Abstract
Microbial activity is known to be high under permanent grassland, but consequences for soil phosphorus (P) dynamics and availability are not well understood. Our main objective was to assess the microbial P turnover derived from the seasonal fluctuations in microbial P (measured as hexanol-labile P (Phex) at 13 sampling times during 9 months) in a permanent grassland in Switzerland as affected by different P fertilization treatments (P inputs of 0 (NK) or 17 kg P ha−1 year−1 in the form of superphosphate (NPK) or dairy slurry (DS)). Plant P uptake, available inorganic P measured as resin-extractable P (Pres), potential organic P mineralization indicated by acid phosphomonoesterase activity and climatic conditions were also recorded. Despite significant differences in plant P uptake and Pres (NPK > DS > NK), the turnover rate of Phex was similar in all treatments (approximately once per growing season). Thus, the seasonal P flux through Phex was similar to the stock of Phex, which was about 18, 25 and 37 kg P ha−1 in NK, NPK and DS, respectively, and larger than the corresponding seasonal plant P uptake of 6, 17 and 12 kg P ha−1. The estimate of Phex turnover based on seasonal dynamics did not confirm previous tracer-based findings of a much faster Phex turnover under low availability of inorganic P, and the magnitude of Phex turnover depended on the number of sampling points taken into account. Fluctuations in Pres and Phex were related to soil moisture and indicated competition between plants and microorganisms for available P.
Similar content being viewed by others
References
Achat DL, Bakker MR, Morel C (2009) Process-based assessment of phosphorus availability in a low phosphorus sorbing forest soil using isotopic dilution methods. Soil Sci Soc Am J 73:2131–2142
Achat DL, Bakker MR, Saur E, Pellerin S, Augusto L, Morel C (2010a) Quantifying gross mineralisation of P in dead soil organic matter: testing an isotopic dilution method. Geoderma 158:163–172
Achat DL, Morel C, Bakker MR, Augusto L, Pellerin S, Gallet-Budynek A, Gonzalez M (2010b) Assessing turnover of microbial biomass phosphorus: combination of an isotopic dilution method with a mass balance model. Soil Biol Biochem 42:2231–2240
Blackwell MSA, Brookes RC, de la Fuente-Martinez N, Gordon H, Murray PJ, Snars KE, Williams JK, Bol R, Haygarth PM (2010) Phosphorus solubilization and potential transfer to surface waters from the soil microbial biomass following drying-rewetting and freezing-thawing. Adv Agron 106:1–35
Bloem J, de Ruiter P, Bouwman L (1997) Soil food webs and nutrient cycling in agroecosystems. In: van Elsas JD, Trevors JT, Wellington EMH (eds) Modern soil microbiology. Marcel Dekker, New York, pp 245–278
Bünemann EK, Marschner P, McNeill AM, McLaughlin MJ (2007) Measuring rates of gross and net mineralisation of organic phosphorus in soils. Soil Biol Biochem 39:900–913
Bünemann EK, Oberson A, Liebisch F, Keller F, Annaheim KE, Huguenin-Elie O, Frossard E (2012) Rapid microbial phosphorus immobilization dominates gross phosphorus fluxes in a grassland soil with low inorganic phosphorus availability. Soil Biol Biochem 51:84–95
Bünemann EK, Keller B, Hoop D, Jud K, Boivin P, Frossard E (2013) Increased availability of phosphorus after drying and rewetting of a grassland soil: processes and plant use. Plant Soil 370:511–526
Chen CR, Condron LM, Davis MR, Sherlock RR (2003) Seasonal changes in soil phosphorus and associated microbial properties under adjacent grassland and forest in New Zealand. For Ecol Manage 177:539–557
Cole CV, Elliott ET, Hunt HW, Coleman DC (1978) Trophic interactions in soils as they affect energy and nutrient dynamics. V. Phosphorus transformations. Microb Ecol 4:381–387
Flisch R, Sinaj S, Charles R, Richner W (2009) Grundlagen für die düngung im acker- und futterbau. Agrarforschung 16:1–100
