Abstract
Much has been learned about the microbial decomposition of plant litter, but relatively little is known about microbial contributions to litter and soil chemistry. We conducted a 3-year litterbag experiment and measured hydrolyzable amino acids (AA) and amino sugars (AS) to gain insights about microbial contributions to the chemical characteristics of decomposing litter and soil. Microscopic observations of hyphae were used to estimate fungal contributions to litter. The carbon (C)-normalized yields of AA and AS increased during decomposition along with nitrogen (N), indicating a shift in chemical characteristics from C-rich plant-derived biopolymers to N-rich, microbially-derived biochemicals. The contributions of fungal biomass to C and N were minor, but necromass of fungi as melanized and clamp-bearing hyphae increased during litter decomposition. Yields of glucosamine and galactosamine in litter approached those in microorganisms, particularly bacteria, suggesting major contributions of bacterial residues to litter during decomposition. The microbial contributions to decomposing litter were consistent with those observed in organic and mineral soils. Microorganisms play important roles in the organization and stabilization of soil organic matter as well as N immobilization and organic C preservation.
Similar content being viewed by others
Change history
19 January 2024
A Correction to this paper has been published: https://doi.org/10.1007/s10533-024-01118-2
Abbreviations
- AA:
-
Amino acid
- AS:
-
Amino sugar
- THAA:
-
Total hydrolyzable amino acid
- THAS:
-
Total hydrolyzable amino sugar
- GlcN:
-
Glucosamine
- GalN:
-
Galactosamine
- OC:
-
Organic carbon
References
Aber JD, Melillo JM (2001) Terrestrial ecosystems, 2nd edn. Academic Press, New York
Amelung W (2001) Methods using amino sugars as markers for microbial residues in soil. In: Lal R, Kimble JM, Follett RF, Stewart BA (eds) Assessment methods for soil carbon pools. Advances in soil science. CRC/Lewis Publishers, Boca Raton, pp 233–270
Amelung W (2003) Nitrogen biomarkers and their fate in soil. J Plant Nutr Soil Sci 166:677–686
Amelung W, Miltner A, Zhang X, Zech W (2001) Fate of microbial residues during litter decomposition as affected by minerals. Soil Sci 166:598–606
Amelung W, Brodowski S, Sandhage-Hofmann A, Bol R (2008) Combining biomarker with stable isotope analyses for assessing the transformation and turnover of soil organic matter. Adv Agron 100:155–250
Angers DA (1992) Changes in soil aggregation and organic carbon under corn and alfalfa. Soil Sci Soc Am J 56:1244–1249
Bååth E, Söderström B (1977) Mycelial lengths and fungal biomasses in some Swedish coniferous forest soils, with special reference to a pine forest in central Sweden. Technical Report. Swedish Coniferous Forest Project, Uppsala, pp 1–45
Bengtsson G, Bengtson P, Månsson KF (2003) Gross nitrogen mineralization-, immobilization-, and nitrification rates as a function of soil C/N ratio and microbial activity. Soil Biol Biochem 35:143–154
Benner R, Kaiser K (2003) Abundance of amino sugars and peptidoglycan in marine particulate and dissolved organic matter. Limnol Oceanogr 48:118–128
Berg B, McClaugherty C (2008) Plant litter, decomposition, humus formation, carbon sequestration, 2nd edn. Springer, Berlin
Bondietti E, Martin JP, Haider K (1972) Stabilization of amino sugar units in humic type polymers. Soil Sci Soc Am J 36:597–602
Calderoni G, Schnitzer M (1984) Nitrogen distribution as a function of raiodcarbon age in Paleosol humic acids. Org Geochem 5:203–209
