Biogeochemistry

, Volume 111, Issue 1–3, pp 41–55 | Cite as

SOM genesis: microbial biomass as a significant source

  • Anja Miltner
  • Petra Bombach
  • Burkhard Schmidt-Brücken
  • Matthias Kästner
Synthesis and Emerging Ideas

Abstract

Proper management of soil organic matter (SOM) is needed for maintaining soil fertility and for mitigation of the global increase in atmospheric CO2 concentrations and should be informed by knowledge about the sources, spatial organisation and stabilisation processes of SOM. Recently, microbial biomass residues (i.e. necromass) have been identified as a significant source of SOM. Here, we propose that cell wall envelopes of bacteria and fungi are stabilised in soil and contribute significantly to small-particulate SOM formation. This hypothesis is based on the mass balance of a soil incubation experiment with 13C-labelled bacterial cells and on the visualisation of the microbial residues by means of scanning electron microscopy (SEM). At the end of a 224-day incubation, 50% of the biomass-derived C remained in the soil, mainly in the non-living part of SOM (40% of the added biomass C). SEM micrographs only rarely showed intact cells. Instead, organic patchy fragments of 200–500 nm size were abundant and these fragments were associated with all stages of cell envelope decay and fragmentation. Similar fragments, developed on initially clean and sterile in situ microcosms during exposure to groundwater, provide clear evidence for their formation during microbial growth and surface colonisation. Microbial cell envelope fragments thus contribute significantly to SOM formation. This origin and the related macromolecular architecture of SOM are consistent with most observations on SOM, including the abundance of microbial-derived biomarkers, the low C/N ratio, the water repellency and the stabilisation of biomolecules, which in theory should be easily degradable.

Keywords

Soil organic matter Humic compounds C turnover Microbial biomass Bacterial cell walls Scanning electron microscopy 

Notes

Acknowledgments

This study was financially supported by the Helmholtz Centre for Environmental Research UFZ, by the German Research Council (DFG, Kä 887/1 and Mi 598/2) and by the European Commission (ModelPROBE, contract number 213161). We acknowledge long and fruitful discussions about this topic with Reimo Kindler (TU Berlin), Christian Schurig (UFZ) and Gabi Schaumann (University of Koblenz-Landau) who also gave helpful comments on earlier versions of this manuscript. Jörg Ackermann (Nano Technology Systems Division, Carl Zeiss NTS GmbH, Carl-Zeiss-Str. 56, 73447 Oberkochen) provided the EDX data and further helpful comments. The Martin Luther University of Halle granted access to their long-term agricultural experiment “Ewiger Roggenbau” for large-scale soil sampling. We thank two anonymous reviewers for valuable comments, which improved this manuscript significantly.

Supplementary material

10533_2011_9658_MOESM1_ESM.doc (26 kb)
Supplementary material 1 (DOC 25 kb)
10533_2011_9658_MOESM2_ESM.doc (1.1 mb)
Supplementary material 2 (DOC 1172 kb)

