Skip to main content

Advertisement

Log in

From humic substances to soil organic matter–microbial contributions. In honour of Konrad Haider and James P. Martin for their outstanding research contribution to soil science

  • Frontiers in Soils and Sediments • Review Article
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

Many decades of research have shown that humic compounds as part of the soil organic matter (SOM) are essential for the stability and ecosystem services of soils. James P. Martin and Konrad Haider based on several pioneers in humus research improved the basis for the current knowledge of key processes in the soil environment, in particular structure and formation of humus triggered mainly by soil fungi. Other major contributions are briefly described but not in the focus of this article, such as their innovative tracer experiments with isotope-labelled xenobiotic chemicals and natural litter to study their fate. Both scientists inspired generations of younger researchers to advance their approaches and laid the cornerstone of the current understanding of soil organic matter formation.

Results and discussion

This article values the key experiments of Martin and Haider in this field and the related follow-up research finally resulting in the current view on formation mechanisms of SOM and non-extractable residues (NER) of xenobiotics. The improved understanding of these processes considering necromass with tissue residues of plants, microbes and animals challenges the traditional views of humic matter as macromolecular organic matrix, which according to the research of the last years represents only a variable part of the total organic matter besides associates of low molecular weight molecules. We discuss views on soil organic matter and humic substances that are nowadays considered not to differ in molecular diversity. We will start by demonstrating the understanding of humus characteristics and humus formation three decades ago closely related to the findings of Martin and Haider. Methodological approaches to characterize relevant structural and mechanistic pictures of SOM such as the priming effect, clay mineral catalysed reactions and the various mechanisms by which natural and xenobiotic chemicals are protected in soil are briefly illustrated by examples. Fungal activities in producing secondary metabolites like polyketides and their probably minor contributions to SOM formation are presented.

Conclusions and perspectives

Open research questions stimulated by these two soil scientists are sketched which are nowadays possible to address by new sophisticated high-resolution techniques.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Adu JK, Oades JM (1978) Utilization of organic materials in soil aggregates by bacteria and fungi. Soil Biol Biochem 10:117–122

    CAS  Google Scholar 

  • Alexander M (1995) How toxic are toxic chemicals in soil? Environ Sci Technol 29:2713–2717

    CAS  Google Scholar 

  • Alexander M (1999) Biodegradation and bioremediation. Academic, San Diego CA, p 453

    Google Scholar 

  • Alexandrova LN, Arshavskay TTH, Dorfman FM, Lyuzin MF, Yurlova OV (1968) Humus acids and their organo-mineral derivatives in soil. Int Soil Sci Congr Trans 3(9):143–152

    Google Scholar 

  • Amelung W (2001) Methods using amino sugars as markers for microbial residues in soil. In: Lal R, Kimble JM, Follettv RF, Stewart BA (eds) Assessment methods for soil carbon. Lewis Publishes, Boca Raton, FL, pp 233–272

    Google Scholar 

  • Anderson TH, Joergensen RG (1997) Relationship between SIR and FE estimates of microbial biomass C in deciduous forest soils at different pH. Soil Biol Biochem 29:1033–1042

    CAS  Google Scholar 

  • Arenella M, Giagnoni L, Masciandaro G, Ceccanti B, Nannipieri P, Renella G (2014) Interactions between proteins and humic substances affect protein identification by mass spectrometry. Biol Fertil Soils 50:447–454

    CAS  Google Scholar 

  • Bakken LR, Frostegard A (2006) Nucleic acid extraction from soil. In: Nannipieri P, Smalla K (eds) Nucleic acids and proteins in soil. Springer, Germany, pp 49–73

    Google Scholar 

  • Baldock JA, Nelson PN (2000) Soil organic matter. In: Huang PM, Li Y, Sumner ME (eds) Handbook of soil science. CRC Press, Boca Raton, FL, pp 25–84

    Google Scholar 

  • Baldock JA, Skjemstad JO (2000) Role of the soil matrix and minerals in protecting natural organic materials against biological attack. Org Geochem 31:697–710

    CAS  Google Scholar 

  • Baldock JA, Oades JM, Waters AG, Peng X, Vassallo AM, Wilson MA (1992) Aspects of the chemical structure of soil organic materials as revealed by solid-state 13C NMR spectroscopy. Biogeochemistry 16:1–42

    CAS  Google Scholar 

  • Beyer L (1996) Soil organic matter composition of spodic horizons in podzols of the northwest German lower plain. Sci Total Environ 181:167–180

    CAS  Google Scholar 

  • Bremner JM (1955) Recent work on soil organic matter at Rothamsted. Z Pflanzenernahr Dung Bodenkd 69:32–38

    CAS  Google Scholar 

  • Bremner JM (1965) Nitrogen-total. In: Sparks DL, Page AL, Helmke PA, Loeppert RH, Soltanpour PN, Tabatabai MA, Johnson CT, Summer ME (eds) Methods of soil analysis, part 3 chemical methods. SSSA, ASA, Madison, WI, pp 1085–1121

