Skip to main content

Advertisement

SpringerLink
Log in

Role of proteins in soil carbon and nitrogen storage: controls on persistence

  • Original Paper
  • Published:
Biogeochemistry Aims and scope Submit manuscript

Abstract

Mechanisms of soil organic carbon (C) and nitrogen (N) stabilization are of great interest, due to the potential for increased CO2 release from soil organic matter (SOM) to the atmosphere as a result of global warming, and because of the critical role of soil organic N in controlling plant productivity. Soil proteins are recognized increasingly as playing major roles in stabilization and destabilization of soil organic C and N. Two categories of proteins are proposed: detrital proteins that are released upon cell death and functional proteins that are actively released into the soil to fulfill specific functions. The latter include microbial surface-active proteins (e.g., hydrophobins, chaplins, SC15, glomalin), many of which have structures that promote their persistence in the soil, and extracellular enzymes, responsible for many decomposition and nutrient cycling transformations. Here we review information on the nature of soil proteins, particularly those of microbial origin, and on the factors that control protein persistence and turnover in the soil. We discuss first the intrinsic properties of the protein molecule that affect its stability, next possible extrinsic stabilizing influences that arise as the proteins interact with other soil constituents, and lastly controls on accessibility of proteins at coarser spatial scales involving microbial cells, clay particles, and soil aggregates. We conclude that research at the interface between soil science and microbial physiology will yield rapid advances in our understanding of soil proteins. We suggest as research priorities determining the relative abundance and turnover time (age) of microbial versus plant proteins and of functional microbial proteins, including surface-active compounds.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Alexandrescu AT (2005) Amyloid accomplices and enforcers. Protein Sci 14:1–12

    Google Scholar 

  • Anderson PA (1985) Interactions between proteins and constituents that affect protein quality. In: Finley GW, Hopkins DT (eds) Digestibility and amino acid availability in cereals and oilseeds. Am. Assoc. Cerea.l Chem., St Paul, pp 31–46

  • Amelung W, Zhang X, Flach KW (2006) Amino acids in grassland soils: climatic effects on concentrations and chirality. Geoderma 130:207–217

    Google Scholar 

  • Angers DA, Recous S, Aita C (1997) Fate of carbon and nitrogen in water-stable aggregates during decomposition of 13C15N-labelled wheat straw in situ. Eur J Soil Sci 48:295–300

    Google Scholar 

  • Arfaioli P, Pantani OL, Bosseto M, Ristori GG (1999) Influence of clay minerals and exchangeable cations on the formation of humic-like substances (melanoidins) from d-glucose and l-tyrosine. Clay Minerals 34:487–497

    Google Scholar 

  • Basaraba J, Starkey RL (1966) Effects of plant tannins on decomposition of organic substances. Soil Sci 101:17–23

    Google Scholar 

  • Bashan Y, Levanony H (1988) Active attachment of Azospirillum-brasilense Cd to quartz sand and to a light-textured soil by protein bridging. J Gen Microbiol 134:2269–2279

    Google Scholar 

  • Benoit RE, Starkey RL, Basaraba J (1968) Effect of purified plant tannins on decomposition of some organic compounds and plant materials. Soil Sci 105:153–158

    Google Scholar 

  • Bernard BA, Newton SA, Olden K (1983) Effect of size and location of the oligosaccharide chain on protease degradation of bovine pancreatic ribonuclease. J Biol Chem 258:12198–12202

    Google Scholar 

  • Blackwood CB, Dell CJ, Smucker AJM, Paul EA (2006) Eubacterial communities in different soil macroaggregate environments and cropping systems. Soil Biol Biochem 38:720–728

    Google Scholar 

  • Blum U, Rice EL (1969) Inhibition of symbiotic nitrogen-fixation by gallic and tannic acid, and possible roles in old-field succession. Bull Torrey Bot Club 96:531–544

    Google Scholar 

  • Böckelmann U, Szewzyk U, Grohmann E (2003) A new enzymatic method for the detachment of particle associated soil bacteria. J Microb Meth 55:201–211

    Google Scholar 

  • Bosetto M, Arfaioli P, Pantani OL (2002) Study of the Maillard reaction products formed by glycine and d-glucose on different mineral substrates. Clay Minerals 37:195–204

    Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for quantification of microgram quantities of protein utilizing the principle of protein-dye-binding. Anal Biochem 72:248–254

    Google Scholar 

  • Bradley R, Titus BD, Preston CM (2000) Changes to mineral N cycling and microbial communities in black spruce humus after addition of (NH4)2SO4 and condensed tannins extracted from Kalmia augustifolia and balsam fir. Soil Biol Biochem 32:1227–1240

    Google Scholar 

  • Bremner JM (1965) Organic forms of nitrogen. Agronomy 9:1238–1255

    Google Scholar 

  • Brewer R (1964) Fabric and mineral analysis of soils. Wiley, NY

    Google Scholar 

  • Brisou JF (1995) Biofilms, methods for enzymatic release of microorganisms. CRC Press. Boca Raton, FL

    Google Scholar 

  • Burdon J (2001) Are the traditional concepts of the structures of humic substances realistic? Soil Sci 166:752–769