Chantigny MH, Angers DA, Prévost D, Vézina L-P, Cahlifour F-P (1997) Soil aggregation and fungal and bacterial biomass under annual and perennial cropping systems. Soil Sci Soc Am J 61:262–267
Chenu C, Cosentino D (2011) Microbial regulation of soil structural dynamics. In: Ritz K, Young I (eds) The architecture and biology and soils: life in inner space. CAB International, London, pp 37–70
Cotrufo MF, Wallenstein MD, Boot CM, Denef K, Paul E (2013) The Microbial Efficiency-Matrix Stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: Do labile plant inputs form stable soil organic matter? Global Change Biol. doi:10.1111/gcb.12113
Cowie GL, Hedges JI (1994) Biochemical indicators of diagenetic alteration in natural organic-matter mixtures. Nature 369:304–307
Dauwe B, Middelburg JJ, Herman PMJ, Heip CHR (1999) Linking diagenetic alteration of amino acids and bulk organic matter reactivity. Limnol Oceanogr 44:1809–1814
Ding X, Zhang X, He H, Xie H (2010) Dynamics of soil amino sugar pools during decomposition processes of corn residues as affected by inorganic N addition. J Soil Sediment 10:758–766
Engelking B, Flessa H, Joergensen RG (2007) Shifts in amino sugar and ergosterol contents after addition of sucrose and cellulose to soil. Soil Biol Biochem 39:2111–2118
Ensminger L, Gieseking JE (1942) Resistance of clay-adsorbed proteins to proteolytic hydrolysis. Soil Sci 53:205–209
Fontaine S, Henault C, Aamor A, Bdioui N, Bloor JMG, Maire V, Mary B, Revaillot S, Maron PA (2011) Fungi mediate long term sequestration of carbon and nitrogen in soil through their priming effect. Soil Biol Biochem 43:86–96
Foster RC, Rovira AD, Cock TW (1983) Ultrastructure of the root-soil interface. American Phytopathological Society, St. Paul
Giroldo D, Vieira AAH (2002) An extracellular sulfated fucose-rich polysaccharide produced by a tropical strain of Cryptomonas obovata (Cryptophyceae). J Appl Phycol 14:185–191
Glaser B, Millar N, Blum H (2006) Sequestration and turnover of bacterial- and fungal- derived carbon in a temperate grassland soil under long-term elevated atmospheric pCO2. Global Change Biol 12:1521–1531
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
Hart SC, Nason GE, Myrold DD (1994) Dynamics of gross nitrogen transformations in an old-growth forest: the carbon connection. Ecology 75:880–891
He HB, Lia XB, Zhang W, Zhang XD (2011a) Differentiating the dynamics of native and newly immobilized amino sugars in soil frequently amended with inorganic nitrogen and glucose. Eur J Soil Sci 62:144–151
He H, Zhang W, Zhang X, Xie H, Zhuang J (2011b) Temporal responses of soil microorganisms to substrate addition as indicated by amino sugar differentiation. Soil Biol Biochem 43:1155–1161
Hsu P-H, Hatcher PG (2005) New evidence for covalent coupling of peptides to humic acids based on 2D NMR spectroscopy: a means for preservation. Geochim Cosmochim Acta 69:4521–4533
Iimura Y, Fujimoto M, Hirota M, Tamura K, Higashi T, Yonebayashi K, Fujitake N (2010) Effects of ecological succession on surface mineral horizons in Japanese volcanic ash soil. Geoderma 159:122–130
Joergensen RG, Wichern F (2008) Quantitative assessment of the fungal contribution to microbial tissue in soil. Soil Biol Biochem 40:2977–2991
Kaiser K, Benner R (2000) Determination of amino sugars in environmental samples with high salt content by high- performance anion-exchange chromatography and pulsed amperometric detection. Anal Chem 72:2566–2572
Kaiser K, Benner R (2008) Major bacterial contribution to the ocean reservoir of detrital organic carbon and nitrogen. Limnol Oceanogr 53:99–112
