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Transformation of Low-Molecular Nitrogen-Containing Compounds in Soil Ya Eurasian Soil Science, Vol. 29, No. 12, 1996, pp. 1333–1341. Translated from Pochvovedenie, No. 12, 1996, pp. 1430–1439. Original Russian Text Copyright © 1996 by Kuzyakov. English Translation Copyright © 1996 by åÄàä ç‡Û͇ /Interperiodica Publishing (Russia). SOIL CHEMISTRY Transformation of Low-Molecular Nitrogen-Containing Compounds in Soil Ya. V. Kuzyakov Timiryazev Agricultural Academy, Timiryazevskii proezd 2, Moscow, 127550 Russia; Humboldt University, Berlin Received December 5, 1994; in final form, October 10, 1995 Abstract—A simple model is proposed to show the decomposition of low-molecular organic compounds in soil. The model permits us to estimate the rate of oxidation of different carbon atoms in amino acid molecules, the share of their use by microorganisms for anabolism, and the inclusion in humus, as well as the number of cycles oriented to microorganism renewal in the soil during the vegetation period. At initial stages of soil evo- lution, passive mechanisms (natural selection of heavily decomposed high-molecular components of plant res- idues) play an essential role in accumulation of humus substances. In the course of soil evolution, active mech- anisms assume ever greater importance (inclusion of low-molecular labile N-containing compounds). Changes in the mechanisms may be considered as an additional factor in the microorganism strategy to be adopted for succession in the ecosystem and as one of the indicators of soil transition from an inert to a bioinert system. INTRODUCTION pounds are decomposed enzymatically to organic oli- Organic matter of soil is essentially responsible for gomers and monomers—amino acid chains and amino sustainability of the balance of many nutrients and, in acids, nucleotides and nucleic bases, respectively. Part particular, carbon on the earth. The soil contains of these monomers come to the soil directly and 1.39 × 1018–1.48 × 1018 g of carbon, which corresponds undergo transformation characteristic to the given type to two-thirds of the whole carbon store in terrestrial of compounds and to the particular soil conditions. ecosystems [13, 51, 52, 54]. It exceeds that of living A comprehensive assessment of the reserves and sup- phytomass by 2–3 times [53] and is twice as much as ply of various nitrogen-containing components in soils the total carbon content in the atmosphere [43]. Pres- is given in a number of papers [5, 6, 9, 18, 20, 22]. ently, the content and many properties of inert soil com- The sequence and one possible scheme of the ponents, which comprise 90–95% of the total mass of decomposition processes of N-containing compounds organic soil substances, are adequately characterized. are considered in Fig. 1. The whole diversity of the nat- However, functioning and transformation of soil ural N-containing compounds can be combined into organic matter is substantially determined by labile several large groups according to the chemical charac- compounds—individual low-molecular organic com- teristics of their monomers. Protein compounds and pounds. The role of these substances in humus formation nucleic acids are attributed to the first two groups. has not been adequately investigated because of their low A special group is distinguished for humic substances, concentration in soil and rapid transformation. because these biopolymers are characterized by irregu- In the present work, the behavior of low-molecular lar structure and high diversity of their constituent organic N-containing compounds is characterized, and monomers. Humus nitrogen is represented by four their role in the formation and renewal of humus is con- major forms [58]: (1) nitrogen of the ammonium anion, sidered. (2) nitrogen of amino acids and aminosugars (hydrolyz- able by 6 N HCl), (3) nitrogen directly bound to aromatic MINERALIZATION nuclei (nonhydrolyzable by 6 N HCl), and (4) nitrogen of heterocycles (nonhydrolyzable by 6 N HCl). The In natural ecosystems, the primary reserve of nitro- presence of at least the second and fourth forms shows gen in soils is produced and then replenished mainly the possible genetic relations of humic substances with through immobilization of atmospheric nitrogen by free-living, associated, and symbiotic microorgan- protein compounds and nucleic acids. The next two isms. It makes up 10–70 kg/ha per year in mature soils groups are represented by nitrogen-containing com- [7, 24, 39]. In primitive soils, the fixation of molecular pounds—chlorophyll and chitin—with lower molecu- nitrogen is considerably lower owing to the lack of lar mass. available energy sources. Nitrogen-fixing bacteria After entering the soil, the high-molecular com- transform molecular nitrogen first to amino acids and pounds mentioned above are decomposed enzymati- then to high-molecular compounds (proteins) or, cally to their corresponding