Biogeochemistry

, Volume 85, Issue 1, pp 25–44 | Cite as

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

  • Matthias C. Rillig
  • Bruce A. Caldwell
  • Han A. B. Wösten
  • Philip Sollins
Original Paper

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.

Keywords

Hydrophobins Glomalin-related soil protein Carbon storage Soil organic nitrogen Soil microbial protein Extracellular enzymes 

References

  1. Alexandrescu AT (2005) Amyloid accomplices and enforcers. Protein Sci 14:1–12Google Scholar
  2. 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 31–46Google Scholar
  3. Amelung W, Zhang X, Flach KW (2006) Amino acids in grassland soils: climatic effects on concentrations and chirality. Geoderma 130:207–217Google Scholar
  4. 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 48:295–300Google Scholar
  5. 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 34:487–497Google Scholar
  6. Basaraba J, Starkey RL (1966) Effects of plant tannins on decomposition of organic substances. Soil Sci 101:17–23Google Scholar
  7. 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 134:2269–2279Google Scholar
  8. Benoit RE, Starkey RL, Basaraba J (1968) Effect of purified plant tannins on decomposition of some organic compounds and plant materials. Soil Sci 105:153–158Google Scholar
  9. 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 258:12198–12202Google Scholar
  10. Blackwood CB, Dell CJ, Smucker AJM, Paul EA (2006) Eubacterial communities in different soil macroaggregate environments and cropping systems. Soil Biol Biochem 38:720–728Google Scholar
  11. 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 96:531–544Google Scholar
  12. Böckelmann U, Szewzyk U, Grohmann E (2003) A new enzymatic method for the detachment of particle associated soil bacteria. J Microb Meth 55:201–211Google Scholar
  13. 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 37:195–204Google Scholar
  14. Bradford MM (1976) A rapid and sensitive method for quantification of microgram quantities of protein utilizing the principle of protein-dye-binding. Anal Biochem 72:248–254Google Scholar
  15. 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 32:1227–1240Google Scholar
  16. Bremner JM (1965) Organic forms of nitrogen. Agronomy 9:1238–1255Google Scholar
  17. Brewer R (1964) Fabric and mineral analysis of soils. Wiley, NYGoogle Scholar
  18. Brisou JF (1995) Biofilms, methods for enzymatic release of microorganisms. CRC Press. Boca Raton, FLGoogle Scholar
  19. Burdon J (2001) Are the traditional concepts of the structures of humic substances realistic? Soil Sci 166:752–769Google Scholar
  20. Burns RG (1978) Soil enzymes. Academic Press, New YorkGoogle Scholar
  21. Burns RG, Dick RP (2002) Enzymes in the environment: activity, ecology, and applications. Marcel Dekker, New YorkGoogle Scholar
  22. Busto MD, Perez-Mateos M (1995) Extraction of humic-β-glucosidase fractions from soils. Biol Fertil Soils 20:77–82Google Scholar
  23. 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 280:212–215Google Scholar
  24. Butler MJ, Day AW (1998) Fungal melanins: a review. Can J Microbiol 44:1115–1136Google Scholar
  25. Caldwell BA (2005) Enzyme activities as a component of soil biodiversity: a review. Pedobiologia 49:637–644Google Scholar
  26. 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 4:55–61Google Scholar
  27. 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 3–40Google Scholar
  28. Cheryan M (1980) Phytic acid interactions in food systems. Crit Rev Food Sci Nutr 13:297–335CrossRefGoogle Scholar
  29. Christensen BT (1992) Physical fractionation of soil and organic matter in primary particle size and density separates. Adv Soil Sci 20:1–90Google Scholar
  30. Claessen D (2004) Structural proteins involved in morphological differentiation of streptomycetes. Thesis (Microbiology, University of Groningen, The NetherlandsGoogle Scholar
  31. 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 17:1714–1726Google Scholar
  32. 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 53:433–443Google Scholar
