung P, Albrecht P (1998) Plant wax n-alkanes trapped in soil humin by noncovalent bonds. Naturwissenschaften 85:449–452

    Article  CAS  Google Scholar 

  • Mangler JE, Tate RL (1982) Source and role of peroxidase in soil organic matter oxidation in Pahokee muck. Soil Sci 134:226–232

    Article  CAS  Google Scholar 

  • Mercer DK, Iqbal M, Miller PGG, McCarthy AJ (1996) Screening actinomycetes for extracellular peroxidase activity. Appl Environ Microb 62:2186–2190

    CAS  Google Scholar 

  • Nadeau JA, Qualls RG, Nowak RS, Blank RR (2007) The potential bioavailability of organic C, N, and P through enzyme hydrolysis in soils of the Mojave Desert. Biogeochemistry 82:305–320

    Article  CAS  Google Scholar 

  • 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 48:743–762

    Article  Google Scholar 

  • Piccolo A (2001) The supramolecular structure of humic substances. Soil Sci 166:810–832

    Article  CAS  Google Scholar 

  • Ramachandra M, Crawford DL, Hertel G (1988) Characterization of an extracellular lignin peroxidase of the lignocellulytic actinomycete Streptomyces viridosporus. Appl Environ Microb 54:3057–3063

    CAS  Google Scholar 

  • Renella G, Landi L, Nannipieri P (2002) Hydrolase activities during and after the chloroform fumigation of soil as affected by protease activity. Soil Biol Biochem 34:51–60

    Article  CAS  Google Scholar 

  • Rezáčová V, Baldrian P, Hrselová H, Larsen J, Gryndler M (2007) Influence of mineral and organic fertilization on soil fungi, enzyme activities and humic substances in a long-term field experiment. Folia Microbiol 52:415–422

    Article  Google Scholar 

  • Rosas A, de la Luz MM, Jara AA, López R, Rao MA, Gianfreda L (2008) Catalytic behaviour of acid phosphatase immobilized on natural supports in the presence of manganese or molybdenum. Geoderma 145:77–83

    Article  CAS  Google Scholar 

  • Ruggeiro P, Radogna VM (1988) Humic acids–tyrosinase interactions as a model of soil humic–enzyme complexes. Soil Biol Biochem 20:353–359

    Article  Google Scholar 

  • Saiya-Cork KR, Sinsabaugh RL, Zak DR (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34:1309–1315

    Article  CAS  Google Scholar 

  • Sánchez C (2009) Lignocellulosic residues: biodegradation and bioconversion by fungi. Biotechnol Adv 27:185–194

    Article  PubMed  Google Scholar 

  • Sinsabaugh RL (2010) Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol Biochem 42:391–404

    Article  CAS  Google Scholar 

  • Sinsabaugh RL, Antibus RK, Linkins AE, McClaugherty CA, Rayburn L, Repert D, Weiland T (1992) Wood decomposition over a first-order watershed: mass loss as a function of lignocellulase activity. Soil Biol Biochem 24:743–749

    Article  CAS  Google Scholar 

  • Sinsabaugh RL, Gallo ME, Lauber C, Waldrop MP, Zak DR (2005) Extracellular enzyme activities and soil organic matter dynamics for northern hardwood forests receiving simulated nitrogen deposition. Biogeochemistry 75:201–215

    Article  CAS  Google Scholar 

  • Sinsabaugh RL, Laube CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw CL, Contosta AR, Cusack D, Frey S, Gallo ME, Gartner TB, Hobbie SE, Holland K, Keeler BL, Powers JS, Stursova M, Takacs-Vesbach C, Waldrop M, Wallenstein M, Zak DR, Zeglin LH (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264

    PubMed  Google Scholar 

  • Souto XC, Chiapusio G, Pellissier F (2000) Relationships between phenolics and soil microorganisms in spruce forests: significance for natural regeneration. J Chem Ecol 26:2025–2034

    Article  CAS  Google Scholar 

  • Sparling GP, Ord BG, Vaughan D (1981) Changes in microbial biomass and activity in soils amended with phenolic acids. Soil Biol Biochem 13:455–460

    Article  CAS  Google Scholar 

  • Stevenson FJ (1982) Humus chemistry: genesis, composition, reactions. Wiley-Interscience, New York

    Google Scholar 

  • Tian L, Dell E, Shi W (2010) Chemical composition of dissolved organic matter in agroecosystems: correlations with soil enzyme activity and carbon and nitrogen mineralization. Appl Soil Ecol 46:426–435

    Article  Google Scholar 

  • Wagner GH, Wolf DC (1998) Carbon transformations and soil organic matter formation. In: Sylvia DM, Fuhrmann JJ, Hartel PG, Zuberer DA (eds) Principles and applications of soil microbiology. Prentice-Hall, Upper Saddle River, NJ, pp 218–258

    Google Scholar 

  • Waldrop MP, Firestone MK (2004) Altered utilization patterns of young and old soil C by microorganisms caused by temperature shifts and N additions. Biogeochemistry 67:235–248

    Article  CAS  Google Scholar 

  • Wang Z, Crawford DL, Magnuson TS, Bleakley BH, Hertel G (1990) Effects of bacterial lignin peroxidase on organic carbon mineralization in soil using recombinant Strepomyces strains. Can J Microbiol 37:287–294

    Article  Google Scholar 

  • Wershaw RL (1999) Molecular aggregation of humic substances. Soil Sci 164:803–811

    Article  CAS  Google Scholar 

  • Wetzel RG (1992) Gradient dominated ecosystems: sources and regulatory functions of dissolved organic matter in freshwater ecosystems. Hydrobiologia 229:181–198

    Article  CAS  Google Scholar 

  • Wong DWS (2009) Structure and action mechanism of ligninolytic enzymes. Appl Biochem Biotechnol 157:174–209

    Article  CAS  PubMed  Google Scholar 

  • Zámocký M, Obinger C (2010) Molecular phylogeny of heme peroxidases. In: Torres E, Ayala M (eds) Biocatalysis based on heme peroxidase. Springer-Verlag, Berlin, pp 7–35

    Chapter  Google Scholar 

  • Zang X, van Heemst JDH, Dria KJ, Hatcher PG (2000) Encapsulation of protein in humic acid from a histosol as an explanation for the occurrence of organic nitrogen in soil and sediment. Org Geochem 31:679–695

    Article  CAS  Google Scholar 

  • Zsolnay A (2003) Dissolved organic matter (DOM): artefacts, definitions, and functions. Geoderma 113:187–209

    Article  CAS  Google Scholar 

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Acknowledgements

We thank Ms. Emily Dell, Ms. Melissa Bell and Dr. Jianjun Dai for helping in soil collection and preparation, and the NCSU Environmental and Agricultural Testing Service laboratory for total soil C and N analyses. This study was financially supported by the USDA-SSARE grant and the North Carolina Agricultural Research Services.

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  1. Department of Soil Science, North Carolina State University, Raleigh, NC, 27695, USA

    Lei Tian & Wei Shi

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  1. Lei Tian
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Correspondence to Wei Shi.

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Tian, L., Shi, W. Soil peroxidase regulates organic matter decomposition through improving the accessibility of reducing sugars and amino acids. Biol Fertil Soils 50, 785–794 (2014). https://doi.org/10.1007/s00374-014-0903-1

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