Abstract
The soil microbial biomass survives as a largely dormant population for long periods without fresh substrates, depending for growth upon a rapid uptake of substrates when they become available. Currently, little investigation has been made into the mechanisms involved in the transition from dormancy to activity. We found that additions of trace amounts of different simple and complex substrates (glutamic acid, amino acids mixture, glucose, protein hydrolysates, carbohydrates, compost extract), even at very low application rates (5-μg C g−1 soil), caused an immediate and significant activation (measured as increased CO2-C evolved) of the soil microbial biomass. The different substrates caused different intensities of respiration response, which were related to the substrates’ composition, complexity, and degradability. The difference between the CO2-C evolved from the amended soil minus that evolved from a similarly incubated but non-amended soil ranged from 80 to 160% of the humified carbon C added as substrate, with most of the substrates causing a positive priming effect, in agreement with previous findings. The activation ended after 5–70 h, depending on the substrate, but the microbial biomass could be reactivated with further additions. It seems that the microbial biomass first responds to traces of substrate by increasing its metabolic activity in anticipation of a larger ‘food event’. Overall, these results indicate that soil micro-organisms have evolved metabolic and physiological strategies that allow them to survive and growth in the generally poor-substrate soil environment.
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References
Amato M, Ladd JN (1988) Assay for microbial biomass based on ninhydrin-reactive nitrogen in extracts of fumigated soils. Soil Biol Biochem 20:107–114
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
Bremer E, Kuikman P (1994) Microbial utilization of 14C[U]glucose in soil is affected by the amount and timing of glucose additions. Soil Biol Biochem 26:511–517
Brookes PC, Newcombe AD, Jenkinson DS (1987) Adenylate energy charge measurements in soil. Soil Biol Biochem 19:211–217
Brookes PC, Tate KR, Jenkinson DS (1983) The adenylate energy charge of the soil microbial biomass. Soil Biol Biochem 15:9–16
Clements MO, Foster SJ (1998) Starvation recovery of Staphylococcus aureus 8325-4. Microbiol 144:1755–1763
Contin M, Todd A, Brookes PC (2001) The ATP concentration in the soil microbial biomass. Soil Biol Biochem 33:701–704
Dalenberg JW, Jager G (1989) Priming effect of some organic additions to 14C-labelled soil. Soil Biol Biochem 21:443–448
Degens BP (1998) Microbial functional diversity can be influenced by the addition of simple organic substrates to soil. Soil Biol Biochem 30:1981–1988
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
Eiler A, Langenheder S, Bertilsson S, Tranvik LJ (2003) Heterotrophic bacterial growth efficiency and community structure at different natural organic carbon concentrations. Appl Environ Microbiol 69:3701–3709
Eivazi F, Tabatabai MA (1988) Glucosidases and galactosidases in soils. Soil Biol Biochem 20:601–606
Falchini L, Naumova N, Kuikman PJ, Bloem J, Nannipieri P (2003) CO2 evolution and denaturing gradient electrophoresis profiles of bacterial communities in soil following addition of low molecular weight substrates to stimulate root exudation. Soil Biol Biochem 36:775–782
Flardh K, Kjelleberg S (1994) Glucose upshift of carbon-starved marine Vibrio sp. strain S14 causes amino acid starvation and induction of the stringent response. J Bacteriol 176:5897–5903
Fontaine S, Bardoux G, Benest D, Verdier B, Mariotti A, Abbadie L (2004) Mechanisms of the priming effect in a savannah soil amended with cellulose. Soil Sci Soc Am J 68:125–131
Fontaine S, Mariotti A, Abbadie L (2003) The priming effect of organic matter: a question of microbial competition? Soil Biol Biochem 35:837–843
Geller A (1986) Comparison of mechanism enhancing biodegradability of refractory lake water constituents. Limnol Oceanogr 31:755–764
Griffiths BS, Ritz K, Ebblewhite N, Dobson G (1998) Soil microbial community structure: effects of substrate loading rates. Soil Biol Biochem 31:145–153
Hamer U, Marschner B (2005a) Priming effects in soils after combined and repeated substrate additions. Geoderma 128:38–51
