Abstract
The number of studies on priming effects (PE) in soil has strongly increased during the last years. The information regarding real versus apparent PE as well as their mechanisms remains controversial. Based on a meta-analysis of studies published since 1980, we evaluated the intensity, direction, and the reality of PE in dependence on the amount and quality of added primers, the microbial biomass and community structure, enzyme activities, soil pH, and aggregate size. The meta-analysis allowed revealing quantitative relationships between the amounts of added substrates as related to microbial biomass C and induced PE. Additions of easily available organic C up to 15% of microbial biomass C induce a linear increase of extra CO2. When the added amount of easily available organic C is higher than 50% of the microbial biomass C, an exponential decrease of the PE or even a switch to negative values is often observed. A new approach based on the assessment of changes in the production of extracellular enzymes is suggested to distinguish real and apparent PE. To distinguish real and apparent PE, we discuss approaches based on the C budget. The importance of fungi for long-term changes of SOM decomposition is underlined. Priming effects can be linked with microbial community structure only considering changes in functional diversity. We conclude that the PE involves not only one mechanism but a succession of processes partly connected with succession of microbial community and functions. An overview of the dynamics and intensity of these processes as related to microbial biomass changes and C and N availability is presented.
Similar content being viewed by others
References
Anderson JPE, Domsch KH (1978) A physiological method for the quantitative measurement of microbial biomass in soils. Soil Biol Biochem 10:215–221
Asmar F, Eiland F, Nielsen NE (1994) Effect of extracellular-enzyme activities on solubilization rate of soil organic nitrogen. Biol Fertil Soils 17:32–38
Bastias BA, Anderson IC, Xuc Z, Cairney JWG (2007) RNA- and DNA-based profiling of soil fungal communities in a native Australian eucalypt forest and adjacent Pinus elliotti plantation. Soil Biol Biochem 39:3108–3114
Baudoin E, Benizri E, Guckert A (2003) Impact of artificial root exudates on the bacterial community structure in bulk soil and maize rhizosphere. Soil Biol Biochem 35:1183–1192
Bell JM, Smith JL, Bailey VL, Bolton H (2003) Priming effect and C storage in semi-arid no-till spring crop rotations. Biol Fertil Soils 37:237–244
Billes G, Bottner P, Gandaisriollet N (1988) Effect of grass roots on soil–nitrogen net mineralization. Revue D Ecologie Et De Biologie Du Sol 25:261–277
Blagodatskaya EV, Anderson T-H (1998) Interactive effects of pH and substrate quality on the fungal-to-bacteria ratio and QCO2 of microbial communities in forest soils. Soil Biol Biochem 30:1269–1274
Blagodatskaya EV, Blagodatsky SA, Anderson T-H, Kuzyakov Y (2007) Priming effects in Chernozem induced by glucose and N in relation to microbial growth strategies. Appl Soil Ecol 37:95–105
Bolton H, Elliott LF, Papendick RI, Bezdicek DF (1985) Soil microbial biomass and selected soil enzyme-activities—effect of fertilization and cropping practices. Soil Biol Biochem 17:297–302
Brant JB, Sulzman EW, Myrold DD (2006) Microbial community utilization of added carbon substrates in response to long-term carbon input manipulation. Soil Biol Biochem 38:2219–2232
Brookes PC, Ocio JA, Wu J (1990) The soil microbial biomass: its measurements, properties and role in soil nitrogen and carbon dynamics following substrate incorporation. Soil Microorganisms 35:39–51
Burmolle M, Hansen LH, Oregaard G, Sorensen SJ (2003) Presence of N-acyl homoserine lactones in soil detected by a whole-cell biosensor and flow cytometry. Microbial Ecology 45:226–236