    Google Scholar 

  • Burns RG (1978) Soil enzymes. Academic Press, New York

    Google Scholar 

  • Burns RG, Dick RP (2002) Enzymes in the environment: activity, ecology, and applications. Marcel Dekker, New York

    Google Scholar 

  • Busto MD, Perez-Mateos M (1995) Extraction of humic-β-glucosidase fractions from soils. Biol Fertil Soils 20:77–82

    Google Scholar 

  • Butko P, Buford JP, Goodwin JS, Stroud PA, McCormick CL, Cannon GC (2001) Spectroscopic evidence for amyloid-like interfacial self-assembly of hydrophobin SC3. Biochem Biophys Res Commun 280:212–215

    Google Scholar 

  • Butler MJ, Day AW (1998) Fungal melanins: a review. Can J Microbiol 44:1115–1136

    Google Scholar 

  • Caldwell BA (2005) Enzyme activities as a component of soil biodiversity: a review. Pedobiologia 49:637–644

    Google Scholar 

  • Carpenter CE, Mueller RJ, Kazmierczak P, Zhang L, Villalon DK, van Alfen NK (1992) Effect of a virus on accumulation of a tissue specific cell surface protein of the fungus Cryphonectria (Endothia) parasitica. Mol Plant-Microbe Interact 4:55–61

    Google Scholar 

  • Chenu C, Stotzky G (2002) Interactions between microorganisms and soil particles: an overview. In: Huang PM, Bollag JM, Senesi N (eds) interactions between soil particles and microorganisms. John Wiley and Sons, Chichester, UK, pp 3–40

    Google Scholar 

  • Cheryan M (1980) Phytic acid interactions in food systems. Crit Rev Food Sci Nutr 13:297–335

    Article  Google Scholar 

  • Christensen BT (1992) Physical fractionation of soil and organic matter in primary particle size and density separates. Adv Soil Sci 20:1–90

    Google Scholar 

  • Claessen D (2004) Structural proteins involved in morphological differentiation of streptomycetes. Thesis (Microbiology, University of Groningen, The Netherlands

  • Claessen D, Rink R, de Jong W, Siebring J, de Vreugd P, Boersma FGH, Dijkhuizen L, Wösten HAB (2003) A novel class of secreted hydrophobic proteins is involved in aerial hyphae formation in Streptomyces coelicolor by forming amyloid-like fibrils. Genes Dev 17:1714–1726

    Google Scholar 

  • Claessen D, Stokroos I, Deelstra HJ, Penninga NA, Bormann C, Salas JA, Dijkhuizen L, Wösten HAB (2004) The formation of the rodlet layer of streptomycetes is the result of the interplay between rodlins and chaplins. Mol Microbiol 53:433–443

    Google Scholar 

  • Coelho RR, Linares LF, Martin JP (1985) Amino acid distribution in some fungal melanins and of soil humic acids from Brazil. Plant Soil 87:337–346

    Google Scholar 

  • Corvis Y, Walcarius A, Rink R, Mrabet NT, Rogalska E (2005) Preparing catalytic surfaces for sensing applications by immobilizing enzymes via hydrophobin layers. Anal Chem 77:1622–1630

    Google Scholar 

  • Cosgrove DJ (1966) The chemistry and biochemistry of inositol polyphosphates. Rev Pure Appl Chem 16:209–224

    Google Scholar 

  • Dalal RC (1977) Soil organic phosphorus. Adv Agron 29:85–117

    Google Scholar 

  • de Gryze S, Six J, Brits C, Merckx R (2005) A quantification of short-term macro-aggregate dynamics: influences of wheat residue input and texture. Soil Biol Biochem 37:55–66

    Google Scholar 

  • de Jong JF (2006) Aerial hyphae of Schizophyllum commune: their function and formation. Thesis, University of Utrecht

  • de Vocht ML, Reviakine I, Ulrich WP, Bergsma-Schutter W, Wösten HAB, Vogel H, Brisson A, Wessels JGH, Robillard GT (2002) Self-assembly of the hydrophobin SC3 proceeds via two structural intermediates. Prot Sci 11:1199–1205

    Google Scholar 

  • de Vries OMH, Fekkes MP, Wösten HAB, Wessels JGH (1993) Insoluble hydrophobin complexes in the walls of Schizophyllum commune and other filamentous fungi. Arch Microbiol 159:330–335

    Google Scholar 

  • Díaz-Zorita M, Perfect E, Grove JH (2002) Disruptive methods for assessing soil structure. Soil Tillage Res 64:3–22

    Google Scholar 

  • Dobson CM (1999) Protein misfolding, evolution and disease. Trend Biochem Sci 24:329–332

    Google Scholar 

  • Dormaar JF, Smoliak S, Willms WD (1990) Soil chemical properties during succession from abandoned cropland to native range. J Range Manag 43:260–265

    Google Scholar 

  • Driver JD, Holben WE, Rillig MC (2005) Characterization of glomalin as a hyphal wall component of arbuscular mycorrhizal fungi. Soil Biol Biochem 37:101–106