    Google Scholar 

  • Bremner JM, Huck RD (1982) Advances in methodology for research in nitrogen transformations in soil. In: Stevenson FJ (ed) Nitrogen in agricultural soils. ASA, Madison, WI, pp 467–502

    Google Scholar 

  • Brodowski S, John B, Flessa H, Amelung W (2006) Aggregate-occluded black carbon in soil. Eur J Soil Sci 57:539–547

    Google Scholar 

  • Certini G, Scalenghe R (2006) Soils. Basic concepts and future challenges. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Cotrufo F, Wallenstein MD, Boot CM, Denef K, Paul EA (2013) The microbial efficiency-matrix stabilization (MEMS) framework integrated plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter? Glob Chang Biol 19:988–995

    Google Scholar 

  • Dawel G, Kaestner M, Michels J, Poppitz W, Guenther W, Fritsche W (1997) Structure of a laccase-mediated product of coupling of 2,4-diamino-6-nitrotoluene to guaiacol, a model for coupling of 2,4,6-trinitrotoluene metabolites to a humic organic soil matrix. Appl Environ Microbiol 63:2560–2565

    CAS  Google Scholar 

  • Demain AL (1999) Pharmaceutically active secondary metabolites of microorganisms. Appl Microbiol Biotechnol 52:455–463

    CAS  Google Scholar 

  • Duchaufour P (1998) Handbook of pedology: soils, vegetation, environment. A A Balkema Publishers

  • Eisenman HC, Casadevail A (2012) Synthesis and assembly of fungal melanin. Appl Microbiol Biotechnol 93:931–940

    CAS  Google Scholar 

  • Elliott ET (1986) Aggregate structure and carbon, nitrogen and phosphorous in native and cultivated soils. Soil Sci Soc Am J 50:627–633

    Google Scholar 

  • Eloff JN, Pauli FW (1975) Extraction and electrophoretic fractionation of soil humic substances. Plant Soil 42:413–422

    CAS  Google Scholar 

  • Ertel JR, Hedges JI (1984) The lignin component of humic substances—distribution among soil and sedimentary humic, fulvic, and base-insoluble fractions. Geochim Cosmochim Acta 48:2065–2074

    CAS  Google Scholar 

  • Filip Z, Haider K, Martin JP (1972) Influence of clay minerals on the formation of humic substances by Epicoccum nigrum and Stahcybotry chartarum. Soil Biol Biochem 4:147–154

    CAS  Google Scholar 

  • Flaig W (1976) Soil organic matter studies. At Energ Rev 14:735–742

    Google Scholar 

  • Flessa H, Amelung W, Helfrich M, Wiesenberg GLB, Gleixner G, Brodowski S, Rethemeyer J, Kramer C, Grootes PM (2008) Storage and stability of organic matter and fossil carbon in a Luvisol and Phaeozem with continuous maize cropping: a synthesis. J Plant Nutr Soil Sci 171:36–51

    CAS  Google Scholar 

  • Flores-Cervantes DX, Maes HM, Schäffer A, Hollender J, Kohler HPE (2014) Slow biotransformation of carbon based nanomaterials by horseradish peroxidase. Environ Sci Technol 48:4826–4834

    CAS  Google Scholar 

  • Fontaine S, Mariotti A, Abbadie L (2003) The priming effect of organic matter: a question of microbial competition? Soil Biol Biochem 35:837–843

    CAS  Google Scholar 

  • Foster RC (1981) Polysaccharides in soil fabrics. Science 214:665–667

    CAS  Google Scholar 

  • Foster RC (1988) Microenvironments of soil microorganisms. Biol Fertil Soils 6:189–203

    Google Scholar 

  • Fox CA, Preston CM, Fyfe CA (1994) Micromorphological and 13C NMR characterization of a humic, lignic, and histic Folisol from British Columbia. Can J Soil Sci 74:1–15

    CAS  Google Scholar 

  • Fründ R, Lüdemann H-D (1991) Quantitative characterization of soil organic matter and its fractionation products by solid state high resolution C-13 (CPMAS) spectroscopy. Z Naturforsch 46c:982–988

    Google Scholar 

  • Fründ R, Haider K, Lüdemann H-D (1993) Impacts of soil management practices on the organic matter structure—investigations by CPMAS 13C NMR-spectroscopy. Z Pflanzenernähr Bodenkd 157:29–35

    Google Scholar 

  • Gillespie AW, Walley FL, Farrell RE, Leinweber P, Eckhardt KU, Regier TZ, Blyth RIR (2011) XANES and pyrolysis-FIMS evidence of organic matter composition in a hummocky landscape. Soil Sci Soc Am J 5:1741–1755

    Google Scholar 

  • González-Vila FJ, Martín F, Saiz-Jimenez C, Lentz H, Lüdemann H-D (1978) 13C nuclear magnetic resonance spectra of fungal melanins. Z Naturforsch 33:291–293

    Google Scholar 

  • Haider K, Martin JP (1967) Synthesis and transformation of phenolic compounds by Epicoccus nigrum in relation to humic acid formation. Soil Sci Soc Am Proc 31:766–772