Cardon ZG (1996) Influence of rhizodeposition under elevated CO2 on plant nutrition and soil organic matter. Plant Soil 187:277–288
Carreiro MM, Sinsabaugh RL, Repert DA, Parkhurst DF (2000) Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology 81:2359–2365
Chander K, Goyal S, Mundra MC, Kapoor KK (1997) Organic matter, microbial biomass and enzyme activity of soils under different crop rotations in the tropics. Biol Fertil Soils 24:306–310
Chaves B, Opoku A, De Neve S, Boeckx P, Van Cleemput O, Hofman G (2006) Influence of DCD and DMPP on soil N dynamics after incorporation of vegetable crop residues. Biol Fertil Soils 43:62–68
Cheng WX (1999) Rhizosphere feedbacks in elevated CO2. Tree Physiology 19:313–320
Cheng WX, Coleman DC (1990) Effect of living roots on soil organic-matter decomposition. Soil Biol Biochem 22:781–787
Cheng W, Kuzyakov Y (2005) Root effects on soil organic matter decomposition. In: Wright S, Zobel R (eds) Roots and soil management: interactions between roots and the soil. agronomy monograph No. 48. ASA, Madison, pp 119–143
Conde E, Cardenas M, Ponce-Mendoza A, Luna-Guido ML, Cruz-Mondragon C, Dendooven L (2005) The impacts of inorganic nitrogen application on mineralization of C-14-labelled maize and glucose, and on priming effect in saline alkaline soil. Soil Biol Biochem 37:681–691
Dalenberg JW, Jager G (1981) Priming effect of small glucose additions to 14C-labeled soil. Soil Biol Biochem 13:219–223
Dalenberg JW, Jager G (1989) Priming effect of some organic additions to C-14-labeled soil. Soil Biol Biochem 21:443–448
De Neve S, Saez SG, Daguilar BC, Sleutel S, Hofman G (2004) Manipulating N mineralization from high N crop residues using on- and off-farm organic materials. Soil Biol Biochem 36:127–134
De Nobili M, Contin M, Mondini C, Brookes PC (2001) Soil microbial biomass is triggered into activity by trace amounts of substrate. Soil Biol Biochem 33:1163–1170
Degens B, Sparling G (1996) Changes in aggregation do not correspond with changes in labile organic C fractions in soil amended with C-14-glucose. Soil Biol Biochem 28:453–462
Denef K, Six J, Bossuyt H, Frey S, Elliott E, Merckx R, Paustian K (2001) Influence of dry–wet cycles on the interrelationship between aggregate, particulate organic matter, and microbial community dynamics. Soil Biol Biochem 33:1599–1611
Deng SP, Tabatabai MA (1996) Effect of tillage and residue management on enzyme activities in soils.1. Amidohydrolases. Biol Fertil Soils 22:202–207
Falchini L, Naumova N, Kuikman PJ, Bloem J, Nannipieri P (2003) CO2 evolution and denaturing gradient gel electrophoresis profiles of bacterial communities in soil following addition of low molecular weight substrates to simulate root exudation. Soil Biol Biochem 35:775–782
Fontaine S, Barot S (2005) Size and functional diversity of microbe populations control plant persistence and long-term soil carbon accumulation. Ecol Lett 8:1075–1087
Fontaine S, Mariotti A, Abbadie L (2003) The priming effect of organic matter: a question of microbial competition? Soil Biol Biochem 35:837–843
Fontaine S, Bardoux G, Abbadie L, Mariotti A (2004) Carbon input to soil may decrease soil carbon content. Ecol Lett 7:314–320
Fontaine S, Barot S, Barre P, Bdioui N, Mary B, Rumpel C (2007) Stability of organic carbon in deep soil layers controlled by fresh carbon supply. Nature 450:277–280
Freeman C, Liska G, Ostle NJ, Jones SE, Lock MA (1995) The use of fluorogenic substrates for measuring enzyme-activity in peatlands. Plant Soil 175:147–152
Gioacchini P, Nastri A, Marzadori C, Giovannini C, Antisari LV, Gessa C (2002) Influence of urease and nitrification inhibitors on N losses from soils fertilized with urea. Biol Fertil Soils 36:129–135
Girvan MS, Bullimore J, Ball AS, Pretty JN, Osborn AM (2004) Responses of active bacterial and fungal communities in soils under winter wheat to different fertilizer and pesticide regimens. Appl Environ Microbiol 70:2692–2701