References

  1. Allison SD, Jastrow JD (2006) Activities of extracellular enzymes in physically isolated fractions of restored grassland soils. Soil Biol Biochem 38:3245–3256CrossRefGoogle Scholar
  2. Barriuso E, Benoit P, Dubus IG (2008) Formation of pesticide nonextractable (bound) residues in soil: magnitude, controlling factors and reversibility. Environ Sci Technol 42:1845–1854CrossRefGoogle Scholar
  3. Bellamy PH, Loveland PJ, Bradley RI, Lark RM, Kirk GJD (2005) Carbon losses from all soils across England and Wales 1978–2003. Nature 437:245–247CrossRefGoogle Scholar
  4. Bombach P, Chatzinotas A, Neu TR, Kästner M, Lueders T, Vogt C (2010) Enrichment and characterization of a sulfate-reducing toluene-degrading microbial consortium by combining in situ microcosms and stable isotope probing techniques. FEMS Microbiol Ecol 71:237–246CrossRefGoogle Scholar
  5. Brodowski S, Amelung W, Haumaier L, Abetz C, Zech W (2005) Morphological and chemical properties of black carbon in physical soil fractions as revealed by scanning electron microscopy and energy-dispersive X-ray spectroscopy. Geoderma 128:116–129CrossRefGoogle Scholar
  6. Burns RG (1982) Enzyme activity in soil: location and a possible role in microbial ecology. Soil Biol Biochem 14:423–427CrossRefGoogle Scholar
  7. Chenu C, Stotzky G (2002) Interactions between microorganisms and soil particles: an overview. In: Huang PM, Bollag J-M, Senesi N (eds) Interactions between soil particles and microorganisms. Wiley, Chichester, pp 3–40Google Scholar
  8. Cozzolino A, Conte P, Piccolo A (2001) Conformational changes of humic substances induced by some hydroxy-, keto-, and sulfonic acids. Soil Biol Biochem 33:2001CrossRefGoogle Scholar
  9. de Jonge LW, Moldrup P, Schjønning P (2009) Soil Infrastructure, interfaces & translocation processes in Inner Space (“Soil-it-is”): towards a road map for the constraints and crossroads of soil architecture and biophysical processes. Hydrol Earth Syst Sci 13:1485–1502CrossRefGoogle Scholar
  10. Drenovsky RE, Elliot GN, Graham KJ, Scow KM (2004) Comparison of phospholipid fatty acid (PLFA) and total soil fatty acid methyl esters (TSFAME) for characterizing soil microbial communities. Soil Biol Biochem 36:1793–1800CrossRefGoogle Scholar
  11. Fan TW-M, Lane AN, Chekmenev E, Wittebort RJ, Higashi RM (2004) Synthesis and physico-chemical properties of peptides in soil humic substances. J Pept Res 63:253–264CrossRefGoogle Scholar
  12. Flaig W (1975) An introductory review on humic substances: aspects of research on their genesis, their physical and chemical properties, and their effect on organisms. In: Povoledo D, Golterman HL (eds) Humic substances: their structure and function in the biosphere. Centre for Agricultural Publishing and Documentation, Wageningen, pp 19–42Google Scholar
  13. Flaig W, Beutelspacher H, Rietz E (1975) Chemical composition and physical properties of humic substances. In: Gieseking JE (ed) Soil components organic components, vol I. Springer Verlag, New York, pp 1–211CrossRefGoogle Scholar
  14. Foster RC (1981) Polysaccharides in soil fabrics. Science 214:665–667CrossRefGoogle Scholar
  15. Foster RC (1988) Microenvironments of soil microorganisms. Biol Fertil Soils 6:189–203CrossRefGoogle Scholar
  16. Geyer R, Peacock AD, Miltner A, Richnow H-H, White DC, Sublette KL, Kästner M (2005) In situ assessment of biodegradation potential using biotraps amended with 13C-labelled benzene or toluene. Environ Sci Technol 39:4983–4989CrossRefGoogle Scholar
  17. Glaser B, Turrión M-B, Alef K (2004) Amino sugars and muramic acid—biomarkers for soil microbial community structure analysis. Soil Biol Biochem 36:399–407CrossRefGoogle Scholar
  18. Gleixner G, Bol R, Balesdent J (1999) Molecular insight into soil carbon turnover. Rapid Commun Mass Spectrom 13:1278–1283CrossRefGoogle Scholar
  19. Graber ER, Tagger S, Wallach R (2009) Role of divalent fatty acid salts in soil water repellency. Soil Sci Soc Am J 73:541–549CrossRefGoogle Scholar
  20. Grandy AS, Neff JC (2008) Molecular C dynamics downstream: the biochemical decomposition sequence and its impact on soil organic matter structure and function. Sci Total Environ 404:297–307CrossRefGoogle Scholar
  21. Grandy AS, Sinsabaugh RL, Neff JC, Stursova M, Zak DR (2008) Nitrogen deposition effects on soil organic matter chemistry are linked to variation in enzymes, ecosystems and size fractions. Biogeochemistry 91:37–49CrossRefGoogle Scholar