    CAS  Google Scholar 

  • Haider K, Martin JP (1970) Humic acid-type phenolic polymers from Aspergillus sydowi culture medium, Stachybotrys ssp. cells and autooxidized phenols mixtures. Soil Biol Biochem 2:145–156

    CAS  Google Scholar 

  • Haider K, Martin JP (1975) Decomposition of specifically C-14 labeled benzoic and cinnamic acid derivatives in soil. Soil Sci Soc Am Proc 39:657–662

    CAS  Google Scholar 

  • Haider K, Martin JP (1981) Decomposition in soil of specifically 14C-labeled model and cornstalk lignins and coniferyl alcohol over two years as influenced by drying, rewetting, and additions of an available C substrate. Soil Biol Biochem 13:447–450

    CAS  Google Scholar 

  • Haider K, Martin JP (1988) Mineralization of 14C labeled humic acids and humic acid bound 14C xenobiotics by Phanerochaete chrysosporium. Soil Biol Biochem 20:425–429

    CAS  Google Scholar 

  • Haider K, Schäffer A (2009) Soil biochemistry. Science Publishers, Jersey, Plymouth, p 132

    Google Scholar 

  • Haider K, Frederick LR, Flaig W (1965) Reactions between amino acid compounds and phenols during oxidation. Plant Soil 22:49–64

    CAS  Google Scholar 

  • Hamer U, Marschner B (2006) Priming effects in different soil types induced by fructose, alanine, oxalic acid and catechol additions. Soil Biol Biochem 37:445–454

    Google Scholar 

  • Handley WR (1961) Further evidence for the importance of residual leaf protein complexes in litter decomposition and the supply of nitrogen for plant growth. Plant Soil 15:37–73

    CAS  Google Scholar 

  • Hatcher PG, Breger IA, Maciel GE, Szeverenyi NM (1985) Geochemistry of humin. In: Aiken GR, McKnight DM, Wershaw RL (eds) Humic substances in soil and water. Wiley, New York, pp 275–302

    Google Scholar 

  • Hatzinger PB, Alexander M (1995) Effect of aging of chemicals in soil on their biodegradability and extractability. Environ Sci Technol 29:537–545

    CAS  Google Scholar 

  • Hayes MH (1970) Adsorption of triazine herbicides on soil organic matter, including a short review on soil organic matter chemistry. Residue Rev 32:131–174

    CAS  Google Scholar 

  • Hayes MHB, Swift RS, Wardle RE, Brown JK (1975) Humic materials from an organic soil—comparison of extractants and of properties of extracts. Geoderma 13:231–245

    CAS  Google Scholar 

  • Hertweck C (2009) The biosynthetic logic of polyketide diversity. Angew Chem Int Ed 48:4688–4716

    CAS  Google Scholar 

  • Ivarson KC, Stevenson IL (1964) The decomposition of radioactive acetate in soils. The distribution of radioactivity in soil organic fractions. Can J Microbiol 10:677–682

    CAS  Google Scholar 

  • Jansson SL, Persson J (1982) Mineralization and immobilization of soil nitrogen. In: Stevenson FJ (ed) Nitrogen in agricultural soils. American Society of Agronomy, Madison, WI, pp 229–252

    Google Scholar 

  • Jenkinson DS (1966) The priming action. In: The use of isotopes in soil organic matter studies. Pergamon Press, Oxford, UK, pp 199–208

    Google Scholar 

  • Jenkinson DS, Ladd JN (1981) Microbial biomass in soil: measurement and turnover. In: Paul EA, Ladd JN (eds) Soil biochemistry. Marcel Dekker, New York, pp 415–471

    Google Scholar 

  • Kästner M, Nowak KM, Miltner A, Trapp S, Schäffer A (2014) Classification and modelling of non-extractable residue (NER) formation of xenobiotics in soil—a synthesis. Crit Rev Environ Sci Technol 44:2107–2171

    Google Scholar 

  • Kelleher BP, Simpson AJ (2006) Humic substances in soil: are they really chemically distinct? Environ Sci Technol 40:4605–4611

    CAS  Google Scholar 

  • Keller NP, Turner G, Bennett JW (2005) Fungal secondary metabolism—from biochemistry to genomics. Nat Rev Microbiol 12:937–947

    Google Scholar 

  • Kellner H, Zak DR (2009) Detection of expressed fungal type I polyketide synthase genes in a forest soil. Soil Biol Biochem 41:1344–1347

    CAS  Google Scholar 

  • Kennedy MJ, Pevear DR, Hill RJ (2002) Mineral surface control of organic carbon in black shale. Science 295:657–660

    CAS  Google Scholar 

  • Kirk TK, Shimada M (1985) Lignin biodegradation: the microorganisms involved and the physiology and biochemistry of degradation by white-rot fungi. In: Higuchi T (ed) Biosynthesis and biodegradation of wood components. Academic, San Diego, CA, pp 579–605

