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Sugars in Soil and Sweets for Microorganisms: Review of Origin, Content, Composition and Fate

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Sugars in Soil and Sweets for Microorganisms: Review of Origin, Content, Composition and Fate Soil Biology & Biochemistry 90 (2015) 87e100 Contents lists available at ScienceDirect Soil Biology & Biochemistry journal homepage: www.elsevier.com/locate/soilbio Review paper Sugars in soil and sweets for microorganisms: Review of origin, content, composition and fate * Anna Gunina a, b, , Yakov Kuzyakov a, c a Department of Agricultural Soil Science, Georg-August-University of Gottingen,€ Germany b Department of Soil Biology and Biochemistry, Dokuchaev Soil Science Institute, Russian Federation c Department of Soil Science of Temperate Ecosystems, Georg-August-University of Gottingen,€ Germany article info abstract Article history: Sugars are the most abundant organic compounds in the biosphere because they are monomers of all Received 21 April 2015 polysaccharides. We summarize the results of the last 40 years on the sources, content, composition and Received in revised form fate of sugars in soil and discuss their main functions. We especially focus on sugar uptake, utilization 24 July 2015 and recycling by microorganisms as this is by far the dominating process of sugar transformation in soil Accepted 25 July 2015 compared to sorption, leaching or plant uptake. Moreover, sugars are the most important carbon (C) and Available online 8 August 2015 energy source for soil microorganisms. Two databases have been created. The 1st database focused on the contents of cellulose, non-cellulose, Keywords: Carbohydrates in soil hot-water and cold-water extractable sugars in soils (348 data, 32 studies). This enabled determining the Glucose primary (plant-derived) and secondary (microbially and soil organic matter (SOM) derived) sources of Microbial utilization carbohydrates in soil based on the galactose þ mannose/arabinose þ xylose (GM/AX) ratio. The 2nd 13 14 Biochemical transformation database focused on the fate of sugar C in soils (734 data pairs, 32 studies using Cor C labeled sugars). Low molecular weight organics 13Cand14C dynamics enabled calculating the: 1) initial rate of sugar mineralization, 2) mean residence time (MRT) of C of the applied sugars, and 3) MRT of sugar C incorporated into 3a) microbial biomass and 3b) SOM. The content of hexoses was 3e4 times higher than pentoses, because hexoses originate from plants and microorganisms. The GM/AX ratio of non-cellulose sugars revealed a lower contribution of hexoses in cropland and grassland (ratio 0.7e1) compare to forest (ratio 1.5) soils. À 13C and 14C studies showed very high initial rate of glucose mineralization (1.1% min 1) and much higher rate of sugars uptake by microorganisms from the soil solution. Considering this rate along with the glucose input from plants and its content in soil solution, we estimate that only about 20% of all sugars in soil originate from the primary source e decomposition of plant litter and rhizodeposits. The remaining 80% originates from the secondary source e microorganisms and their residues. The esti- mated MRT of sugar C in microbial biomass was about 230 days, showing intense and efficient internal recycling within microorganisms. The assessed MRT of sugar C in SOM was about 360 days, reflecting the considerable accumulation of sugar C in microbial residues and its comparatively slow external recycling. The very rapid uptake of sugars by microorganisms and intensive recycling clearly demonstrate the importance of sugars for microbes in soil. We speculate that the most important functions of sugars in soil are to maintain and stimulate microbial activities in the rhizosphere and detritusphere leading to mobilization of nutrients by accelerated SOM decomposition e priming effects. We conclude that the actual contribution of sugar C (not only whole sugar molecules, which are usually determined) to SOM is much higher than the 10 ± 5% commonly measured based on their content. © 2015 Elsevier Ltd. All rights reserved. 1. Introduction e why sugars? * Corresponding author. Department of Agricultural Soil Science, Georg-August- Sugars are the most abundant organic compounds in the University of Gottingen,€ Büsgenweg 2, 37077 Gottingen,€ Germany. Tel.: þ49 biosphere because they are the basic components of all poly- 55139 33505. saccharides: cellulose, hemicellulose (polyoses), starch, pectin, E-mail address: [email protected] (A. Gunina). http://dx.doi.org/10.1016/j.soilbio.2015.07.021 0038-0717/© 2015 Elsevier Ltd. All rights reserved. 