Gray EJ, Smith DL (2005) Intracellular and extracellular PGPR: commonalities and distinctions in the plant–bacterium signaling processes. Soil Biol Biochem 37:395–412
Guggenberger G, Elliott ET, Frey SD, Six J, Paustian K (1999) Microbial contributions to the aggregation of a cultivated grassland soil amended with starch. Soil Biol Biochem 31:407–419
Hamer U, Marschner B (2005) Priming effects in different soil types induced by fructose, alanine, oxalic acid and catechol additions. Soil Biol Biochem 37:445–454
Helal HM, Sauerbeck DR (1984) Influence of plant–roots on c and p metabolism in soil. Plant Soil 76:175–182
Hopkins DW, Sparrow AD, Elberling B, Gregorich EG, Novis PM, Greenfield LG, Tilston EL (2006) Carbon, nitrogen and temperature controls on microbial activity in soils from an Antarctic dry valley. Soil Biol Biochem 38:3130–3140
Jenkinson DS, Fox RH, Rayner JH (1985) Interactions between fertilizer nitrogen and soil nitrogen—the so-called ‘priming’ effect. J Soil Sci 36:425–444
Johnsen K, Jacobsen CS, Torsvik V, Sørensen J (2001) Pesticide effects on bacterial diversity in agricultural soils—a review. Biol Fertil Soils 33:443–453
Kandeler E (2007) Physiological and biochemical methods for studying soil biota and their function. In: Paul E (eds) Soil microbiology, ecology, and biochemistry. Elsevier, Amsterdam, pp 53–83
Kandeler E, Eder G, Sobotik M (1994) Microbial biomass, N mineralization, and the activities of various enzymes in relation to nitrate leaching and root distribution in a slurry-amended grassland. Biol Fertil Soils 18:7–12
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
Klose S, Tabatabai MA (2002) Response of glycosidases in soils to chloroform fumigation. Biol Fertil Soils 35:262–269
Klose S, Moore JM, Tabatabai MA (1999) Arylsulfatase activity of microbial biomass in soils as affected by cropping systems. Biol Fertil Soils 29:46–54
Kramer C, Gleixner G (2006) Variable use of plant- and soil-derived carbon by microorganisms in agricultural soils. Soil Biol Biochem 38:3267–3278
Krsek M, Gaze WH, Morris NZ, Wellington EMH (2006) Gene detection, expression and related enzyme activity in soil. In: Nannipieri P, Smalla K (eds) Nucleic acids and proteins in soil, vol. 8. Springer-Verlag, Berlin Heidelberg New york, pp 217–255
Kuzyakov Y (2002) Review: Factors affecting rhizosphere priming effects. J Plant Nutr Soil Sci 165:382–396
Kuzyakov Y, Bol R (2006) Sources and mechanisms of priming effect induced in two grassland soils amended with slurry and sugar. Soil Biol Biochem 38:747–758
Kuzyakov Y, Friedel JK, Stahr K (2000) Review of mechanisms and quantification of priming effects. Soil Biol Biochem 32:1485–1498
Kuzyakov Y, Shevtzova E, Pustovoytov K (2006) Carbonate re-crystallization in soil revealed by C-14 labeling: Experiment, model and significance for paleo-environmental reconstructions. Geoderma 131:45–58
Landi L, Valori F, Ascher J, Renella G, Falchini L, Nannipieri P (2006) Root exudate effects on the bacterial communities, CO2 evolution, nitrogen transformations and ATP content of rhizosphere and bulk soils. Soil Biol Biochem 38:509–516
Lazazzera BA (2000) Quorum sensing and starvation: signals for entry into stationary phase. Curr Opin Microbiol 3:177–182
Liljeroth E, Kuikman P, Vanveen JA (1994) Carbon translocation to the rhizosphere of maize and wheat and influence on the turnover of native soil organic-matter at different soil–nitrogen levels. Plant Soil 161:233–240
Little AEF, Robinson CJ, Peterson SB, Raffa KF, Handelsman J (2008) Rules of engagement: interspecies interactions that regulate microbial communities. Annu Rev Microbiol 62:375–401
Luna-Guido ML, Beltran-Hernandez RI, Dendooven L (2001) Dynamics of C-14-labelled glucose in alkaline saline soil. Soil Biol Biochem 33:707–719