    Google Scholar 

  • Kleber M, Johnson MG (2010) Advances in understanding of molecular structure of soil organic matter: implications for interaction in the environment. Adv Agron 106:77–142

    CAS  Google Scholar 

  • Kleber M, Hong JP, Stahr K (1998) Microbial biomass C- and N dynamics in grassland soil amended with liquid manure. Z Pflanzenernähr Bodenkd 161:87–92

    CAS  Google Scholar 

  • Kleber M, Mikutta R, Torn S, Jahn R (2005) Poorly crystalline mineral phases protect organic matter in acid subsoil horizons. Eur J Soil Sci 56:717–725

    CAS  Google Scholar 

  • Kleber M, Sollins P, Sutton R (2007) A conceptual model of organo-mineral interactions in soils: self-assembly of organic molecular fragments into zonal structures on mineral surfaces. Biogeochemistry 85:9–24

    Google Scholar 

  • Knicker H, Fründ R, Lüdemann H-D (1993) The chemical nature of nitrogen in soil organic matter. Naturwissenschaften 80:219–221

    CAS  Google Scholar 

  • Knicker H, Almendros G, González-Vila FJ, Lüdemann H-D, Martín F (1995) 13C and 15N NMR analysis of some fungal melanins in comparison with other bio- and geomacromolecules. Org Geochem 23:1023–1028

    CAS  Google Scholar 

  • Knicker H, Lüdemann H-D, Haider K (1997) Incorporation studies of NH4 + during incubation of organic residues by 15N-CPMAS-NMR-spectroscopy. Eur J Soil Sci 48:431–441

    CAS  Google Scholar 

  • Kogel-Knabner I (2002) The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biol Biochem 34:139–162

    CAS  Google Scholar 

  • Kononova MM (1984) Organic matter and soil fertility. Soviet Soil Sci 16:71–86

    Google Scholar 

  • Koroleva OV, Kulikova NA, Alekseeva TN, Stepanova EV, Davidchik VN, Beliaeva EI, Tsvetkova EA (2007) Prikl Biokhim Mikrobiol 43:69–76

    CAS  Google Scholar 

  • Kuzyakov (2010) Priming effects: interactions between living and dead organic matter. Soil Biol Biochem 42:1363–1371

    CAS  Google Scholar 

  • Ladd JN, Butler JHA (1966) Comparison of some properties of soil humic acids and synthetic phenolic polymers incorporating amino derivatives. Aust J Soil Res 4:41–54

    CAS  Google Scholar 

  • Ladd JN, Foster RC, Nannipieri P, Oades JM (1996) Soil structure and biological activity. In: Stotzky G, Bollag J-M (eds). Marcel Dekker, New York, pp 23–78

  • Lammirato C, Miltner A, Wick L, Kästner M (2010) Hydrolysis of cellobiose by b-glucosidase in the presence of soil minerals interactions at solide liquid interfaces and effects on enzyme activity levels. Soil Biol Biochem 42:2203–2210

    CAS  Google Scholar 

  • Leinweber P, Blumenstein O, Schulten HR (1996) Organic matter composition in sewage farm soils: investigations by C-13-NMR and pyrolysis-field ionization mass spectrometry. Eur J Soil Sci 47:71–80

    Google Scholar 

  • Leinweber P, Kruse J, Baum C, Arcand M, Knight JD, Farrell R, Eckhardt KU, Kiersch K, Jandl G (2013) Advances in understanding organic nitrogen chemistry in soils using state-of-the-art analytical techniques. Adv Agron 119:83–151, Sparks DL (ed)

    CAS  Google Scholar 

  • Liang C, Balser TC (2010) Microbial production of recalcitrant organic matter in global soils: implications for productivity and climate policy. Nat Rev Microbiol 9:75

    Google Scholar 

  • Liang C, Balser TC (2011) Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nat Rev Microbiol 8:593–599

    Google Scholar 

  • Liang C, Cheng G, Wixson DL, Balser TC (2010) An absorbing Markov chain approach in understanding the microbial role in soil carbon stabilization. Biogeochemistry 106:303–309

    Google Scholar 

  • Longnecker K, Kuwajinski EB (2011) Composition of dissolved organic matter in groundwater. Geochim Cosmochim Acta 75:2752–2761

    CAS  Google Scholar 

  • Lüdemann HD, Lentz H, Martín JP (1982) Carbon-13 NMR spectra of some fungal melanins and humic acids. Soil Sci Soc Am J 46:957–962

    Google Scholar 

  • Marschner B, Brodowski S, Dreves A, Gleixner G, Gude A, Grootes PM, Hamer U, Heim A, Jandl G, Rong J, Kaiser K, Kalbitz K, Kramer C, Leinweber P, Rethemeyer J, Schaeffer A, Schmidt MWI, Schwark L, Wiesenburg GLB (2008) How relevant is recalcitrance for the stabilization of organic matter in soils? J Plant Nutr Soil Sci 171:91–110

    CAS  Google Scholar 

  • Martin JP, Haider K (1969) Phenolic polymers of Stachybotrys atra, Stachybotrys chartarum and Epicoccus nigrumin relation to humic acid formation. Soil Sci 107:260–270