  33. Coelho RR, Linares LF, Martin JP (1985) Amino acid distribution in some fungal melanins and of soil humic acids from Brazil. Plant Soil 87:337–346Google Scholar
  34. 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 77:1622–1630Google Scholar
  35. Cosgrove DJ (1966) The chemistry and biochemistry of inositol polyphosphates. Rev Pure Appl Chem 16:209–224Google Scholar
  36. Dalal RC (1977) Soil organic phosphorus. Adv Agron 29:85–117Google Scholar
  37. 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 37:55–66Google Scholar
  38. de Jong JF (2006) Aerial hyphae of Schizophyllum commune: their function and formation. Thesis, University of UtrechtGoogle Scholar
  39. 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 11:1199–1205Google Scholar
  40. 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 159:330–335Google Scholar
  41. Díaz-Zorita M, Perfect E, Grove JH (2002) Disruptive methods for assessing soil structure. Soil Tillage Res 64:3–22Google Scholar
  42. Dobson CM (1999) Protein misfolding, evolution and disease. Trend Biochem Sci 24:329–332Google Scholar
  43. Dormaar JF, Smoliak S, Willms WD (1990) Soil chemical properties during succession from abandoned cropland to native range. J Range Manag 43:260–265Google Scholar
  44. Driver JD, Holben WE, Rillig MC (2005) Characterization of glomalin as a hyphal wall component of arbuscular mycorrhizal fungi. Soil Biol Biochem 37:101–106Google Scholar
  45. Elliott ET, Coleman DC (1988) Let the soil work for us. Ecol Bull 39:23–32Google Scholar
  46. 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 17:1727–1740Google Scholar
  47. 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 33:1827–1839Google Scholar
  48. Friedel JK, Scheller E (2002) Composition of hydrolysable amino acids in soilk organic matter and soil microbial biomass. Soil Biol Biochem 34:315–325Google Scholar
  49. Friedenauer S, Berlet HH (1989) Sensitivity and variability of the Bradford protein assay in the presence of detergents. Anal Biochem 178:263–268Google Scholar
  50. Gadkar V, Rillig MC (2006) The arbuscular mycorrhizal fungal protein glomalin is a putative homolog of heat shock protein 60. FEMS Microbiol Lett 263:93–101Google Scholar
  51. Gallet C, Lebreton P (1995) Evolution of phenolic patterns and associated litters and humus of a mountain forest ecosystem. Soil Biol Biochem 27:157–165Google Scholar
  52. Gebbink MFBG, Claessen D, Bouma B, Dijkhuizen L, Wösten HAB (2005) Amyloids – a functional coat for microorganisms. Nat Rev Microbiol 3:333–341Google Scholar
  53. Gil H, Mata-Segreda JF, Schowen RL (1991) Effect of non-enzymatic glycosylation on reactivity in proteolysis [in Spanish] Acta Cient Venez 42:16–23Google Scholar
  54. Grossman RB, Lynn WC (1967) Gel-like films that may form at the air-water interface in soils. Soil Sci Soc Am Proc 31:259–262CrossRefGoogle Scholar
  55. 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 46:2590–2595Google Scholar
  56. Hagerman AE, Robbins CT (1987) Implication of soluble tannin–protein complexes for tannin analysis and plant defense mechanisms. J Chem Ecol 13:1243–1258Google Scholar
  57. Harner MJ, Ramsey PW, Rillig MC (2004) Protein accumulation and distribution in floodplain soils and river foam. Ecol Lett 7:829–836Google Scholar
  58. Harris P (1972) Micro-organisms in surface films from soil crumbs. Soil Biol Biochem 4:105–106Google Scholar
  59. Haslam E (1989) Plant polyphenols: vegetable tannins revisited. Cambridge University Press, 230 ppGoogle Scholar
  60. Hättenschwiler S, Vitousek P (2000) The role of polyphenols in terrestrial ecosystem nutrient cycling. Trends Ecol Evol 15:238–243Google Scholar
  61. Horner JD, Gosz JR, Cates RG (1988) The role of carbon-based plant secondary metabolites in decomposition in terrestrial ecosystems. Am Nat 132:869–883Google Scholar
  62. 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 25:1249–1256Google Scholar