    Google Scholar 

  • Elliott ET, Coleman DC (1988) Let the soil work for us. Ecol Bull 39:23–32

    Google Scholar 

  • Elliot MA, Karoonuthaisiri N, Huang J, Bibb MJ, Cohen SN, Kao CM, Buttner MJ (2003) The chaplins: a family of hydrophobic cell-surface proteins involved in aerial mycelium formation in Streptomyces coelicolor. Genes Dev 17:1727–1740

    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

    Google Scholar 

  • Friedel JK, Scheller E (2002) Composition of hydrolysable amino acids in soilk organic matter and soil microbial biomass. Soil Biol Biochem 34:315–325

    Google Scholar 

  • Friedenauer S, Berlet HH (1989) Sensitivity and variability of the Bradford protein assay in the presence of detergents. Anal Biochem 178:263–268

    Google Scholar 

  • Gadkar V, Rillig MC (2006) The arbuscular mycorrhizal fungal protein glomalin is a putative homolog of heat shock protein 60. FEMS Microbiol Lett 263:93–101

    Google Scholar 

  • Gallet C, Lebreton P (1995) Evolution of phenolic patterns and associated litters and humus of a mountain forest ecosystem. Soil Biol Biochem 27:157–165

    Google Scholar 

  • Gebbink MFBG, Claessen D, Bouma B, Dijkhuizen L, Wösten HAB (2005) Amyloids – a functional coat for microorganisms. Nat Rev Microbiol 3:333–341

    Google Scholar 

  • Gil H, Mata-Segreda JF, Schowen RL (1991) Effect of non-enzymatic glycosylation on reactivity in proteolysis [in Spanish] Acta Cient Venez 42:16–23

    Google Scholar 

  • Grossman RB, Lynn WC (1967) Gel-like films that may form at the air-water interface in soils. Soil Sci Soc Am Proc 31:259–262

    Article  Google Scholar 

  • Hagerman AE, Rice ME, Ritchard NT (1998) Mechanisms of protein precipitation for two tannins, pentagalloyl glucose and epicatechin16 (4→ 8) catechin (procyanidin). J Agric Food Chem 46:2590–2595

    Google Scholar 

  • Hagerman AE, Robbins CT (1987) Implication of soluble tannin–protein complexes for tannin analysis and plant defense mechanisms. J Chem Ecol 13:1243–1258

    Google Scholar 

  • Harner MJ, Ramsey PW, Rillig MC (2004) Protein accumulation and distribution in floodplain soils and river foam. Ecol Lett 7:829–836

    Google Scholar 

  • Harris P (1972) Micro-organisms in surface films from soil crumbs. Soil Biol Biochem 4:105–106

    Google Scholar 

  • Haslam E (1989) Plant polyphenols: vegetable tannins revisited. Cambridge University Press, 230 pp

  • Hättenschwiler S, Vitousek P (2000) The role of polyphenols in terrestrial ecosystem nutrient cycling. Trends Ecol Evol 15:238–243

    Google Scholar 

  • Horner JD, Gosz JR, Cates RG (1988) The role of carbon-based plant secondary metabolites in decomposition in terrestrial ecosystems. Am Nat 132:869–883

    Google Scholar 

  • Howard PJA, Howard DM (1993) Ammonification of complexes prepared from gelatin and aqueous extracts of leaves and freshly-fallen litter of trees on different soil types. Soil Biol Biochem 25:1249–1256

    Google Scholar 

  • Ho JGS, Kitov PI, Paszkiewicz E, Sadowska J, Bundlet DR, Ng KK-S (2005) Ligand-assisted aggregation of proteins. J Biol Chem 280:31999–32008

    Google Scholar 

  • Hu P-H, Hatcher PG (2003) New evidence for covalent coupling of peptides to humic acids based on 2D NMR spectroscopy: a means for preservation. Geochim Cosmochim Acta 69:4521–4533

    Google Scholar 

  • Ikan R (1996) The Maillard reaction. Consequences for the chemical and life sciences. John Wiley & Sons, Chichester, UK

    Google Scholar 

  • Jahnel JB, Frimmel FH (1995) Enzymatic release of amino acids from different humic substances. Acta Hydrochim Hydrobiol 23:31–35

    Google Scholar 

  • Jakas A, Horvat \({\hat{\hbox{S}}}\) (2004) The effect of glycation on the chemical and enzymatic stability of the endogenous opioid peptide, leucine-enkephalin, and related fragments. Bioorg Chem 32:516–526

    Google Scholar 

  • Janssen MI, van Leeuwen MBM, Scholtmeijer K, van Kooten TG, Dijkhuizen L, Wösten HAB (2002) Coating with genetic engineered hydrophobin promotes growth of fibroblasts on a hydrophobic solid. Biomaterials 23:4847–4854

    Google Scholar 

  • Janssen MI, van Leeuwen MBM, van Kooten TG, de Vries J, Dijkhuizen L and Wösten HAB (2004) Promotion of cell activity by coating with hydrophobin in the β-sheet end state. Biomaterials 25:2731–2739

    Google Scholar 

  • Jastrow JD (1996) Soil aggregate formation and the accrual of particulate and mineral-associated organic matter. Soil Biol Biochem 28:665–676