    CAS  Google Scholar 

  • Martin JP, Haider K (1971) Microbial activity in relation to soil humus formation. Soil Sci 111:54–63

    CAS  Google Scholar 

  • Martin JP, Haider K (1976) Effect of montmorillonite and humate on growth and metabolic activity of some actinomycetes. Soil Biol Biochem 8:409–413

    CAS  Google Scholar 

  • Martin JP, 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

    CAS  Google Scholar 

  • Martin JP, Haider K, Wold D (1972) Synthesis of phenols and phenolic polymers by hendersonula toruloidea in relation to humic acid formation. Soil Sci Soc Am J 36:311–315

    CAS  Google Scholar 

  • Martin JP, Haider K, Farmer WJ, Fustec-Mathon E (1974) Decomposition and distribution of residual activity of some 14C-microbial polysaccharides and cells, glucose, cellulose and wheat straw in soil. Soil Biol Biochem 6:221–230

    CAS  Google Scholar 

  • Martin JP, Haider K, Kassim G (1980) Biodegradation and stabilization after 2 years of specific crop, lignin, and polysaccharide carbons in soils. Soil Sci Soc Am J 44:1250–1255

    CAS  Google Scholar 

  • Martin JP, Zunino H, Borie F, Aguilera S, Haider K (1982) Decomposition of 14C-labeled lignins, model humic acid polymers and fungal melanins in allophonic soils. Soil Biol Biochem 14:289–293

    CAS  Google Scholar 

  • Martins MR, Angers DA, Cora JE (2012) Co-accumulation of microbial residues and particulate organic matter in the surface layer of a no-till Oxisol under different crops. Soil Biol Biochem 50:208–213

    CAS  Google Scholar 

  • Mayaudon J (1986) The role of carbohydrates in the free enzymes in soil. In: Fichsman CH (ed) Peat and water. Aspects of water retention and dewatering in peat. Elsevier, New York, pp 263–309

    Google Scholar 

  • Mayaudon J, Simonart P (1963) Humification of microorganisms marques par 14C dans le sol. Ann Inst Pasteur 105:257–266

    CAS  Google Scholar 

  • Mayer LM, Schick LL, Hardy KR, Wagal R, McCarthy J (2004) Organic matter in small mesopores in sediments and soils. Geochim Cosmochim Acta 68:3868–3872

    Google Scholar 

  • Meuzelaar HLC, Haider K, Nagar BR, Martin JP (1977) Comparative studies of pyrolysis mass-spectra of melanins, model phenolic polymers, and humic acids. Geoderma 17:239–252

    CAS  Google Scholar 

  • Miltner A, Bombach P, Schmidt-Bruecken B, Kaestner M (2012) SOM genesis: microbial biomass as a significant source. Biogeochemistry 111:41–55

    CAS  Google Scholar 

  • Miyanaga A, Funa N, Awakawa T, Horinouchi S (2008) Direct transfer of starter substrates from type I fatty acid synthase to type III polyketide synthases in phenolic lipid synthesis. Proc Natl Acad Sci U S A 105:871–876

    CAS  Google Scholar 

  • Monreal CM, Schnitzer M (2013) The chemistry and biochemistry of organic components in the soil solutions of wheat rhizospheres. In: Sparks DL (ed) Advances in agronomy, vol 121, Book series advances in agronomy., pp 179–251

    Google Scholar 

  • Moritz LK, Liang C, Wagai R, Kitayama K, Balser TC (2009) Vertical distribution and pools of microbial residues in tropical forest soils formed from distinct parent materials. Biogeochemistry 92:83–94

    Google Scholar 

  • Morrison RI (1963) Products of the alkaline-nitrobenzene oxidation of soil organic matter. J Soil Sci 14:201–216

    CAS  Google Scholar 

  • Mueller CW, Koelbl A, Hoeschen C, Hilion F, Heister K, Herrmann M, Koegel-Knabner I (2012) Submicron scale imaging of soil organic matter dynamics using NanoSIMS—from single particles to intact aggregates. Org Geochem 42:1476–1488

    Google Scholar 

  • Murugan R, Kumar S (2013) Influence of long-term fertilisation and crop rotation on changes in fungal and bacterial residues in a tropical rice-field soil. Biol Fertil Soils 49:847–856

    Google Scholar 

  • Murugan R, Koch H-J, Joergensen RG (2014) Long-term influence of different tillage intensities on soil microbial biomass, residues and community structure at different depths. Biol Fertil Soils 50:487–498

    CAS  Google Scholar 

  • Myrold DD, Nannipieri P (2014) Classical techniques versus omics approaches. In: Nannipieri P, Pietramellara G, Renella G (eds) Omics in soil science. Caister Academic Press, Norfolk, UK, pp 179–187

    Google Scholar 

  • Nannipieri P, Paul EA (2009) The chemical and functional characterization of soil N and its biotic components. Soil Biol Biochem 41:2357–2369