Guitian R, Bardgett RD (2000) Plant and soil microbial responses to defoliation in temperate semi-natural grassland. Plant Soil 220:271–277
Harden T, Joergensen RG (2000) Relationship between simulated spatial variability and some estimates of microbial biomass turnover. Soil Biol Biochem 32:139–142
He ZL, Wu J, O’Donnell AG, Syers JK (1997) Seasonal responses in microbial biomass carbon, phosphorus and sulphur in soils under pasture. Biol Fert Soils 24:421–428
Henderson R, Kabengi N, Mantripragada N, Cabrera M, Hassan S, Thompson A (2012) Anoxia-induced release of colloid- and nanoparticle-bound phosphorus in grassland soils. Env Sci Techn 46:11727–11734
Huguenin-Elie O, Gago R, Stutz CJ, Lüscher A, Kessler W (2006) Long-term effects of fertilisation on herbage composition, yield and quality of an Arrhenatherion-type meadow. Grassl Sci Eur 11: 550–552. http://www.europeangrassland.org/printed-matter/proceedings.html
IDAWEB (2009) Meteo Swiss, the Swiss Federal Office of Meteorology and Climatology. http://www.meteoschweiz.admin.ch. Accessed 16 Mar 2010
Jupp AP, Newman EI (1987) Phosphorus uptake from soil by Lolium perenne during and after severe drought. J Appl Ecol 24:979–990
Kouno K, Tuchiya Y, Ando T (1995) Measurement of soil microbial biomass phosphorus by an anion exchange membrane method. Soil Biol Biochem 27:1353–1357
Kuzyakov Y, Xu X (2013) Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytol 198:656–669
Liebisch F, Bunemann EK, Huguenin-Elie O, Jeangros B, Frossard E, Oberson A (2013) Plant phosphorus nutrition indicators evaluated in agricultural grasslands managed at different intensities. Eur J Agron 44:67–77
Magid J, Nielsen NE (1992) Seasonal variation in organic and inorganic phosphorus fractions of temperate climate sandy soils. Plant Soil 144:155–165
Marschner P, Crowley D, Rengel Z (2011) Rhizosphere interactions between microorganisms and plants govern iron and phosphorus acquisition along the root axis—model and research methods. Soil Biol Biochem 43:883–894
Marx MC, Wood M, Jarvis SC (2001) A microplate fluorimetric assay for the study of enzyme diversity in soils. Soil Biol Biochem 33:1633–1640
Mawdsley JL, Bardgett RD (1997) Continuous defoliation of perennial ryegrass (Lolium perenne) and white clover (Trifolium repens) and associated changes in the composition and activity of the microbial population of an upland grassland soil. Biol Fert Soils 24:52–58
McGill WB, Cannon KR, Robertson JA, Cook FD (1986) Dynamics of soil microbial biomass and water-soluble organic C in Breton L after 50 years of cropping to two rotations. Can J Soil Sci 66:1–19
Nannipieri P, Johnson RL, Paul EA (1978) Criteria for measurement of microbial growth and activity in soil. Soil Biol Biochem 10:223–229
Nannipieri P, Giagnoni L, Landi L, Renella G (2011) Role of phosphatase enzymes in soil. In: Bünemann EK, Oberson A, Frossard E (eds) Phosphorus in action—biological processes in soil phosphorus cycling. Springer, Heidelberg, pp 215–243
Oberson A, Joner EJ (2005) Microbial turnover of phosphorus in soil. In: Turner BL, Frossard E, Baldwin D (eds) Organic phosphorus in the environment. CABI, Wallingford, pp 133–164
Oberson A, Besson J-M, Maire N, Sticher H (1995) The role of microbiological processes in soil organic phosphorus transformations in conventional and biological farming systems. In: Mäder P, Raupp J (Eds) Effects of low and high external input agriculture on soil microbial biomass and activities in view of sustainable agriculture. Proceedings of the second meeting in Oberwil (Switzerland), Sep 15–16, 1995. Research Institute of Organic Agriculture (Oberwil) and Institute for Biodynamic Research (Darmstadt), pp 13–23