    Google Scholar 

  • Jokic A, Frenkel AI, Vairavamurthy MA, Huang PM (2001) Birnssite catalysis of the Maillard reaction: its significance in natural humification. Geophys Res Lett 28:3899–3902

    Google Scholar 

  • Jokic A, Wang MC, Liu C, Frenkel AI, Huang PM (2004) Integration of the polyphenol and Maillard reactions into a unified abiotic pathway for humification in nature: the role of δ-MnO2. Org Geochem 35:747–762

    Google Scholar 

  • Keeney DR, Bremner JM (1964) Effect of cultivation on the nitrogen distribution in soils. Soil Sci Soc Am Proc 28:653–656

    Article  Google Scholar 

  • Kleber M, Sollins P, Sutton R (2006) A conceptual model of organo-mineral interactions in soils: self assembly of organic molecular fragments into zonal structures on mineral surfaces. Biogeochemistry (this volume)

  • Knicker H (2006) Vegetation fires and burnings; how do they affect the nature and stability of soil organic nitrogen and carbon? – A review. Biogeochemistry (this volume)

  • Knicker H (2000) Biogenic Nitrogen in soils as revealed by solid-state Carbon-13 and Nitrogen-15 Nuclear Magnetic Resonance spectroscopy. J Environ Qual 29:715–723

    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

    Google Scholar 

  • Knicker H, Schmidt MWI, Kögel-Knabner I (2000) Nature of organic nitrogen in fine particle separates of sandy soils in highly industrialized area as revealed by NMR spectroscopy. Soil Biol Biochem 32:241–252

    Google Scholar 

  • Kojima RT (1947) Soil organic nitrogen: I. Nature of the organic nitrogen in a muck soil from Geneva, New York. Soil Sci 64:157–165

    Google Scholar 

  • Kranabetter JM, Banner A (2000) Selected biological and chemical properties of forest floors across bedrock types on the northern coast of British Columbia. Can J For Res 30:971–981

    Google Scholar 

  • Kraus TEC, Dahlgren RA, Zasoski RJ (2003a) Tannins in nutrient dynamics of forest ecosystems: a review. Plant Soil 256:41–66

    Google Scholar 

  • Kraus TEC, Yu Z, Preston CM, Dahlgren RA, Zasoski RJ (2003b) Linking chemical reactivity and protein precipitation to structural characteristics of foliar tannins. J Chem Ecol 29:703–730

    Google Scholar 

  • Kuiters AT, Denneman CAJ (1987) Water-soluble phenolic substances in soils under several coniferous and deciduous tree species. Soil Biol Biochem 19:765–769

    Google Scholar 

  • Kuo M-J, Alexander M (1967) Inhibition of the lysis of fungi by melanins. J Bacteriol 94:624–629

    Google Scholar 

  • Ladd JN, Brisbane PG (1967) Release of amino acids from soil humic acids by proteolytic enzymes. Aust J Soil Res 5:161–171

    Google Scholar 

  • Leinweber P, Schulten H-R (2000) Nonhydrolyzable forms of soil organic nitrogen: extractability and composition. J Plant Nutr Soil Sci 163:433–439

    Google Scholar 

  • Lewis JA, Starkey RL (1968) Vegetable tannins, their decomposition and effects on decomposition of some organic compounds. Soil Sci 106:241–247

    Google Scholar 

  • Linder M, Szilvay GR, Nakari-Setälä T, Söderlund H, Penttilä M (2002) Surface adhesion of fusion proteins containing the hydrophobins HFBI and HFBII from Trichoderma reesei. Protein Sci 11:2257–2266

    Google Scholar 

  • Lipson DA, Schmidt SK, Monson RK (1999) Links between microbial population dynamics and nitrogen availability in an alpine ecosystem. Ecology 80:1623–1631

    Google Scholar 

  • Lockwood JL (1960) Lysis of mycelia of plant pathogenic fungi by natural soil. Phytopathology 50:787–789

    Google Scholar 

  • Loll MJ, Bollag J-M (1983) Protein transformation in soil. Adv Agron 36:351–382

    Google Scholar 

  • Loomis WD, Battaile J (1966) Plant phenolic compounds and the isolation of plant enzymes. Phytochemistry 5:423–438

    Google Scholar 

  • Lorenz K, Preston CM (2002) Characterization of high-tannin fractions from humus by carbon-13 cross-polarization and magic angle spinning nuclear magnetic resonance. J Environ Qual 31:431–436

    Google Scholar 

  • Lorenz K, Preston CM, Raspe S, Morrison IK, Feger KH (2000) Litter composition and humus characteristics in Canadian and German spruce ecosystems: information from tannin analysis and 13C CPMAS NMR. Soil Biol Biochem 32:779–792

    Google Scholar 

  • Lovelock CE, Wright SF, Clark DA, Reuss RW (2004) Soil stocks of glomalin produced by arbuscular mycorrhizal fungi across a tropical rain forest landscape. J Ecol 92:278–287