  63. Ho JGS, Kitov PI, Paszkiewicz E, Sadowska J, Bundlet DR, Ng KK-S (2005) Ligand-assisted aggregation of proteins. J Biol Chem 280:31999–32008Google Scholar
  64. 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 69:4521–4533Google Scholar
  65. Ikan R (1996) The Maillard reaction. Consequences for the chemical and life sciences. John Wiley & Sons, Chichester, UKGoogle Scholar
  66. Jahnel JB, Frimmel FH (1995) Enzymatic release of amino acids from different humic substances. Acta Hydrochim Hydrobiol 23:31–35Google Scholar
  67. 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 32:516–526Google Scholar
  68. 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 23:4847–4854Google Scholar
  69. 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 25:2731–2739Google Scholar
  70. Jastrow JD (1996) Soil aggregate formation and the accrual of particulate and mineral-associated organic matter. Soil Biol Biochem 28:665–676Google Scholar
  71. Jokic A, Frenkel AI, Vairavamurthy MA, Huang PM (2001) Birnssite catalysis of the Maillard reaction: its significance in natural humification. Geophys Res Lett 28:3899–3902Google Scholar
  72. 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 35:747–762Google Scholar
  73. Keeney DR, Bremner JM (1964) Effect of cultivation on the nitrogen distribution in soils. Soil Sci Soc Am Proc 28:653–656CrossRefGoogle Scholar
  74. 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)Google Scholar
  75. 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)Google Scholar
  76. Knicker H (2000) Biogenic Nitrogen in soils as revealed by solid-state Carbon-13 and Nitrogen-15 Nuclear Magnetic Resonance spectroscopy. J Environ Qual 29:715–723Google Scholar
  77. Knicker H, Hatcher PG (1997) Survival of protein in an organic-rich sediment. Possible protection by encapsulation in organic matter. Naturwissenschaften 84:231–234Google Scholar
  78. 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 32:241–252Google Scholar
  79. Kojima RT (1947) Soil organic nitrogen: I. Nature of the organic nitrogen in a muck soil from Geneva, New York. Soil Sci 64:157–165Google Scholar
  80. 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 30:971–981Google Scholar
  81. Kraus TEC, Dahlgren RA, Zasoski RJ (2003a) Tannins in nutrient dynamics of forest ecosystems: a review. Plant Soil 256:41–66Google Scholar
  82. 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 29:703–730Google Scholar
  83. Kuiters AT, Denneman CAJ (1987) Water-soluble phenolic substances in soils under several coniferous and deciduous tree species. Soil Biol Biochem 19:765–769Google Scholar
  84. Kuo M-J, Alexander M (1967) Inhibition of the lysis of fungi by melanins. J Bacteriol 94:624–629Google Scholar
  85. Ladd JN, Brisbane PG (1967) Release of amino acids from soil humic acids by proteolytic enzymes. Aust J Soil Res 5:161–171Google Scholar
  86. Leinweber P, Schulten H-R (2000) Nonhydrolyzable forms of soil organic nitrogen: extractability and composition. J Plant Nutr Soil Sci 163:433–439Google Scholar
  87. Lewis JA, Starkey RL (1968) Vegetable tannins, their decomposition and effects on decomposition of some organic compounds. Soil Sci 106:241–247Google Scholar
  88. 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 11:2257–2266Google Scholar
  89. Lipson DA, Schmidt SK, Monson RK (1999) Links between microbial population dynamics and nitrogen availability in an alpine ecosystem. Ecology 80:1623–1631Google Scholar
  90. Lockwood JL (1960) Lysis of mycelia of plant pathogenic fungi by natural soil. Phytopathology 50:787–789Google Scholar
  91. Loll MJ, Bollag J-M (1983) Protein transformation in soil. Adv Agron 36:351–382Google Scholar
  92. Loomis WD, Battaile J (1966) Plant phenolic compounds and the isolation of plant enzymes. Phytochemistry 5:423–438Google Scholar
  93. 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 31:431–436Google Scholar
  94. 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 32:779–792Google Scholar
  95. 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 92:278–287Google Scholar