    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

    Google Scholar 

  • O’Hagan D (1991) The polyketide metabolites. Ellis Horwood, Chicester, UK

    Google Scholar 

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

    CAS  Google Scholar 

  • Oades JM (1993) The role of biology in the formation, stabilization and degradation of soil structure. Geoderma 56:377–400

    Google Scholar 

  • Oades JM (1995) An overview of processes affecting the cycling of organic carbon in soils. In: Zepp RG, Sonntag C (eds) Role of nonliving organic matter in the earth’s carbon cycle. Wiley, New York, pp 293–303

    Google Scholar 

  • Olness A (2004) Humic substances: nature’s most versatile materials. Soil Sci 169:611–612

    CAS  Google Scholar 

  • Orlov DS, Sadovnikova LK (1975) Content and distribution of carbohydrates in major soil groups of USSR. Soviet Soil Sci 7:440–449

    Google Scholar 

  • Orlov DS, Biryukova ON, Sadovnikova LK, Fridland YF (1979) Use of the group composition of humus and of some biochemical characteristics to identify soils. Soviet Soil Sci 11:232–243

    Google Scholar 

  • Palm S, Linhares LF, As M, Martin JP (1990) Characterization of fungal melanins and soil humic acids by chemical analysis and infrared spectroscopy. Biol Fertil Soils 10:72–76

    Google Scholar 

  • Piccolo A (1996) Humus and soil conservation. In: Piccolo A (ed) Humic substances in terrestrial ecosystems. Elsevier, Amsterdam, pp 225–264

    Google Scholar 

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

    CAS  Google Scholar 

  • Piccolo A (2002) The supramolecular structure of humic substances: a novel understanding of humus chemistry and implications in soil science. Adv Agron 75:57–134

    CAS  Google Scholar 

  • Piel J, Hoang K, Moore BS (2000) Natural metabolic diversity encoded by the enterocin biosynthesis gene cluster. J Amer Chem Soc 122:5415–5416

    CAS  Google Scholar 

  • Pietramellara G, Ascher J, Borgogni F, Ceccherini MT, Guerri G, Nannipieri P (2009) Extracellular DNA in soil and sediment: fate and ecological relevance. Biol Fertil Soils 45:219–235

    CAS  Google Scholar 

  • Remusat L, Hatton PJ, Nico PS, Zeller B, Kleber M, Derrien D (2012) NanoSIMS study of organic matter associated with soil aggregates: advantages, limitations, and combination with STXM. Environ Sci Technol 46:3943–3949

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Rennert T, Haendel M, Hoeschen C, Lugmeier J, Steffens M, Totsche KU (2014) A nano SIMS study on the distribution of soil organic matter, iron and manganese in a nodule from a stagnosol. Eur J Soil Sci 65:684–692

    CAS  Google Scholar 

  • Robert M, Chenu C (1992) Interactions between microorganisms and soil minerals. In: Bollag JM, Stotzky G (eds) Soil biochemistry. Marcel Dekker, New York, pp 307–404

    Google Scholar 

  • Rumpel C, Kögel-Knabner I, Bruhn F (2002) Vertical distribution, age, and chemical composition of organic carbon in two forest soils of different pedogenesis. Org Geochem 33:1131–1142

    CAS  Google Scholar 

  • Saiz-Jimenez C, Haider K, Martin JP (1975) Anthraquinones and phenols as intermediates in formation of dark-colored, humic acid-like pigments by Eurotium echinolatum. Soil Sci Soc Am Proc 39:649–653

    CAS  Google Scholar 

  • Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88(6):1386–1394

    Google Scholar 

  • Schlichting A, Rimmer DL, Eckhardt KU, Heumann S, Abbott GD, Leinweber P (2013) Identifying potential antioxidant compounds in NaOH extracts of UK soils and vegetation by untargeted mass spectrometric screening. Soil Biol Biochem 58:16–26

    CAS  Google Scholar 

  • Schmidt MWI, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kogel-Knabner I, Lehmann J, Manning DAC, Nannipieri P, Rasse DP, Weiner S, Trumbore SE (2011) Persistence of soil organic matter as an ecosystem property. Nature 478:49–56

    CAS  Google Scholar 

  • Schnitzer M, Neyroud JA (1975) Further investigations on the chemistry of fungal “humic acids”. Soil Biol Biochem 7:365–371

    CAS  Google Scholar 

  • Schnitzer M, Monreal JA (2011) Quo Vadis soil organic matter research?: a biological link to the chemistry of humification. Adv Agron 113:139–213

    Google Scholar 

  • Schurig C, Smittenberg R, Berger J, Kraft F, Woche S, Goebel MO, Heipieper HJ, Miltner A, Kästner M (2013) Microbial cell-envelope fragments and the formation of soil organic matter—a case study from a glacier forefield. Biogeochemistry 113:595–612

    CAS  Google Scholar 

  • Senesi N, Loffredo E (1999) The chemistry of soil organic matter. In: Sparks DL (ed) Soil physical chemistry. CRC Press, Roca Baton, FL, pp 239–370