    Google Scholar 

  • Lugones LG, Bosscher JS, Scholtmeijer K, de Vries OMH, Wessels JGH (1996) An abundant hydrophobin (ABH1) forms hydrophobic rodlet layers in Agaricus bisporus fruiting bodies. Microbiology 142:1321–1329

    Google Scholar 

  • Lugones LG, Wösten HAB, Wessels JGH (1998) A hydrophobin (ABH3) specifically secreted by vegetatively growing hyphae of Agaricus bisporus (common white button mushroom). Microbiology 144:2345–2353

    Article  Google Scholar 

  • Lugones LG, Wösten HAB, Birkenkamp KU, Sjollema KA, Zagers J, Wessels JGH (1999) Hydrophobins line air channels in fruiting bodies of Schizophyllum commune and Agaricus bisporus. Mycol Res 103:635–640

    Google Scholar 

  • Lugones LG, de Jong JF, de Vries OMH, Jalving R, Dijksterhuis J, Wösten HAB (2004) The SC15 protein of Schizophyllum commune mediates formation of aerial hyphae and attachment in the absence of the SC3 hydrophobin. Mol Microbiol 53:707–716

    Google Scholar 

  • Lutgen ER, Clairmont DL, Graham J, Rillig MC (2003) Seasonality of arbuscular mycorrhizal hyphae and glomalin in a western Montana grassland. Plant Soil 257:71–83

    Google Scholar 

  • Martens DA, Reedy TE, Lewis DT (2003) Soil organic carbon content and composition of 130-year crop, pasture and forest land-use managements. Global Change Biol 10:65–78

    Google Scholar 

  • Martens DA, Loeffelmann KL (2003) Soil amino acid composition quantified by acid hydrolysis and anion-chromatography-pulsed amperometry. J Agric Food Chem 51:6521–6529

    Google Scholar 

  • Martin JP, Parsa AA, Haider K (1978) Influence of intimate association with humic polymers on biodegradation of [14C]labeled organic substrates in soil. Soil Biol Biochem 10:483–486

    Google Scholar 

  • Matsumoto S, Ae N, Yamagata M (2000) Extraction of mineralizable organic nitrogen from soils by a neutral phosphate buffer solution. Soil Biol Biochem 32:1293–1299

    Google Scholar 

  • McManus JP, Davis KG, Lilley TH, Haslam E (1981) The association of proteins with polyphenols. J Chem Soc Commun 309–311

  • Merlini G, Belloti V (2003) Molecular mechanisms of amyloidosis. N Engl J Med 349:583–596

    Google Scholar 

  • Miltner A, Zech W (1999) Microbial degradation and resynthesis of protein during incubation of beech leaf litter in the presence of mineral phases. Biol Fertil Soils 30:48–51

    Google Scholar 

  • Mummey DL, Holben W, Six J, Stahl P (2006) Spatial stratification of soil bacterial populations in aggregates of diverse soils. Microb Ecol 51:404–411

    Google Scholar 

  • Nakas JP, Klein DA (1979) Decomposition of microbial cell components in a semi-arid grassland soil. Appl Environ Microbiol 38:454–460

    Google Scholar 

  • Németh K, Bartels H, Vogel M, Mengel K (1988) Organic nitrogen compounds extracted from arable and forest soils by electro-ultrafiltration and recovery rates of amino acids. Biol Fertil Soils 5:271–275

    Google Scholar 

  • Nierop KGJ, Verstaten JM, Tietma A, Westervald JW, Wartenbergh PE (2006) Short- and long-term tannin induced carbon, nitrogen and phosphorus dynamics in Corsican pine litter. Biogeochemistry 79:275–296

    Google Scholar 

  • Northup RR, Yu Z, Dahlgren RA, Vogt KA (1995) Polyphenol control of nitrogen release from pine litter. Nature 377: 227–229

    Google Scholar 

  • Northup RR, Dahlgren DA, McColl JG (1998) Polyphenols as regulators of plant–litter–soil interactions in northern California’s pygmy forest: A positive feedback? Biogeochemistry 42:189–220

    Google Scholar 

  • Nyman BF (1985) Protein-proanthocyanidin interactions during extraction of Scots pine needles. Phytochemistry 24:2939–2944

    Google Scholar 

  • Oades JM (1984) Soil organic matter and structural stability: mechanisms and implications for management. Plant Soil 76:319–337

    Google Scholar 

  • Oh HI, Hoff JE, Armstrong GS, Haff LA (1980) Hydrophobic interactions in tannin–protein complexes. J Agric Food Chem 28:394–398

    Google Scholar 

  • Omoike A, Chorover J (2004) Spectroscopic study of extracellular polymeric substances from Bacillus subtilis: aqueous chemistry and adsorption effects. Biomacromolecules 5:1219–1230

    Google Scholar 

  • Opdenakker G, Rudd PM, Ponting CP, Dwek RA (1993) Concepts and principles pf glycobiology. FASEB J 7:1330–1337

    Google Scholar 

  • Parsek MR, Fuqua C (2004) Biofilms 2003: emerging themes and challenges in studies of surface-associated microbial life. J Bacteriol 186:4427–4440

    Google Scholar 

  • Paul EA, Clark FE (1996) Soil microbiology and biochemistry, 2nd edn. Academic Press, Orlando