  96. 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 142:1321–1329Google Scholar
  97. Lugones LG, Wösten HAB, Wessels JGH (1998) A hydrophobin (ABH3) specifically secreted by vegetatively growing hyphae of Agaricus bisporus (common white button mushroom). Microbiology 144:2345–2353CrossRefGoogle Scholar
  98. 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 103:635–640Google Scholar
  99. 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 53:707–716Google Scholar
  100. Lutgen ER, Clairmont DL, Graham J, Rillig MC (2003) Seasonality of arbuscular mycorrhizal hyphae and glomalin in a western Montana grassland. Plant Soil 257:71–83Google Scholar
  101. 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 10:65–78Google Scholar
  102. Martens DA, Loeffelmann KL (2003) Soil amino acid composition quantified by acid hydrolysis and anion-chromatography-pulsed amperometry. J Agric Food Chem 51:6521–6529Google Scholar
  103. 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 10:483–486Google Scholar
  104. Matsumoto S, Ae N, Yamagata M (2000) Extraction of mineralizable organic nitrogen from soils by a neutral phosphate buffer solution. Soil Biol Biochem 32:1293–1299Google Scholar
  105. McManus JP, Davis KG, Lilley TH, Haslam E (1981) The association of proteins with polyphenols. J Chem Soc Commun 309–311Google Scholar
  106. Merlini G, Belloti V (2003) Molecular mechanisms of amyloidosis. N Engl J Med 349:583–596Google Scholar
  107. 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 30:48–51Google Scholar
  108. Mummey DL, Holben W, Six J, Stahl P (2006) Spatial stratification of soil bacterial populations in aggregates of diverse soils. Microb Ecol 51:404–411Google Scholar
  109. Nakas JP, Klein DA (1979) Decomposition of microbial cell components in a semi-arid grassland soil. Appl Environ Microbiol 38:454–460Google Scholar
  110. 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 5:271–275Google Scholar
  111. 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 79:275–296Google Scholar
  112. Northup RR, Yu Z, Dahlgren RA, Vogt KA (1995) Polyphenol control of nitrogen release from pine litter. Nature 377: 227–229Google Scholar
  113. 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 42:189–220Google Scholar
  114. Nyman BF (1985) Protein-proanthocyanidin interactions during extraction of Scots pine needles. Phytochemistry 24:2939–2944Google Scholar
  115. Oades JM (1984) Soil organic matter and structural stability: mechanisms and implications for management. Plant Soil 76:319–337Google Scholar
  116. Oh HI, Hoff JE, Armstrong GS, Haff LA (1980) Hydrophobic interactions in tannin–protein complexes. J Agric Food Chem 28:394–398Google Scholar
  117. Omoike A, Chorover J (2004) Spectroscopic study of extracellular polymeric substances from Bacillus subtilis: aqueous chemistry and adsorption effects. Biomacromolecules 5:1219–1230Google Scholar
  118. Opdenakker G, Rudd PM, Ponting CP, Dwek RA (1993) Concepts and principles pf glycobiology. FASEB J 7:1330–1337Google Scholar
  119. Parsek MR, Fuqua C (2004) Biofilms 2003: emerging themes and challenges in studies of surface-associated microbial life. J Bacteriol 186:4427–4440Google Scholar
  120. Paul EA, Clark FE (1996) Soil microbiology and biochemistry, 2nd edn. Academic Press, OrlandoGoogle Scholar
  121. Piccolo A (2001) The supramolecular structure of humic substances. Soil Sci 166:810–832Google Scholar
  122. 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 66:79–92Google Scholar
  123. Plante AF, Feng Y, McGill WB (2002) A modeling approach to quantifying soil macroaggregate dynamics. Can J Soil Sci 82:181–190Google Scholar
  124. Raab TK, Lipson DA, Monson RK (1999) Soil amino acid utilization among species of the Cyperaceae: plant and soil processes. Ecology 80:2408–2419CrossRefGoogle Scholar
  125. Ravindran V, Bryden WL, Kornegay ET (1995) Phytates: occurrence, bioavailability and implications in poultry nutrition. Poult Avian Bio Rev 6:125–143Google Scholar