Lundquist E, Jackson L, Scow K, Hsu C (1999) Changes in microbial biomass and community composition, and soil carbon and nitrogen pools after incorporation of rye into three California agricultural soils. Soil Biol Biochem 31:221–236
Lynch JM, Benedetti A, Insam H, Nuti MP, Smalla K, Torsvik V, Nannipieri P (2004) Microbial diversity in soil: ecological theories, the contribution of molecular techniques and the impact of transgenic plants and transgenic microorganisms. Biol Fertil Soils 40:363–385
Marinari S, Masciandaro G, Ceccanti B, Grego S (2000) Influence of organic and mineral fertilisers on soil biological and physical properties. Bioresource Technol 72:9–17
Martin-Olmedo P, Rees RM, Grace J (2002) The influence of plants grown under elevated CO2 and N fertilization on soil nitrogen dynamics. Glob Chang Biol 8:643–657
Marxsen J, Witzel KP (1991) Significance of extracellular enzymes for organic matter degradation and nutrient regeneration in small streams. Springer, New York
Miller M, Palojarvi A, Rangger A, Reeslev M, Kjoller A (1998) The use of fluorogenic substrates to measure fungal presence and activity in soil. Appl Environ Microbiol 64:613–617
Mondini C, Cayuela ML, Sanchez-Monedero MA, Roig A, Brookes PC (2006) Soil microbial biomass activation by trace amounts of readily available substrate. Biol Fertil Soils 42:542–549
Nannipieri P (2006) Role of stabilized enzymes in microbial ecology and enzyme extraction from soil with potential applications in soil proteomics. In: Nannipieri P, Smalla K (eds) Nucleic acids and proteins in soil, vol. 8. Springer-Verlag, Berlin Heidelberg New york, pp 217–255
Nannipieri P, Ceccanti B, Cervelli S, Sequi P (1978) Stability and kinetic properties of humus-urease complexes. Soil Biol Biochem 10:143–147
Nannipieri P, Muccini L, Ciardi C (1983) Microbial biomass and enzyme activities: production and persistence. Soil Biol Biochem 15:679–685
Nannipieri P, Kandeler E, Ruggiero P (2002) Enzyme activities and microbiological and biochemical processes in soil. In: Buns RG, Dick RP (eds) Enzymes in the environment. Activity, ecology and applications. Marcel, New York, pp 1–33
Nannipieri P, Ascher J, Ceccherini MT, Loretta L, Giacomo P, Giancarlo R (2003) Microbial diversity and soil functions. Eur J Soil Sci 54:655–670
Niklaus PA, Falloon P (2006) Estimating soil carbon sequestration under elevated CO2 by combining carbon isotope labelling with soil carbon cycle modelling. Glob Chang Biol 12:1909–1921
Ohm H, Hamer U, Marschner B (2007) Priming effects in soil size fractions of a podzol Bs horizon after addition of fructose and alanine. Z PflanzenernaÉhr. Bodenkd 170:551–559
Panikov NS (1995) Microbial growth kinetics. Chapman & Hall, London
Parham JA, Deng SP (2000) Detection, quantification and characterization of b-glucosaminidase activity in soil. Soil Biol Biochem 32:1183–1190
Paul EA, Clark FE (1989) Soil microbiology and biochemistry. Academic, San Diego
Pennanen T, Caul S, Daniell TJ, Griffiths BS, Ritz K, Wheatley RE (2004) Community-level responses of metabolically-active soil microorganisms to the quantity and quality of substrate inputs. Soil Biol Biochem 36:841–848
Perelo LW, Munch JC (2005) Microbial immobilisation and turnover of C-13 labelled substrates in two arable soils under field and laboratory conditions. Soil Biol Biochem 37:2263–2272
Raffa RB, Iannuzzo JR, Levine DR, Saeid KK, Schwartz RC, Sucic NT, Terleckyj OD, Young JM (2005) Bacterial communication (“quorum sensing”) via ligands and receptors: a novel pharmacologic target for the design of antibiotic drugs. J Pharmacol Exp Ther 312:417–423
Renella G, Mench M, Landi L, Nannipieri P (2005) Microbial activity and hydrolase synthesis in long-term Cd-contaminated soils. Soil Biol Biochem 37:133–139
Sallih Z, Bottner P (1988) Effect of wheat (Triticum–Aestivum) roots on mineralization rates of soil organic-matter. Biol Fertil Soils 7:67–70