    Google Scholar 

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

    Google Scholar 

  • Plante A, McGill W (2002) Soil aggregate dynamics and the retention of organic matter in laboratory-incubated soil with differing simulated tillage frequencies. Soil Tillage Res 66:79–92

    Google Scholar 

  • Plante AF, Feng Y, McGill WB (2002) A modeling approach to quantifying soil macroaggregate dynamics. Can J Soil Sci 82:181–190

    Google Scholar 

  • Raab TK, Lipson DA, Monson RK (1999) Soil amino acid utilization among species of the Cyperaceae: plant and soil processes. Ecology 80:2408–2419

    Article  Google Scholar 

  • Ravindran V, Bryden WL, Kornegay ET (1995) Phytates: occurrence, bioavailability and implications in poultry nutrition. Poult Avian Bio Rev 6:125–143

    Google Scholar 

  • Rice EL, Pancholy SK (1973) Inhibition of nitrification by climax ecosystems II Additional evidence and possible role of tannins. Am J Bot 60:691–702

    Google Scholar 

  • Rillig MC (2004) Arbuscular mycorrhizae, glomalin and soil quality. Can J Soil Sci 84:355–363

    Google Scholar 

  • Rillig MC (2005) A connection between fungal hydrophobins and soil water repellency. Pedobiologia 49:395–399

    Google Scholar 

  • Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 171:41–53

    Google Scholar 

  • Rillig MC, Wright SF, Allen MF, Field CB (1999) Rise in carbon dioxide changes soil structure. Nature 400:628–628

    Google Scholar 

  • Rillig MC, Wright SF, Nichols KA, Schmidt WF, Torn MS (2001) Large contribution of arbuscular mycorrhizal fungi to soil carbon pools in tropical forest soils. Plant Soil 233:167–177

    Google Scholar 

  • Rillig MC, Wright SF, Eviner VT (2002) The role of arbuscular mycorrhizal fungi and glomalin in soil aggregation: comparing effects of five plant species. Plant Soil 238:325–333

    Google Scholar 

  • Rillig MC, Ramsey PW, Morris S, Paul EA (2003) Glomalin, an arbuscular-mycorrhizal fungal soil protein, responds to land-use change. Plant Soil 253:293–299

    Google Scholar 

  • Rosier CL, Hoye A, Rillig MC (2006) Glomalin-related soil protein: assessment of current detection and quantification tools. Soil Biol Biochem 38:2205–2211

    Google Scholar 

  • Russo PS, Blum FD, Ipsen JD, Miller WG, Abul-Hajj YJ (1982) The surface activity of the phytotoxin cerato-ulmin. Can J Bot 60:1414–1422

    Google Scholar 

  • Sarkar JM, Burns RG (1984) Synthesis and properties of β-glucosidase-phenolic copolymers as analogues of soil humic-enzyme complexes. Soil Biol Biochem 16:619–625

    Google Scholar 

  • Schlesinger WH (1991) Biogeochemistry – an analysis of global change. Academic Press, San Diego

    Google Scholar 

  • Schofield JA, Hagerman AE, Harold A (1998) Loss of tannins and other phenolics from willow litter. J Chem Ecol 24:1409–1421

    Google Scholar 

  • Scholtmeijer K, Janssen MI, Gerssen B, de Vocht ML, van Leeuwen MBM, van Kooten TG, Wösten HAB, Wessels JGH (2002) Surface modification created by using engineered hydrophobins. Appl Environ Microbiol 68:1367–1373

    Google Scholar 

  • Schulten H-R, Schnitzer M (1993) A state of the art structural concept for humic substances. Naturwissenschaften 80:29–30

    Google Scholar 

  • Schulze WX (2005) Protein analysis in dissolved organic matter: what proteins from organic debris, soil leachate and surface water can tell us – a perspective. Biogeosciences 2:75–86

    Google Scholar 

  • Schulze WX, Gleixner G, Kaiser K, Guggenberger G, Mann M, Schulze ED (2005) A proteomic fingerprint of dissolved organic carbon and of soil particles. Oecologia 142:335–343

    Google Scholar 

  • Sen R (2003) The root-microbe-soil interface: new tools for sustainable plant production. New Phytol 157:391–393

    Google Scholar 

  • Sexstone AJ, Revsbech NP, Parkin TB, Tiedje JM (1985) Direct measurement of oxygen profiles and denitrification rates in soil aggregates. Soil Sci Soc Am J 49:645–651

    Article  Google Scholar 

  • Simonart P, Batistic L, Mayaudon J (1967) Isolation of protein from humic acid extracted from soil. Plant Soil 27:153–161

    Google Scholar 

  • Singh M, Krikorian AD (1982) Inhibition of trypsin activity in vitro by phytate. J Agric Food Chem 30:799–800

    Google Scholar 

  • Six J, Feller C, Denef K, Ogle SM, de Moraes JC, Albrecht A (2002) Soil organic matter, biota and aggregation in temperate and tropical soils – effects of no-tillage. Agronomie 22:755–775