Kaiser K, Benner R (2009) Biochemical composition and size distribution of organic matter at the Pacific and Atlantic time-series stations. Mar Chem 113:63–77
Kato J, Hayasi I (2006) Quantitative analysis of a stand of Pinus densiflora undergoing succession to Quercus mongolica ssp. crispula: 1. A 31-year record of growth and population dynamics of the canopy trees. Ecol Res 21:503–509
Kawasaki N, Benner R (2006) Bacterial release of dissolved organic matter during cell growth and decline: molecular origin and composition. Limnol Oceanogr 51:2170–2180
Knicker H (2004) Stabilization of N-compounds in soil and organic matter rich sediments - What is the difference? Marine Chem 92:167–195
Knicker H (2011) Soil organic N—An under-rated player for C sequestration in soils? Soil Biol Biochem 43:1118–1129
Knicker H, Fründ R, Lüdemann H-D (1993) The chemical nature of nitrogen in soil organic matter. Naturwissenschaften 80:219–221
Knicker H, Schmidt MWI, Kögel-Knabner I (2000) Nature of organic nitrogen in fine particle size separates of sandy soils of highly industrialized areas as revealed by NMR spectroscopy. Soil Biol Biochem 32:241–252
Leinweber P, Schulten HR (2000) Nonhydrolyzable forms of soil organic nitrogen: extractability and composition. J Plant Nutr Soil Sci 163:433–439
Liang C, Balser TC (2011) Microbial production of recalcitrant organic matter in global soils: implications for productivity and climate policy. Nature Rev Microbiol 9:75
Liang C, Zhang X, Balser TC (2007) Net microbial amino sugars accumulation process in soil as influenced by different plant material inputs. Biol Fert Soils 44:1–7
Liang C, Cheng G, Wixon DL, Balser TC (2011) An absorbing Markov chain approach to understanding the microbial role in soil carbon stabilization. Biogeochemistry 106:303–309
Linhares LF, Martin JP (1978) Decomposition in soil of the humic acid-type polymers (melanins) of Eurotium echinulatum, Aspergillus glaucus sp. and other fungi. Soil Sci Soc Am J 42:738–743
Martens DA, Loeffelmann KL (2003) Soil amino acid composition quantified by acid hydrolysis and anion chromatography-pulsed amperometry. J Agr Food Chem 51:6521–6529
Martin JP, Haider K (1986) Influence of mineral colloids on turnover rates of soil organic carbon. In: Huang PM, Shnitzer M (eds) Interactions of soil minerals with natural organics and microbes, vol 17. SSSA Special Publication, Madison, pp 283–304
Marumoto T, Anderson JPE, Domsch KH (1982) Decomposition of 14C- and 15N-labelled microbial cells in soil. Soil Biol Biochem 14:461–467
Mengel K (1996) Turnover of organic nitrogen in soils and its availability to crops. Plant Soil 181:83–93
Mikutta R, Kaiser K, Dörr N, Vollmer A, Chadwick OA, Chorover J, Kramer MG, Guggenberger G (2010) Mineralogical impact on organic nitrogen across a long-term soil chronosequence (0.3–4100 kyr). Geochim Cosmochim Acta 74:2142–2164
Miltner A, Bombach P, Schmidt-Brücken B, Kästner M (2011) SOM genesis: microbial biomass as a significant source. Biogeochemistry. doi:10.1007/s10533-011-9658-z
Ogawa H, Amagai Y, Koike I, Kaiser K, Benner R (2001) Production of refractory dissolved organic matter by bacteria. Science 292:917–920
Ono Y (1998) A study on the initial decomposition process of needle litter in a Chamaecyparis obtusa forest. Masters Thesis, Kyoto University, Kyoto, Japan (in Japanese)
Osono T (2010) Decomposition of grass leaves by ligninolytic litter-decomposing fungi. Grassland Sci 56:31–36
Osono T, Takeda H (2001) Organic chemical and nutrient dynamics in decomposing beech leaf litter in relation to fungal ingrowth and succession during 3-year decomposition processes in a cool temperate deciduous forest in Japan. Ecol Res 16:649–670