  22. Guggenberger G, Frey SD, Six J, Paustian K, Elliott ET (1999) Bacterial and fungal cell-wall residues in conventional and no-tillage agroecosystems. Soil Sci Soc Am J 63:1188–1198CrossRefGoogle Scholar
  23. Jobbágy EG, Jackson RB (2000) The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol Appl 10(2):423–436CrossRefGoogle Scholar
  24. Jones DL (1999) Amino acid biodegradation and its potential effects on organic nitrogen capture by plants. Soil Biol Biochem 31:613–622CrossRefGoogle Scholar
  25. Kaiser K, Eusterhues K, Rumpel C, Guggenberger G, Kögel-Knabner I (2002) Stabilization of organic matter by soil minerals—investigations of density and particle-size fractions from two acid forest soils. J Plant Nutr Soil Sci 165:451–549CrossRefGoogle Scholar
  26. Kandeler E, Palli S, Stemmer M, Gerzabek MH (1999) Tillage changes microbial biomass and enzyme activities in particle-size fractions of a Haplic Chernozem. Soil Biol Biochem 31:1253–1264CrossRefGoogle Scholar
  27. Kappler A, Straub KL (2005) Geomicrobiological cycling of iron. Rev Mineral Geochem 59:85–108CrossRefGoogle Scholar
  28. Kästner M (2000) “Humification” process or formation of refractory soil organic matter. In: Klein J (ed) Environmental processes II, vol 11b. Biotechnology, 2nd edn. Wiley-VCH, Weinheim, pp 89–125Google Scholar
  29. Kästner M, Richnow HH (2001) Formation of residues of organic pollutants within the soil matrix—mechanisms and stability. In: Stegmann R, Brunner G, Calmano W, Matz G (eds) Treatment of contaminated soil—fundamentals, analysis, applications. Springer-Verlag, Berlin, pp 219–251Google Scholar
  30. Kästner M, Fischer A, Nijenhuis I, Geyer R, Stelzer N, Bombach P, Tebbe CC, Richnow HH (2006) Assessment of microbial in situ activity in contaminated aquifers. Eng Life Sci 6:234–251CrossRefGoogle Scholar
  31. Kelleher BP, Simpson AJ (2006) Humic substances in soil: are they really chemically distinct? Environ Sci Technol 40:4605–4611CrossRefGoogle Scholar
  32. Kiem R, Kögel-Knabner I (2003) Contribution of lignin and polysaccharides to the refractory carbon pool in C-depleted arable soils. Soil Biol Biochem 35:101–118CrossRefGoogle Scholar
  33. Kindler R, Miltner A, Richnow H-H, Kästner M (2006) Fate of gram-negative bacterial biomass in soil—mineralization and contribution to SOM. Soil Biol Biochem 38:2860–2870CrossRefGoogle Scholar
  34. Kindler R, Miltner A, Thullner M, Richnow H-H, Kästner M (2009) Fate of bacterial biomass-derived fatty acids in soil and their contribution to soil organic matter. Org Geochem 40:29–37CrossRefGoogle Scholar
  35. 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 85:9–24CrossRefGoogle Scholar
  36. Knicker H, Fründ R, Lüdemann HD (1993) The chemical nature of nitrogen in native soil organic matter. Naturwissenschaften 80:219–221CrossRefGoogle Scholar
  37. Kögel-Knabner I (2002) The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biol Biochem 34:139–162CrossRefGoogle Scholar
  38. Kong AYY, Scow KM, Córdova-Kreylos AL, Holmes WC, Six J (2011) Microbial community composition and carbon cycling within soil microenvironments of conventional, low-input, and organic cropping systems. Soil Biol Biochem 43:20–30CrossRefGoogle Scholar
  39. Krull ES, Baldock JA, Skjemstad JO (2003) Importance of mechanisms and processes of the stabilization of soil organic matter for modelling carbon turnover. Funct Plant Biol 30:207–222CrossRefGoogle Scholar
  40. Lal R (2004) Soil carbon sequestration impacts on global climate change and food security. Science 304:1623–1627CrossRefGoogle Scholar
  41. Lamparter A, Bachmann J, Goebel M-O, Woche SK (2009) Carbon mineralization in soil: impact of wetting-drying, aggregation and water repellency. Geoderma 150:324–333CrossRefGoogle Scholar
  42. Liang C, Balser TC (2010) Microbial production of recalcitrant organic matter in global soils: implications for productivity and climate policy. Nat Rev Microbiol 9:75CrossRefGoogle Scholar
  43. Liang C, Cheng G, Wixon DL, Balser TC (2010) An absorbing markov chain approach to understanding the microbial role in soil carbon stabilization. Biogeochemistry (in press). doi: 10.1007/s10533-010-9525-3
  44. Lichtfouse É, Berthier G, Houot S, Barriuso E, Bergheaud V, Vallaeys T (1995) Stable carbon isotope evidence for the microbial origin of C14–C18 n-alkanoic acids in soils. Org Geochem 23:849–852CrossRefGoogle Scholar
  45. Lueders T, Kindler R, Miltner A, Friedrich MW, Kaestner M (2006) Identification of bacterial micropredators distinctively active in a soil microbial food web. Appl Environ Microbiol 72:5342–5348CrossRefGoogle Scholar