    Google Scholar 

  • Setia R, Smith P, Marschner P (2011) Introducing a decomposition rate modifier in the Rothamsted carbon model to predict soil organic carbon stocks in saline soils. Environ Sci Technol 45:6396–6403

    CAS  Google Scholar 

  • Shen B (2003) Polyketide biosynthesis beyond the type I, II, and III polyketide synthase paradigms. Curr Opin Chem Biol 7:285–295

    CAS  Google Scholar 

  • Shields JA, Paul EA, Lowe WE, Parkinson D (1973) Turnover of microbial tissue in soil under field conditions. Soil Biol Biochem 5:753–764

    Google Scholar 

  • Simpson AJ, Simpson MJ, Smith E, Kelleher BP (2007a) Microbially derived inputs to soil organic matter: are current estimates too low? Environ Sci Technol 41:8070–8076

    CAS  Google Scholar 

  • Simpson AJ, Song G, Smith E, Lam B, NE H, Hayes MHB (2007b) Unraveling the structural components of soil humin by use of solution-state nuclear magnetic resonance spectroscopy. Environ Sci Technol 41:876–883

    CAS  Google Scholar 

  • Simpson AJ, McNally DJ, Simpson MJ (2011) NMR spectroscopy in environmental research: from molecular interactions to global processes. Prog Nucl Magn Reson Spectrosc 58:97–175

    CAS  Google Scholar 

  • Sithole BB, Guy RD (1987) Models of tetracycline in aquatic environments. Water Air Soil Pollut 32:315–321

    CAS  Google Scholar 

  • Six J, Feller C, Denef K, Ogle SM, de Moraes Sa 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 

  • Smeijkalova D, Piccolo A (2008) Aggregation and disaggregation of humic supramolecular assemblies by NMR diffusion ordered spectroscopy DOSY-NMR. Environ Sci Technol 42:699–709

    Google Scholar 

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

    Google Scholar 

  • Solomon D, Lehmann J, Wang J, Kinyangi J, Heymann K, Lu YS, Wirick S, Jacobsen C (2012a) Micro- and nano-environments of C sequestration in soil: a multi-elemental STXM-NEXAFS assessment of black C and organomineral associations. Sci Total Environ 438:372–388

    CAS  Google Scholar 

  • Solomon D, Lehmann J, Harden J, Wang J, Kinyangi J, Heyman K, Karunakaran C, Lu Y, Wirick S, Jacobsen C (2012b) Micro and nano-environments of carbon sequestration: multi-element STXM-NEXAFS spectromicroscopy assessment of microbial carbon and mineral associations. Chem Geol 329:53–73

    CAS  Google Scholar 

  • Sorensen LH (1966) Formation of soil organic matter during decomposition of plant components. In: The use of isotopes in soil organic matter studies. Pergamon Press, Oxford, UK, pp 271–274

    Google Scholar 

  • Sorensen LH (1974) Rate of decomposition of organic matter in soil as influenced by repeated air drying rewetting and drying and repeated addition of organic matter. Soil Biol Biochem 6:287–292

    Google Scholar 

  • Stevenson FJ (1976) Organic matter reactions involving pesticides in soil. ACS Symp Ser 29:180–207

    CAS  Google Scholar 

  • Stevenson FJ (1994) Humus chemistry, genesis, composition, reactions. Book. Wiley, New York, p 512

    Google Scholar 

  • Stott DE, Kassim G, Jarrel WM, Martin JP, Haider K (1983) Stabilization and incorporation into biomass of specific plant carbons during biodegradation in soil. Plant Soil 70:15–26

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Swaby RJ, Ladd JN (1963) Stability and origin of soil humus. The use of isotopes in organic matter studies. IAEA, Vienna, pp 153–159

    Google Scholar 

  • Swift RS, Chaney K (1979) Role of soil organic colloids in the formation and stabilization of soil colloids. J Sci Food Agric 30:329–330

    Google Scholar 

  • Theng BKG (2012) Humic substances. In: Theng BKG (ed) Formation and properties of clay-polymer-complexes. Develop Clay Sci 4:391–456

  • Theng BKG, Churchman GJ, Newman RH (1986) The occurrence of interlayer clay-organic complexes in two New Zealand soils. Soil Sci 142:262–266

    CAS  Google Scholar 

  • Thiele-Bruhn S (2003) Pharmaceutical antibiotic compounds in soil: a review. J Plant Nutr Soil Sci 166:145–167

    CAS  Google Scholar 

  • Thiele-Bruhn S, Leinweber P, Eckhardt KU, Siem HK, Blume HP (2014) Chernozem properties of black soils in the Baltic region of Germany as revealed by mass-spectrometric fingerprinting of organic matter. Geoderma 213:144–154

    CAS  Google Scholar 

  • van Groenigen KJ, Bloem J, Bååth E, Boeckx P, Rousk J, Bodé S, Forristal D, Jones MB (2010) Abundance, production and stabilization of microbial biomass under conventional and reduced tillage. Soil Biol Biochem 42:48–55