  126. Rice EL, Pancholy SK (1973) Inhibition of nitrification by climax ecosystems II Additional evidence and possible role of tannins. Am J Bot 60:691–702Google Scholar
  127. Rillig MC (2004) Arbuscular mycorrhizae, glomalin and soil quality. Can J Soil Sci 84:355–363Google Scholar
  128. Rillig MC (2005) A connection between fungal hydrophobins and soil water repellency. Pedobiologia 49:395–399Google Scholar
  129. Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 171:41–53Google Scholar
  130. Rillig MC, Wright SF, Allen MF, Field CB (1999) Rise in carbon dioxide changes soil structure. Nature 400:628–628Google Scholar
  131. 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 233:167–177Google Scholar
  132. 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 238:325–333Google Scholar
  133. Rillig MC, Ramsey PW, Morris S, Paul EA (2003) Glomalin, an arbuscular-mycorrhizal fungal soil protein, responds to land-use change. Plant Soil 253:293–299Google Scholar
  134. Rosier CL, Hoye A, Rillig MC (2006) Glomalin-related soil protein: assessment of current detection and quantification tools. Soil Biol Biochem 38:2205–2211Google Scholar
  135. Russo PS, Blum FD, Ipsen JD, Miller WG, Abul-Hajj YJ (1982) The surface activity of the phytotoxin cerato-ulmin. Can J Bot 60:1414–1422Google Scholar
  136. Sarkar JM, Burns RG (1984) Synthesis and properties of β-glucosidase-phenolic copolymers as analogues of soil humic-enzyme complexes. Soil Biol Biochem 16:619–625Google Scholar
  137. Schlesinger WH (1991) Biogeochemistry – an analysis of global change. Academic Press, San DiegoGoogle Scholar
  138. Schofield JA, Hagerman AE, Harold A (1998) Loss of tannins and other phenolics from willow litter. J Chem Ecol 24:1409–1421Google Scholar
  139. 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 68:1367–1373Google Scholar
  140. Schulten H-R, Schnitzer M (1993) A state of the art structural concept for humic substances. Naturwissenschaften 80:29–30Google Scholar
  141. 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 2:75–86Google Scholar
  142. 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 142:335–343Google Scholar
  143. Sen R (2003) The root-microbe-soil interface: new tools for sustainable plant production. New Phytol 157:391–393Google Scholar
  144. 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 49:645–651CrossRefGoogle Scholar
  145. Simonart P, Batistic L, Mayaudon J (1967) Isolation of protein from humic acid extracted from soil. Plant Soil 27:153–161Google Scholar
  146. Singh M, Krikorian AD (1982) Inhibition of trypsin activity in vitro by phytate. J Agric Food Chem 30:799–800Google Scholar
  147. 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 22:755–775Google Scholar
  148. 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 79:7–31Google Scholar
  149. 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 62:1367–1377CrossRefGoogle Scholar
  150. Smernik RJ, Baldock JA (2005) Does solid-state 15N NMR spectroscopy detect all soil organic nitrogen? Biogeochemistry 75:507–528Google Scholar
  151. 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 37:1309–1318Google Scholar
  152. Sollins P, Homan P, Caldwell BA (1996) Stabilization and destabilization of soil organic matter: mechanisms and controls. Geoderma 74:65–105Google Scholar
  153. Sommerville K, Preston T (2001) Characterization of dissolved combined amino acids in marine waters. Rapid Commun Mass Spectrom 15:1287–1290Google Scholar
  154. 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 7:171–177Google Scholar
  155. Sowden FJ, Chen Y, Schnitzer M (1977). The nitrogen distribution in soils formed under widely differing climatic conditions. Geochim Cosmochim Acta 41:1524–1526Google Scholar
  156. Steinberg PD, Rillig MC (2003) Differential decomposition of arbuscular mycorrhizal fungal hyphae and glomalin. Soil Biol Biochem 35:191–194Google Scholar
  157. Sternberger RE, Holden PA (2004) Macromolecular composition of unsaturated Psuedomonas aeruginosa biofilms with time and carbon source. Biofilms 1:37–47Google Scholar