  46. Madigan MT, Martinko JM (2006) Brock biology of microorganisms, 11th edn. Pearson Education Inc., Prentice HallGoogle Scholar
  47. Marschner B, Brodowski S, Dreves A, Gleixner G, Gude A, Grootes PM, Hamer U, Heim A, Jandl G, Ji R, Kaiser K, Kalbitz K, Kramer C, Leinweber P, Rethemeyer J, Schäffer A, Schmidt MWI, Schwark L, Wiesenberg GLB (2008) How relevant is recalcitrance for the stabilization of organic matter in soils? J Plant Nutr Soil Sci 171:91–110CrossRefGoogle Scholar
  48. Martin JP, Haider K (1971) Microbial activity in relation to soil humus formation. Soil Sci 111:54–63CrossRefGoogle Scholar
  49. Miltner A, Kindler R, Knicker H, Richnow H-H, Kästner M (2009) Fate of microbial biomass-derived amino acids in soil and their contribution to soil organic matter. Org Geochem 40:978–985CrossRefGoogle Scholar
  50. Nowak KM, Miltner A, Gehre M, Schäffer A, Kästner M (2011) Formation and fate of bound residues from microbial biomass during 2,4-D degradation in soil. Environ Sci Technol 45:999–1006CrossRefGoogle Scholar
  51. Ranjard L, Richaume A, Jocteur-Monrozier L, Nazaret S (1997) Response of soil bacteria to Hg(II) in relation to soil characteristics and cell location. FEMS Microbiol Ecol 24:321–331CrossRefGoogle Scholar
  52. Rasse DP, Dignac M-F, Bahri H, Rumpel C, Mariotti A, Chenu C (2006) Lignin turnover in an agricultural field: from plant residues to soil-protected fractions. Eur J Soil Sci 57:530–538CrossRefGoogle Scholar
  53. Schink B (1999) Habitats of Prokaryotes. In: Lengeler JW, Drews G, Schlegel HG (eds) Biology of the prokaryotes. Georg Thieme Verlag, Stuttgart, pp 763–803Google Scholar
  54. Simpson RT, Frey SD, Six J, Thiet RK (2004) Preferential accumulation of microbial carbon in aggregate structures of no-tillage soils. Soil Sci Soc Am J 68:1249–1255CrossRefGoogle Scholar
  55. Simpson AJ, Simpson MJ, Smith E, Kelleher BP (2007a) Microbially derived inputs to soil organic matter: are current estimates too low? Environ Sci Technol 41:8070–8076CrossRefGoogle Scholar
  56. 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 41:876–883CrossRefGoogle Scholar
  57. Six J, Elliott ET, Keith P (2000) Soil macroaggregate turnover and microaggregate formation: a mechanism for C sequestration under no-tillage agriculture. Soil Biol Biochem 32:2099–2103CrossRefGoogle Scholar
  58. Six J, Frey SD, Thiet RK, Batten KM (2006) Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci Soc Am J 70:555–569CrossRefGoogle Scholar
  59. Sollins P, Homann P, Caldwell BA (1996) Stabilization and destabilization of soil organic matter: mechanisms and controls. Geoderma 74:65–105CrossRefGoogle Scholar
  60. Stemmer M, Gerzabek MH, Kandeler E (1998) Organic matter and enzyme activity in particle-size fractions of soils obtained after low-energy sonication. Soil Biol Biochem 30:9–17CrossRefGoogle Scholar
  61. Stevenson FJ (1994) Humus chemistry: genesis, composition, reactions, 2nd edn. Wiley, New YorkGoogle Scholar
  62. Tisdall JM, Oades JM (1982) Organic matter and water-stable aggregates in soils. J Soil Sci 33:141–163CrossRefGoogle Scholar
  63. von Lützow M, Kögel-Knabner I, Ekschmitt K, Matzner E, Guggenberger G, Marschner 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 57:426–445CrossRefGoogle Scholar
  64. von Lützow M, Kögel-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 171:111–124CrossRefGoogle Scholar
  65. von Wandruszka R (1998) The micellar model of humic acid: evidence from pyrene fluorescence measurements. Soil Sci 163:921–930CrossRefGoogle Scholar
  66. Wershaw RL (1993) Model for humus in soils and sediments. Environ Sci Technol 27:814–816CrossRefGoogle Scholar
  67. Wershaw RL (1999) Molecular aggregation of humic substances. Soil Sci 164:803–813CrossRefGoogle Scholar
  68. Young IM, Crawford JW (2004) Interactions and self-organization in the soil-microbe complex. Science 304:1634–1637CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Anja Miltner
    • 1
  • Petra Bombach
    • 2
  • Burkhard Schmidt-Brücken
    • 3
    • 4
  • Matthias Kästner
    • 1
  1. 1.UFZ – Helmholtz-Centre for Environmental Research, Department of Environmental BiotechnologyLeipzigGermany
  2. 2.UFZ – Helmholtz-Centre for Environmental Research, Department of Isotope BiogeochemistryLeipzigGermany
  3. 3.Institute of Material ScienceTechnische Universität DresdenDresdenGermany
  4. 4.Papiertechnische StiftungAbteilung Oberflächenveredelung – Funktionale OberflächenHeidenauGermany

Personalised recommendations