Parsons JW (1981) Chemistry and distribution of amino sugars in soils and soil organisms. In: Paul EA, Ladd JN (eds) Soil Biochemistry, vol 5. Marcel Dekker, New York, pp 197–227
Paul EA, Clark FE (1989) Soil microbiology and biochemistry. Academic Press, New York
Reverter M, Lundh T, Lindberg JE (1997) Determination of free amino acids in pig plasma by precolumn derivatization with 6-N- aminoquinolyl-N-hydroxysuccinimidyl carbamate and high performance liquid chromatography. J Chromatogr B Biomed Sci Appl. 696((1):1–8
Rovira P, Kurz-Besson C, Hernández P, Coûteaux M–M, Vallejo VR (2008) Searching for an indicator of N evolution during organic matter decomposition based on amino acids behaviour: a study on litter layers of pine forests. Plant Soil 307:149–166
Saito T (1955) The significance of plate counts of soil fungi and the detection of their mycelia. Ecol Rev 14:69–74
Schäffer C, Messner P (2001) Glycobiology of surface layer proteins. Biochimie 83:591–599
Schmidt MWI, Knicker H, Hatcher PG, Kögel-Knabner I (1997) Improvement of 13C and 15N CPMAS NMR spectra of bulk soils, particle size fractions and organic material by treatment with 10% hydrofluoric acid. Eur J Soil Sci 48:319–328
Simpson AJ, Simpson MJ, Smith E, Kelleher BP (2007) Microbially derived inputs to soil organic matter: are current estimates too low? Environ Sci and Techonol 41:8070–8076
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
Smernik RJ, Baldock JA (2005) Does solid-state 15N NMR spectroscopy detect all soil organic nitrogen? Biogeochemistry 75:507–528
Solomon D, Fritzsche F, Tekalign M, Lehmann J, Zech W (2002) Soil organic matter composition in the Subhumid Ethiopian Highlands as influenced by deforestation and agricultural management. Soil Sci Soc Am J 66:68–82
Sutton R, Sposito G (2005) Molecular structure in soil humic substances: the new view. Environ Sci Technol 39:9009–9015
Swift MJ, Heal OW, Anderson JM (1979) Decomposition in terrestrial ecosystems. Studies in ecology, vol 5. University of California Press, Berkeley
Tisdall JM, Oades JM (1980) The management of ryegrass to stabilize aggregates of a red-brown earth. Aust J Soil Res 18:415–422
Tremblay L, Benner R (2006) Microbial contributions to N-immobilization and organic matter preservation in decomposing plant detritus. Geochim Cosmochim Acta 70:133–146
Wanek W, Mooshammer M, Blöchl A, Hanreich A, Richter A (2010) Determination of gross rates of amino acid production and immobilization in decomposing leaf litter by a novel 15N isotope pool dilution technique. Soil Biol Biochem 42:1293–1302
Acknowledgments
We thank Karl Kaiser and Mike Philben for analyzing C, N, and AA in several microorganisms and for assistance with AA and AS analyses. We also thank Yoko Morimoto, Ruth Flerus, Tomohiro Kasuga, Seiya Shiratori, Marin Otomichi, Hiroki Inoue, Hidetomo Iwano, Isao Kato, Hiroshi Yokota, and Teruo Matsunaka for support in the laboratory. This research was supported by grant from the Japanese Society for the Promotion of Science (No. 21710014) and by Grants-in-Aid to Cooperative Research from Rakuno Gakuen University (2008). Ronald Benner acknowledges support from NSF grant 0843417.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Kathleen Lohse
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Hobara, S., Osono, T., Hirose, D. et al. The roles of microorganisms in litter decomposition and soil formation. Biogeochemistry 118, 471–486 (2014). https://doi.org/10.1007/s10533-013-9912-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10533-013-9912-7