    Google Scholar 

  • Six J, Bossuyt H, Degryze S, Denef K (2004) A history of research on the link between (micro)aggregates, soil biota, and soil organic matter dynamics. Soil Tillage Res 79:7–31

    Google Scholar 

  • Six J, Elliott ET, Paustian K, Doran JW (1998) Aggregation and soil organic matter accumulation in cultivated and native grassland soils. Soil Sci Soc Am J 62:1367–1377

    Article  Google Scholar 

  • Smernik RJ, Baldock JA (2005) Does solid-state 15N NMR spectroscopy detect all soil organic nitrogen? Biogeochemistry 75:507–528

    Google Scholar 

  • Smolander A, Loponen J, Suominen K, Kitunen V (2005) Organic matter characteristics and C and N transformations in the humus layer under two tree species, Betula pendula and Picea abies. Soil Biol Biochem 37:1309–1318

    Google Scholar 

  • Sollins P, Homan P, Caldwell BA (1996) Stabilization and destabilization of soil organic matter: mechanisms and controls. Geoderma 74:65–105

    Google Scholar 

  • Sommerville K, Preston T (2001) Characterization of dissolved combined amino acids in marine waters. Rapid Commun Mass Spectrom 15:1287–1290

    Google Scholar 

  • Sørensen LH (1975) The influence of clay on the rate of decay of amino acid metabolites synthesized in soils during decomposition of cellulose. Soil Biol Biochem 7:171–177

    Google Scholar 

  • Sowden FJ, Chen Y, Schnitzer M (1977). The nitrogen distribution in soils formed under widely differing climatic conditions. Geochim Cosmochim Acta 41:1524–1526

    Google Scholar 

  • Steinberg PD, Rillig MC (2003) Differential decomposition of arbuscular mycorrhizal fungal hyphae and glomalin. Soil Biol Biochem 35:191–194

    Google Scholar 

  • Sternberger RE, Holden PA (2004) Macromolecular composition of unsaturated Psuedomonas aeruginosa biofilms with time and carbon source. Biofilms 1:37–47

    Google Scholar 

  • Stevenson FJ (1994) Humus chemistry: genesis, composition, reactions. Wiley Interscience, New York

    Google Scholar 

  • Suominen K, Kitunen V, Smolander A (2003) Characteristics of dissolved organic matter and phenolic compounds in forest soils under silver birch (Betula pendula), Norway spruce (Picea abies) and Scots pine (Pinus sylvestris). Eur J Soil Sci 54:287–293

    Google Scholar 

  • Sutton R, Sposito G (2005) Molecular structure in soil humic substances: the new view. Environ Sci Technol 39:9009–9015

    Google Scholar 

  • Takai S, Richards WC (1978) Cerato-ulmin, a wilting toxin of Ceratocystis ulmi: isolation and some properties of cerato-ulmin from the culture of C. ulmi Phytopathol Z 91:129–146

    Google Scholar 

  • Theng BKG (1979) Formation and properties of clay-polymer complexes. Elsevier Scientific Pub C, New York

    Google Scholar 

  • Tisdall JM, Oades JM (1982) Organic matter and water-stable aggregates in soils J Soil Sci 33:141–163

    Google Scholar 

  • Torkkeli M, Serimaa R, Ikkala O, Linder M (2002) Aggregation and self-assembly of hydrophobins from Trichoderma reesei: low-resolution structural models. Biophys J 83:2240–2247

    Article  Google Scholar 

  • Varki A (1993) Biological roles of oligosaccharides: all of the theories are correct. Glycobiology 3:97–130

    Google Scholar 

  • Verma L, Martin JP, Haider K (1975) Decomposition of carbon-14-labeled proteins, peptides, and amino acids; free and complexed with humic polymers. Soil Sci Soc Am Proc 39:279–284

    Article  Google Scholar 

  • Wang X, Shi F, Wösten HAB, Hektor H, Poolman B, Robillard GT (2005) The SC3 hydrophobin self-assembles into a membrane with distinct mass transfer properties. Biophys J 88:3434–3443

    Google Scholar 

  • Waksman SA (1938) Humus. Williams & Wilkins, Baltimore

    Google Scholar 

  • Waksman SA, Iyer KRN (1932) Contribution to our knowledge of the chemical nature and origin of humus: I On the synthesis of the “humus nucleus”. Soil Sci 34:43–69

    Article  Google Scholar 

  • Weintraub MN, Schimel JP (2005) Seasonal protein dynamics in Alaskan arctic tundra soils. Soil Biol Biochem 37:1469–1475

    Google Scholar 

  • Wessels JGH (1994) Developmental regulation of fungal cell wall formation. Ann Rev Phytopathol 32:413–437

    Google Scholar 

  • Wessels JGH,Ásgeirsdóttir SA, Birkenkamp KU, de Vries OMH, Lugones LG, Scheer JMJ, Schuren FHJ, Schuurs TA, van Wetter M-A, Wösten HAB (1995) Genetic regulation of emergent growth in Schizophyllum commune. Can J Bot 73: S273–S281

    Google Scholar 

  • Wessels JGH, de Vries OMH, Ásgeirsdóttir SA, Schuren FHJ (1991a) Hydrophobin genes involved in formation of aerial hyphae and fruit bodies in Schizophyllum. Plant Cell 3:793–799