monomers: protein com- through the stage of nucleic bases, to RNA and DNA. pounds, to amino acids, and RNA and DNA, to nucle- After the bacteria die off, these high-molecular com- otides and nucleic bases. During decomposition of 1333 1334 KUZYAKOV Nucleic HUMUS Proteins Polymers acids D i Chitin v Chlorophyll R e a M Oligomers r t o s l e e i Nucleic Amino acids t bases o c u y Fragmental Amino sugars f ëé2 l Monomers o renewal ëé2 H2O p a f H2O A NH4 r r NH4 m (NH ) ëé s 2 2 o u (NH2)2ëé i n c b m s o e Chemically Biologically s a t s a a s n c e s c i s e d s Inorganic s products of decomposition ëé2 NH4 H O Slow2 Fast Rate of substances turnover Fig. 1. Scheme of transformation of organic N-containing compounds in soil. humic substances, the residues of amino acids and utilized in anabolism of microorganisms, while a small some amount of nucleic bases are eliminated from part of the nitrogen and carbon of amino acids is them [16]. In the cells of microorganisms, nucleic bases involved chemically in humus, at sites of previously are transformed primarily to amino acids: pyrimidine- eliminated less stable fragments [15, 23, 30, 46, 57]. ous, to β-alanine [34, 35], and purineous, to glycine during anaerobic decomposition and to urea during an As was shown earlier, amino acids play a key role in aerobic one [34]. (It should be mentioned, however, that the transformation of organic N-containing compounds at the decomposition of both nucleic bases and other in soils, which is why we shall consider mainly this nitrogen-containing organic compounds, the ammonia class of compounds, taking into account that at the groups are sequentially eliminated, and besides β-ala- same time amino acids are intermediate metabolites of nine and glycine, the final organic product of decomposi- other N-containing substances. tion of nucleic bases is urea [34, 35].) Chlorophyll is also The lower part of the scheme (Fig. 1), which decomposed through protoporphyrine to glycine [34]. describes the transformation of low-molecular N-con- Similar to other amino sugars, D-glucosamine pro- taining components in soil, can be simplified as a duced from chitin brings its amino group through tran- model (Fig. 2). Immediately after a low-molecular samination to glutamine [35]. organic compound (A) comes into the soil, some part of Hence, during decomposition, all natural organic it (H) is chemically included in humic substances. In N-containing compounds pass through the stage of the conditions of homogeneous media that occur in the amino acids independently of the type of nitrogen bind- absence of high local accumulations of microorganisms in ing in the initial compound, molecular mass, and chem- the decomposed material, the rate of the direct chemical ical and physical properties. All the diversity of N-con- incorporation of an individual compound considerably taining compounds is reduced to several amino acids exceeds that of its microbiological destruction [38, 56]. (glycine, alanine, and glutamine) with the amine as the The fragments incorporated in humus (Ah), as well as final form of organic-bound nitrogen before its complete the ones remaining in the soil solution (Af), are micro- mineralization. According to Knyazev (personal com- biologically utilized (Bf + Bh = Bio) at different rates munication, 1989), this sequence of natural destruction (g, a). As a result, a part of compound (Y) is utilized in of organic N-containing compounds in soils is named anabolism, while another one (1-Y) is oxidized to CO2. “amino acid funnel” (Fig. 1). At the final stage of min- Then the microorganisms continue either to consume eralization, about half of the amino acid carbon is enzy- new portions of entering compounds or to die off matically oxidized to carbon dioxide, and about one- accompanied by CO2 production at the rate b. A more third of the carbon and a major part of the nitrogen is exhaustive description of this model is given in [46]. EURASIAN SOIL SCIENCE Vol. 29 No. 12 1996 TRANSFORMATION OF LOW-MOLECULAR NITROGEN-CONTAINING COMPOUNDS 1335 The present model was described parametrically in a the laboratory for several low-molecular organic com- Af AfCO2 Y 1-Y pounds (alanine, glycine, glucose, urea), labeled with b 14C at different sites of the molecule in different soils: 1-H Bf BfCO2 A Bio b CO2 Bh soddy-podzolic with different humus content [46] and H BhCO2 sierozem with various levels of salinization [15]. The Y 1-Y parameters obtained characterize the ratio and rates in Ah AhCO2 the model (Fig. 2) and schemes of decomposition of g low-molecular organic compounds (Fig. 1) in the soils studied: Fig. 2. Scheme of decomposition of low-molecular organic (1) The initial chemical incorporation of the sec- compounds entering the soil (comments in the text). ond carbon atom of amino acids into humus makes up 25–35% of the inflow amount. For the carbon of a lier [47, 56].
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