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SOM genesis: microbial biomass as a significant source

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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.

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References

  • Allison SD, Jastrow JD (2006) Activities of extracellular enzymes in physically isolated fractions of restored grassland soils. Soil Biol Biochem 38:3245–3256

    Article  Google Scholar 

  • Barriuso E, Benoit P, Dubus IG (2008) Formation of pesticide nonextractable (bound) residues in soil: magnitude, controlling factors and reversibility. Environ Sci Technol 42:1845–1854

    Article  Google Scholar 

  • Bellamy PH, Loveland PJ, Bradley RI, Lark RM, Kirk GJD (2005) Carbon losses from all soils across England and Wales 1978–2003. Nature 437:245–247

    Article  Google Scholar 

  • 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 71:237–246

    Article  Google Scholar 

  • 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 128:116–129

    Article  Google Scholar 

  • Burns RG (1982) Enzyme activity in soil: location and a possible role in microbial ecology. Soil Biol Biochem 14:423–427

    Article  Google Scholar 

  • 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 3–40

    Google Scholar 

  • Cozzolino A, Conte P, Piccolo A (2001) Conformational changes of humic substances induced by some hydroxy-, keto-, and sulfonic acids. Soil Biol Biochem 33:2001

    Article  Google Scholar 

  • 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 13:1485–1502

    Article  Google Scholar 

  • 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 36:1793–1800

    Article  Google Scholar 

  • 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 63:253–264

    Article  Google Scholar 

  • 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 19–42

    Google Scholar 

  • 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 1–211

    Chapter  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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 39:4983–4989

    Article  Google Scholar 

  • Glaser B, Turrión M-B, Alef K (2004) Amino sugars and muramic acid—biomarkers for soil microbial community structure analysis. Soil Biol Biochem 36:399–407

    Article  Google Scholar 

  • Gleixner G, Bol R, Balesdent J (1999) Molecular insight into soil carbon turnover. Rapid Commun Mass Spectrom 13:1278–1283

    Article  Google Scholar 

  • Graber ER, Tagger S, Wallach R (2009) Role of divalent fatty acid salts in soil water repellency. Soil Sci Soc Am J 73:541–549

    Article  Google Scholar 

  • 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 404:297–307

    Article  Google Scholar 

  • 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 91:37–49

    Article  Google Scholar 

  • 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 63:1188–1198

    Article  Google Scholar 

  • Jobbágy EG, Jackson RB (2000) The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol Appl 10(2):423–436

    Article  Google Scholar 

  • Jones DL (1999) Amino acid biodegradation and its potential effects on organic nitrogen capture by plants. Soil Biol Biochem 31:613–622

    Article  Google Scholar 

  • 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 165:451–549

    Article  Google Scholar 

  • 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 31:1253–1264

    Article  Google Scholar 

  • Kappler A, Straub KL (2005) Geomicrobiological cycling of iron. Rev Mineral Geochem 59:85–108

    Article  Google Scholar 

  • 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 89–125

    Google Scholar 

  • 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 219–251

    Google Scholar 

  • 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 6:234–251

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Kiem R, Kögel-Knabner I (2003) Contribution of lignin and polysaccharides to the refractory carbon pool in C-depleted arable soils. Soil Biol Biochem 35:101–118

    Article  Google Scholar 

  • 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 38:2860–2870

    Article  Google Scholar 

  • 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 40:29–37

    Article  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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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 43:20–30

    Article  Google Scholar 

  • 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 30:207–222

    Article  Google Scholar 

  • Lal R (2004) Soil carbon sequestration impacts on global climate change and food security. Science 304:1623–1627

    Article  Google Scholar 

  • Lamparter A, Bachmann J, Goebel M-O, Woche SK (2009) Carbon mineralization in soil: impact of wetting-drying, aggregation and water repellency. Geoderma 150:324–333

    Article  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

    Article  Google Scholar 

  • 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

  • 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 23:849–852

    Article  Google Scholar 

  • 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 72:5342–5348

    Article  Google Scholar 

  • Madigan MT, Martinko JM (2006) Brock biology of microorganisms, 11th edn. Pearson Education Inc., Prentice Hall

    Google Scholar 

  • 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 171:91–110

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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 40:978–985

    Article  Google Scholar 

  • 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 45:999–1006

    Article  Google Scholar 

  • 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 24:321–331

    Article  Google Scholar 

  • 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 57:530–538

    Article  Google Scholar 

  • Schink B (1999) Habitats of Prokaryotes. In: Lengeler JW, Drews G, Schlegel HG (eds) Biology of the prokaryotes. Georg Thieme Verlag, Stuttgart, pp 763–803

    Google Scholar 

  • 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 68:1249–1255

    Article  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

    Article  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

    Article  Google Scholar 

  • 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 32:2099–2103

    Article  Google Scholar 

  • Six J, Frey SD, Thiet RK, Batten KM (2006) Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci Soc Am J 70:555–569

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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 30:9–17

    Article  Google Scholar 

  • Stevenson FJ (1994) Humus chemistry: genesis, composition, reactions, 2nd edn. Wiley, New York

    Google Scholar 

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

    Article  Google Scholar 

  • 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 57:426–445

    Article  Google Scholar 

  • 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 171:111–124

    Article  Google Scholar 

  • von Wandruszka R (1998) The micellar model of humic acid: evidence from pyrene fluorescence measurements. Soil Sci 163:921–930

    Article  Google Scholar 

  • Wershaw RL (1993) Model for humus in soils and sediments. Environ Sci Technol 27:814–816

    Article  Google Scholar 

  • Wershaw RL (1999) Molecular aggregation of humic substances. Soil Sci 164:803–813

    Article  Google Scholar 

  • Young IM, Crawford JW (2004) Interactions and self-organization in the soil-microbe complex. Science 304:1634–1637

    Article  Google Scholar 

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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.

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Correspondence to Anja Miltner.

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Miltner, A., Bombach, P., Schmidt-Brücken, B. et al. SOM genesis: microbial biomass as a significant source. Biogeochemistry 111, 41–55 (2012). https://doi.org/10.1007/s10533-011-9658-z

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