  158. Stevenson FJ (1994) Humus chemistry: genesis, composition, reactions. Wiley Interscience, New YorkGoogle Scholar
  159. 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 54:287–293Google Scholar
  160. Sutton R, Sposito G (2005) Molecular structure in soil humic substances: the new view. Environ Sci Technol 39:9009–9015Google Scholar
  161. 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 91:129–146Google Scholar
  162. Theng BKG (1979) Formation and properties of clay-polymer complexes. Elsevier Scientific Pub C, New YorkGoogle Scholar
  163. Tisdall JM, Oades JM (1982) Organic matter and water-stable aggregates in soils J Soil Sci 33:141–163Google Scholar
  164. Torkkeli M, Serimaa R, Ikkala O, Linder M (2002) Aggregation and self-assembly of hydrophobins from Trichoderma reesei: low-resolution structural models. Biophys J 83:2240–2247CrossRefGoogle Scholar
  165. Varki A (1993) Biological roles of oligosaccharides: all of the theories are correct. Glycobiology 3:97–130Google Scholar
  166. 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 39:279–284CrossRefGoogle Scholar
  167. 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 88:3434–3443Google Scholar
  168. Waksman SA (1938) Humus. Williams & Wilkins, BaltimoreGoogle Scholar
  169. 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 34:43–69CrossRefGoogle Scholar
  170. Weintraub MN, Schimel JP (2005) Seasonal protein dynamics in Alaskan arctic tundra soils. Soil Biol Biochem 37:1469–1475Google Scholar
  171. Wessels JGH (1994) Developmental regulation of fungal cell wall formation. Ann Rev Phytopathol 32:413–437Google Scholar
  172. 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–S281Google Scholar
  173. 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 3:793–799Google Scholar
  174. 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 137:2439–2445Google Scholar
  175. West CM (1986) Current ideas on the significance of protein glycosylation. Mol Cell Biochem 72:3–20Google Scholar
  176. Whiteford JR, Spanu PD (2002) Hydrophobins and the interactions between fungi and plants. Mol Plant Pathol 3:391–400Google Scholar
  177. Wösten HAB (2001) Hydrophobins: multipurpose proteins. Ann Rev Microbiol 55:625–646Google Scholar
  178. Wösten HAB, de Vocht ML (2000) Hydrophobins, the fungal coat unravelled. Biochim Biophys Acta 1469:79–86Google Scholar
  179. Wösten HAB, de Vries OMH, Wessels JGH (1993) Interfacial self-assembly of a fungal hydrophobin into a hydrophobic rodlet layer. Plant Cell 5:1567–1574Google Scholar
  180. 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 5:189–195Google Scholar
  181. 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: 5848–5854Google Scholar
  182. 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 15:4274–4281Google Scholar
  183. 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 9:85–88Google Scholar
  184. Wright SF, Anderson RL (2000) Aggregate stability and glomalin in alternative crop rotations for the central Great Plains. Biol Fertil Soils 31:249–253Google Scholar
  185. 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 198:97–107Google Scholar
  186. 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 161:575–586Google Scholar
  187. 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 61:173–198Google Scholar
  188. 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 31:679–695Google Scholar
  189. Zucker WV (1983) Tannins: does structure determine function ? An ecological perspective. Am Nat 121:335–365Google Scholar

Copyright information

© Springer Science+Business Media, Inc. 2007

Authors and Affiliations

  • Matthias C. Rillig
    • 1
    • 2
  • Bruce A. Caldwell
    • 3
  • Han A. B. Wösten
    • 4
  • Philip Sollins
    • 3
  1. 1.Institut für BiologieFreie Universität BerlinBerlinGermany
  2. 2.Microbial Ecology Program, Division of Biological SciencesUniversity of MontanaMissoulaUSA
  3. 3.Department of Forest ScienceOregon State UniversityCorvallisUSA
  4. 4.Microbiologie, H.R. KruytgebouwUniversiteit UtrechtUtrechtThe Netherlands

Personalised recommendations