88 A. Gunina, Y. Kuzyakov / Soil Biology & Biochemistry 90 (2015) 87e100 fructanes, and glucanes as well as of chitin (consists from amino - estimating annual sugar production and its microbial recycling sugars) (Kogel-Knabner,€ 2002). Considering the dominance of in soil based on the cellulose and non-cellulose sugar content polysaccharides in plants (50e70% of dry mass), they are the most and their decomposition rates; important primarily input of organic carbon (C) in soil. With a mean - evaluating the role of sugars for aggregates formation, SOM residence time (MRT) of few weeks to months (Martin et al., 1974), accumulation and priming effects; and polysaccharides are decomposed by exoenzymes (cellulases, xyla- - providing an overall scheme of sugar transformation and recy- nases, glucosidases, hydrolases, chitinases) to oligo- and mono- cling in soil. saccharides (termed sugars). Cellulose is the most abundant biopolymer and, consequently, glucose is the most abundant It is beyond the scope of this review to provide methodological monomer released by its decomposition in soil. Sugars therefore details of carbohydrate extraction, purification and analysis dominate within low molecular weight organic substances (Cheshire, 1979; Amelung et al., 1996). (LMWOS) in all soils and affect various processes not only as a chemical compound group per se, but especially as C and an energy 2. Materials and methods source for microorganisms. All oligo- and monosaccharides are soluble, easily available for We use the term carbohydrates when we refer to mono- microorganisms, and are captured rapidly by microbes and used for saccharides, disaccharides, oligosaccharides and polysaccharides maintenance (both respiration and anabolism), growth and C without their differentiation. In some literature, ‘saccharides’ are storage. Because sugars dominate LMWOS and cell metabolism, used as a synonym of carbohydrates. For specification we use the their role for microbial life in soil cannot be overestimated. For respective terms (i.e. polysaccharides, monosaccharides, etc.). The example, sugar concentration in soil solution stimulates the tran- term ‘sugars’ is used for mono- and disaccharides. sition of microorganisms from dormant or potentially active to the For the review preparation, two sets of literature data were active stages (Blagodatskaya and Kuzyakov, 2013). This activation collected: 1) content and concentration of various groups of sugars contributes further to exoenzyme production, thus accelerating the in soils and soil solutions, respectively and 2) mineralization rates decomposition of soil organic matter (SOM) and the release of of sugars in soil and their participation in various fluxes including stored nutrients, mainly N, P and S. This makes sugars the most incorporation into microbial biomass (MB) and SOM. common and no doubt very efficient substance group to induce priming effects (Kuzyakov, 2010). Another important and frequently neglected relevance of car- 2.1. Sugar content and composition bohydrates is their contribution to aggregates formation e and thus to the formation of soils from parent materials. Poly-, oligo- and The first database is focused on sugar contents in soils and soil monosaccharides become sticky with increasing the concentra- solutions and contains 348 data from 32 studies. Articles were tions and drying, and bind mineral and organic particles, resulting searched in the Web of Knowledge and Scopus using the key in microaggregates formation (Oades, 1984; Six et al., 1999). Even words: “soil*” AND “carbohydrate*”, “sugar content” AND “soil*”. the role of particulate organic matter (POM) for aggregates for- Information was collected on total sugars as well as content of in- mation is mainly connected with the release of polysaccharides and dividual sugars extracted by various procedures. Based on the sugars due to POM decomposition. extractants and pre-treatments (e.g. various hydrolysis procedures, Within the three most abundant classes of LMWOS in soil e temperature and soil:solution ratios), all sugars were divided into sugars, carboxylic acids and amino acids e the concentration of the following groups: 1) total, 2) non-cellulose, 3) hot-water sugars is about 2e3 times higher than both other classes. The fate extractable and 4) cold-water extractable. The specific soil param- and significance of other LMWOS in soil were intensively reviewed eters (C and N contents, pH, texture), land use, experiment condi- earlier: carboxylic acids (Jones, 1998) and amino acids (Jones et al., tions, depth of soil sampling and climate were included in the 2005), and we refer the readers to these excellent reviews for database. Only articles with total C in soil <6% of dry weight were further information. No overview, however, focused on the included in order to consider mineral soils only. Soil texture was composition, fate and relevance of sugars in soil. The sole detailed classified according to clay content as: clayey (>25% clay), loamy review about carbohydrates in soils was published about 40 years (15e25% clay) and sandy (10e15% clay). We found no carbohydrate ago (Cheshire, 1979) and focused
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