Santruckova H, Picek T, Tykva R, Simek M, Pavlu B (2004) Short-term partitioning of C-14-[U]-glucose in the soil microbial pool under varied aeration status. Biol Fertil Soils 40:386–392
Schimel JP, Weintraub MN (2003) The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem 35:549–563
Schneckenberger K, Demin D, Stahr K, Kuzyakov Y (2008) Microbial utilization and mineralization of [14C]glucose added in six orders of concentration to soil. Soil Biol Biochem 40:1981–1988
Schubert WJ (1965) Lignin biochemistry. Academic, New York
Shackle V, Freeman C, Reynolds B (2006) Exogenous enzyme supplements to promote treatment efficiency in constructed wetlands. Sci Total Environ 361:18–24
Shen J, Bartha R (1997) Priming effect of glucose polymers in soil-based biodegradation tests. Soil Biol Biochem 29:1195–1198
Six J, Jastrow J (2002) Organic matter turnover. Marcel Dekker, New York
Skujins JJ (1976) Extracellular enzymes in soil. CRC Crit Rev Microbiol 4:383–421
Sowerby A, Emmett B, Beier C, Tietema A, Penuelas J, Estiarte M, Van Meeteren MJM, Hughes S, Freeman C (2005) Microbial community changes in heathland soil communities along a geographical gradient: interaction with climate change manipulations. Soil Biol Biochem 37:1805–1813
Sparling GP, Fermor TR, Wood DA (1982) Measurement of the microbial biomass in composted wheat straw, and the possible contribution of the biomass to the nutrition of Agaricus bisporus. Soil Biol Biochem 14:609–611
Stenstrom J, Svensson K, Johansson M (2001) Reversible transition between active and dormant microbial states in soil. Fems Microbiol Ecol 36:93–104
Stevenson FJ, Cole MA (1999) Cycles of soil: carbon, nitrogen, phosphorus, sulfur, micronutrients. Wiley, New York
vanGinkel JH, Gorissen A, vanVeen JA (1997) Carbon and nitrogen allocation in Lolium perenne in response to elevated atmospheric CO2 with emphasis on soil carbon dynamics. Plant Soil 188:299–308
Vong PC, Dedourge O, Lasserre-Joulin F, Guckert A (2003) Immobilized-S, microbial biomass-S and soil arylsulfatase activity in the rhizosphere soil of rape and barley as affected by labile substrate C and N additions. Soil Biol Biochem 35:1651–1661
Waldrop MP, Firestone MK (2004) Microbial community utilization of recalcitrant and simple carbon compounds: impact of oak-woodland plant communities. Oecologia 138:275–284
Wang YJ, Leadbetter JR (2005) Rapid acyl-homoserine lactone quorum signal biodegradation in diverse soils. Appl Environ Microbiol 71:1291–1299
Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–346
Wu J, Brookes PC, Jenkinson DS (1993) Formation and destruction of microbial biomass during the decomposition of glucose and ryegrass in soil. Soil Biol Biochem 25:1435–1441
Xue JM, Sands R, Clinton PW, Payn TW, Skinner MF (2003) Carbon and net nitrogen mineralisation in two forest soils amended with different concentrations of biuret. Soil Biol Biochem 35:855–866
Zyakun AM, Dilly O (2005) Use of carbon isotope composition for characterization of microbial activity in arable soils. Appl Biochem Microbiol 41:512–520
Acknowledgments
This research was supported by the European Commission (Marie Curie IIF program, project MICROSOM) for Evgenia Blagodatskaya and by the Russian Foundation for Basic Researches (Project No. 06-04-48756). We are highly indebted to Dr. Sergey Blagodatsky for helpful comments and to Editor-in-Chief Professor Paolo Nannipieri and Review Editor Professor Hans Van Veen for the invitation to prepare this review. We thank two anonymous reviewers for substantial improvement of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Blagodatskaya, Е., Kuzyakov, Y. Mechanisms of real and apparent priming effects and their dependence on soil microbial biomass and community structure: critical review. Biol Fertil Soils 45, 115–131 (2008). https://doi.org/10.1007/s00374-008-0334-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00374-008-0334-y