Oehl F, Oberson A, Sinaj S, Frossard E (2001) Organic phosphorus mineralization studies using isotopic dilution techniques. Soil Sci Soc Am J 65:780–787
Oehl F, Frossard E, Fliessbach A, Dubois D, Oberson A (2004) Basal organic phosphorus mineralization in soils under different farming systems. Soil Biol Biochem 36:667–675
Ohno R, Zibilske LM (1991) Determination of low concentrations of phosphorus in soil extracts using malachite green. Soil Sci Soc Am J 55:892–895
Perrott KW, Sarathchandra SU, Waller JE (1990) Seasonal storage and release of phosphorus and potassium by organic matter and the microbial biomass in a high-producing pastoral soil. Aus J Soil Res 28:593–608
Perrott KW, Sarathchandra SU, Dow BW (1992) Seasonal and fertilizer effects on the organic cycle and microbial biomass in a hill country soil under pasture. Aus J Soil Res 30:383–394
Philipp A, Huguenin-Elie O, Flisch R, Gago R, Stutz C, Kessler W (2004) Einfluss der phosphordüngung auf eine fromentalwiese. Agrarforschung 11:86–91
Poll C, Ingwersen J, Stemmer M, Gerzabek MH, Kandeler E (2006) Mechanisms of solute transport affect small-scale abundance and function of soil microorganisms in the detritusphere. Eur J Soil Sci 57:583–595
R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria ISBN 3-900051-07-0. http://www.R-project.org.
Rousk J, Bååth E, Göransson H, Fransson AM (2007) Assessing plant-microbial competition for P-33 using uptake into phospholipids. Appl Soil Ecol 36:233–237
Saunders WMH, Williams EG (1955) Observations on the determination of total organic phosphorus in soils. J Soil Sci 6:254–267
Simpson M, McLenaghen RD, Chirino-Valle I, Condron LM (2012) Effects of long-term grassland management on the chemical nature and bioavailability of soil phosphorus. Biol Fert Soils 48:607–611
Tamburini F, Pfahler V, Bünemann EK, Gülland K, Bernasconi SM, Frossard E (2012) Oxygen isotopes unravel the role of microorganisms in phosphate cycling in soils. Env Sci Techn 46:5956–5962
Tan H, Barret M, Mooij MJ, Rice O, Morrissey JP, Dobson A, Griffiths B, O’Gara F (2013) Long-term phosphorus fertilisation increased the diversity of the total bacterial community and the phoD phosphorus mineraliser group in pasture soils. Biol Fert Soils 49:661–672
Turner BL, Cade-Menum BJ, Westermann DT (2003a) Organic phosphorus composition and potential bioavailability in semi-arid arable soils of the western United States. Soil Sci Soc Am J 67:1168–1179
Turner BL, Mahieu N, Condron LM (2003b) The phosphorus composition of temperate pasture soils determined by NaOH-EDTA extraction and solution 31P NMR spectroscopy. Org Geochem 34:1199–1210
von Lützow M, Ottow JCG (1994) Effect of conventional and biological farming on microbial biomass and its nitrogen turnover in agriculturally used luvisols of the Friedberg plains. J Plant Nutr Soil Sci 157:359–367
Wanner BL (1996) Phosphorus assimilation and control of the phosphate regulon. In: Neidhardt FC (ed) Escherichia coli and Salmonella—cellular and molecular biology. ASM Press, Washington, pp 1357–1381
Wardle DA (1998) Controls of temporal variability of the soil microbial biomass: a global-scale synthesis. Soil Biol Biochem 30:1627–1637
Whitehead DC (1995) Grassland nitrogen. CAB International, Wallingford
Acknowledgments
We are grateful to Angela Erb for analysing the soil phosphomonoesterase activity. This study was conducted within COST action 869 in a project funded by the Swiss State Secretariat for Education and Research.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(PDF 96 kb)
Rights and permissions
About this article
Cite this article
Liebisch, F., Keller, F., Huguenin-Elie, O. et al. Seasonal dynamics and turnover of microbial phosphorusin a permanent grassland. Biol Fertil Soils 50, 465–475 (2014). https://doi.org/10.1007/s00374-013-0868-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00374-013-0868-5