Hamer U, Marschner B (2005b) Priming effects in different soil types induced by fructose, alanine, oxalic acid and catechol additions. Soil Biol Biochem 37:445–454
Jenkinson DS (1988) Determination of microbial biomass carbon and nitrogen in soil. In: Wilson JR (ed) Advances in nitrogen cycling in agricultural ecosystems. Commonwealth Agricultural Bureau International, Wallingford, pp 368–386
Joergensen RG, Brookes PC (1990) Ninhydrin reactive nitrogen measurements of microbial biomass in 0.5 M K2SO4 soil extracts. Soil Biol Biochem 22:1023–1027
Joergensen RG, Brookes PC, Jenkinson DS (1990) Survival of the soil biomass at elevated temperatures. Soil Biol Biochem 22:1129–1136
Jones DL, Shannon D (1999) Mineralization of amino acids applied to soil: impact of soil sieving, storage, and inorganic nitrogen additions. Soil Sci Soc Am J 63:1199–1206
Kandeler E, Gerber H (1988) Short-term assay of soil urease activity using colorimetric determination of ammonium. Biol Fertil Soils 6:68–72
Koch AL (1997) Microbial physiology and ecology of slow growth. Microbiol Mol Biol Rev 61:305–318
Kuzyakov Y, Friedel JK, Stahr K (2000) Review of mechanisms and quantification of priming effects. Soil Biol Biochem 32:1485–1498
Marouga R, Kjelleberg S (1996) Synthesis of immediate upshift (Iup) proteins during recovery of marine Vibrio sp. strain S14 subjected to long-term carbon starvation. J Bacteriol 178:817–822
Morita RY (1988) Bioavailability of energy and its relationship to growth and starvation survival in nature. Can J Microbiol 34:436–441
Roszak DB, Colwell RR (1987) Survival strategies of bacteria in the natural environment. Microbiol Rev 51:365–379
Schnurer J, Rosswall T (1982) Fluorescine diacetate hydrolysis as a measure of total microbial activity in soil and litter. Appl Environ Microbiol 43:1256–1261
Siegele DA, Guynn LJ (1996) Escherichia coli proteins synthesized during recovery from starvation. J Bacteriol 178:6352–6356
Siegele DA, Kolter R (1992) Life after log. J Bacteriol 174:345–348
Srinivasan S, Ostling J, Charlton T, de Nys R, Takayama K, Kjelleberg S (1998) Extracellular signal molecule(s) involved in the carbon starvation response of marine Vibrio sp. strain S14. J Bacteriol 180:201–209
Steele HL, Streit WR (2005) Metagenomics: advances in ecology and biotechnology. FEMS Microbiol Lett 247:105–111
Tabatabai MA (1994) Soil enzymes. In: Weaver RW et al (eds) Methods of soil analysis: Part 2. Microbiological and biochemical properties. Soil Science Society of America, Madison, WI, USA, pp775–833
Tappe W, Laverman A, Bohland M, Braster M, Rittershaus S, Groeneweg J, van Verseveld HW (1999) Maintenance energy demand and starvation recovery dynamics of Nitrosomonas europaea and Nitrobacter winogradskyi cultivated in a retentostat with complete biomass retention. Appl Environ Microbiol 65:2471–2477
Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass. Soil Biol Biochem 19:703–707
Weinbauer GM, Hofle MG (1998) Distribution and life strategies of two bacterial populations in a eutrophic lake. Appl Environ Microbiol 64:3776–3783
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
Acknowledgements
We are grateful to Dr. Alessandro Peressotti (University of Udine) for theoretical background and Mr. Riul Ennio and Riul Luca for technical assistance in the operation of the automated system for continuous gas sampling and analysis. We also thank ILSA for providing protein hydrolysates and carbohydrates samples. This research was supported by a grant from the Italian Ministry for Agricultural and Forestry Policies (MiPAF), Project PARSIFAL, General Series, Paper No. 16. Rothamsted Research receives grant-aided support from the Biological and Biotechnological Sciences Research Council.
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Contribution presented at the Exploratory Workshop: ‘Non-molecular manipulation of soil microbial communities’, held at the University of Udine, Udine, Italy from 17 to 20 October, 2004. The workshop was funded by the European Science Foundation and the University of Udine.
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Mondini, C., Cayuela, M.L., Sanchez-Monedero, M.A. et al. Soil microbial biomass activation by trace amounts of readily available substrate. Biol Fertil Soils 42, 542–549 (2006). https://doi.org/10.1007/s00374-005-0049-2
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DOI: https://doi.org/10.1007/s00374-005-0049-2