    Google Scholar 

  • Wessels JGH, de Vries OMH, Ásgeirsdóttir SA, Springer J (1991b) The thn mutation of Schizophyllum commune which suppresses formation of aerial hyphae affects expression of the SC3 hydrophobin gene. J Gen Microbiol 137:2439–2445

    Google Scholar 

  • West CM (1986) Current ideas on the significance of protein glycosylation. Mol Cell Biochem 72:3–20

    Google Scholar 

  • Whiteford JR, Spanu PD (2002) Hydrophobins and the interactions between fungi and plants. Mol Plant Pathol 3:391–400

    Google Scholar 

  • Wösten HAB (2001) Hydrophobins: multipurpose proteins. Ann Rev Microbiol 55:625–646

    Google Scholar 

  • Wösten HAB, de Vocht ML (2000) Hydrophobins, the fungal coat unravelled. Biochim Biophys Acta 1469:79–86

    Google Scholar 

  • Wösten HAB, de Vries OMH, Wessels JGH (1993) Interfacial self-assembly of a fungal hydrophobin into a hydrophobic rodlet layer. Plant Cell 5:1567–1574

    Google Scholar 

  • Wösten HAB, Ruardy TG, van der Mei HC, Busscher HJ, Wessels JGH (1995) Interfacial self-assembly of a Schizophyllum commune hydrophobin into an insoluble amphipathic protein membrane depends on surface hydrophobicity. Colloids Surf B: Biointerfaces 5:189–195

    Google Scholar 

  • Wösten HAB, Schuren FHJ, Wessels JGH (1994) Interfacial self-assembly of a hydrophobin into an amphipathic protein membrane mediates fungal attachment to hydrophobic surfaces. EMBO J 13: 5848–5854

    Google Scholar 

  • Wösten HAB, Bohlmann R, Eckerskorn C, Lottspeich F, Bölker M, Kahmann R (1996) A novel class of small amphipathic peptides affect aerial hyphal growth and surface hydrophobicity in Ustilago maydis. EMBO J 15:4274–4281

    Google Scholar 

  • Wösten HAB, van Wetter M-A, Lugones LG, van der Mei HC, Busscher HJ, Wessels JGH (1999) How a fungus escapes the water to grow into the air. Curr Biol 9:85–88

    Google Scholar 

  • Wright SF, Anderson RL (2000) Aggregate stability and glomalin in alternative crop rotations for the central Great Plains. Biol Fertil Soils 31:249–253

    Google Scholar 

  • Wright SF, Upadhyaya A (1998) A survey of soils for aggregate stability and glomalin, a glycoprotein produced by hyphae of arbuscular mycorrhizal fungi. Plant Soil 198:97–107

    Google Scholar 

  • Wright SF, Upadhyaya A (1996) Extraction of an abundant and unusual protein from soil and comparison with hyphal protein of arbuscular mycorrhizal fungi. Soil Sci 161:575–586

    Google Scholar 

  • Yu Z, Zhang Q, Kraus TEC, Dahlgren RA, Anastacio C, Zasoski RJ (2002) Contribution of amino compounds to dissolved organic nitrogen in forest soils. Biogeochemistry 61:173–198

    Google Scholar 

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

    Google Scholar 

  • Zucker WV (1983) Tannins: does structure determine function ? An ecological perspective. Am Nat 121:335–365

    Google Scholar 

Download references

Acknowledgements

Funding for the Asilomar Conference on Mechanisms of SOM Stabilization, which brought the authors together for the first time, was provided by NSF, USDA-NRI, Kearney Foundation of Soil Science, Livermore National Laboratory, NASA, and the Forest Science Department, Oregon State University. MCR, BAC and PS acknowledge funding by the NSF Ecosystem Studies program and USDA NRI CSREES. We thank Dr. D. Mummey for comments on an earlier version of the manuscript.

Author information

Authors and Affiliations

  1. Institut für Biologie, Freie Universität Berlin, Altensteinstr. 6, 14195, Berlin, Germany

    Matthias C. Rillig

  2. Microbial Ecology Program, Division of Biological Sciences, University of Montana, 32 Campus Drive, Missoula, MT, 59812, USA

    Matthias C. Rillig

  3. Department of Forest Science, Oregon State University, 321 Richardson Hall, Corvallis, OR, 97331, USA

    Bruce A. Caldwell & Philip Sollins

  4. Microbiologie, H.R. Kruytgebouw, Universiteit Utrecht, Padualaan 8, 3584 CH, Utrecht, The Netherlands

    Han A. B. Wösten

Authors
  1. Matthias C. Rillig
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bruce A. Caldwell
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Han A. B. Wösten
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Philip Sollins
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Matthias C. Rillig.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rillig, M.C., Caldwell, B.A., Wösten, H.A.B. et al. Role of proteins in soil carbon and nitrogen storage: controls on persistence. Biogeochemistry 85, 25–44 (2007). https://doi.org/10.1007/s10533-007-9102-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10533-007-9102-6

Keywords

Search

Navigation