    Google Scholar 

  • Verma L, Martin JP, Haider K (1975) Decomposition of carbon-14-1abeled proteins, peptides, and amino acids; free and complexed with humic polymers. Soil Sci Soc Am Proc 39:279–283

    CAS  Google Scholar 

  • Violante A, Gianfreda L (2000) Role of biomolecules in the formation and reactivity toward nutrients and organics of variable charge minerals and organomineral complexes in soil environments. In: Bollag JM, Stotzky G (eds) Soil biochemistry. Marcel Dekker, New York, pp 207–270

    Google Scholar 

  • Vogel C, Mueller C, Hoeschen C, Buegger F, Heister K, Schulz S, Schloter M, Koegel-Knabner I (2014) Submicron structures provide preferential spots for carbon and nitrogen sequestration in soils. Nat Commun 5:2947

    Google Scholar 

  • von Lutzow M, Koegel-Knabner I, Ekschmitt K, Matzner E, Guggenberger G, Marschern B, Flessa H (2006) Stabilization of organic matter in temperate soils: mechanisms and their relevance under different soil conditions—a review. Eur J Soil Sci 57:426–445

    Google Scholar 

  • von Lutzow M, Kogel-Knabner I, Ludwig B, Matzner E, Flessa H, Ekschmitt K, Guggenberger G, Marschner B, Kalbitz K (2008) Stabilization mechanisms of organic matter in four temperate soils: development and application of a conceptual model. J Plant Nutr Soil Sci 171:111–124

    Google Scholar 

  • Wagner GH (1968) Significance of microbial tissue to soil organic matter. In: Isotopes and radiation in soil organic matter studies. FAO/IAEA, Vienna, pp 197–205

    Google Scholar 

  • Waksman SA (1925a) The soil population. Proc Natl Acad Sci U S A 11:476–481

    CAS  Google Scholar 

  • Waksman SA (1925b) What is humus? Proc Natl Acad Sci U S A 11:463–468

    CAS  Google Scholar 

  • Waksman SA (1926) Microorganisms concerned in the decomposition of celluloses in the soil. J Bacteriol 12:57–84

    CAS  Google Scholar 

  • Waksman SA (1936) Humus, origin, chemical composition and importance in nature. The Williams and Wilkin Company, Baltimore, MD

    Google Scholar 

  • Waksman SA (1939) The role of microorganisms in the conservation of the soil. Science 90:304–305

    CAS  Google Scholar 

  • Wershaw RL (1986) A new model for humic materials and their interactions with hydrophobic organic chemicals in soil-water or sediment-water systems. J Contam Hydrol 1:29–46

    CAS  Google Scholar 

  • Wilcken H, Sorge C, Schulten HR (1997) Molecular composition and chemometric differentiation and classification of soil organic matter in Podzol B-horizons. Geoderma 76:193–219

    CAS  Google Scholar 

  • Wildung RE, Chester G, Behmer DE (1970) Alkaline nitrobenzene oxidation of plant lignins and soil humic colloids. Plant Soil 32:221–237

    CAS  Google Scholar 

  • Wilson MA (1987) NMR techniques and applications in geochemistry and soil chemistry. Pergamon Press, Oxford, UK, p 353

    Google Scholar 

  • Wilson MA, Pugmire RJ, Grant DM (1983) Nuclear magnetic resonance spectroscopy of soils and related materials. Relaxation of 13C nuclei in cross polarization nuclear magnetic resonance experiments. Org Geochem 5:121–129

    CAS  Google Scholar 

  • Wright AL, Dou F, Hons FM (2007) Crop species and tillage effects on carbon sequestration in subsurface soil. Soil Sci 172:124–131

    CAS  Google Scholar 

  • Xiang L, Kalaitzis JA, Moore BS (2004) EncM, a versatile enterocin biosynthetic enzyme involved in Favorskii oxidative rearrangement, aldol condensation, and heterocycle-forming reactions. Proc Natl Acad Sci U S A 101:15609–15614

    CAS  Google Scholar 

  • Zavgorodnyaya YA, Demin VV, Kurakov AV (2002) Biochemical degradation of soil humic acids and fungal melanins. Org Geochem 33:347–355

    CAS  Google Scholar 

  • Zunino H, Borie F, Aguilera S, Martin JP, Haider K (1982) Decomposition of 14C-labeled glucose, plant and microbial products and phenols in volcanic ash-derived soils of Chile. Soil Biol Biochem 14:37–43

    CAS  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge support of the German Research Foundation (DFG) in the frame of the Priority Programme 1315 ‘Biogeochemical Interfaces in Soils’.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Andreas Schaeffer.

Additional information

Responsible editor: Zhihong Xu

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Schaeffer, A., Nannipieri, P., Kästner, M. et al. From humic substances to soil organic matter–microbial contributions. In honour of Konrad Haider and James P. Martin for their outstanding research contribution to soil science. J Soils Sediments 15, 1865–1881 (2015). https://doi.org/10.1007/s11368-015-1177-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-015-1177-4

Keywords

Navigation