Skip to main content

Advertisement

Log in

Microbial immobilisation of phosphorus in soils exposed to drying-rewetting and freeze-thawing cycles

  • Original Paper
  • Published:
Biology and Fertility of Soils Aims and scope Submit manuscript

Abstract

Drying-rewetting and freezing-thawing can drastically alter P availability in soil. We studied how these weather events affect microbial immobilisation/mobilisation of P on the four soil types from a climatic gradient with increasing annual mean temperatures and a progressive decrease in precipitation: Podzol, Phaeozem, Chernozem and Kastanozem. Soils were exposed to (1) optimal moisture and temperature, (2) drying-rewetting and (3) freezing-thawing. Soils were treated with a 33P spike immediately after rewetting or thawing to simulate P pulse. Thereafter, P immobilisation by soil microorganisms was estimated by direct fumigation and anion exchange membrane techniques. To ensure correct estimation of microbial P (Pmic), the conversion factors kP were determined individually for each soil by 33P labelling with the correction for 33P sorption and 31P–33P isotopic exchange. The membrane extraction minimised both sorption and isotopic exchange of P released with both sorption and isotopic exchange coefficients close to 0.9 irrespectively of the soil. Specific kP varied from 0.19 to 0.38. Pmic values followed the pattern freezing-thawing < drying-rewetting < optimal conditions, varying from 2.0 to 36.6 mg P kg−1. Intensive microbial immobilisation of 33P after rewetting (up to 41 %) demonstrated a conversion of dissolved P to Pmic potentially available for plant nutrition. Remarkably, no detectable microbial immobilisation of 33P was found in the freezing-thawing treatment. In contrast to drying, freezing decreased total Pmic by up to 7.5 times. Values of membrane-extractable 33P increased in the order drying-rewetting < control < freezing-thawing, and up to 77 % of added 33P was recovered in dissolved P forms after thawing, indicating the potential risk of P leaching after freezing-thawing events.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Achat DL, Bakker MR, Augusto L, Saur E, Dousseron L, Morel C (2009) Evaluation of the phosphorus status of P-deficient podzols in temperate pine stands: combining isotopic dilution and extraction methods. Biogeochem 92:183–200

    Article  CAS  Google Scholar 

  • Achat DL, Bakker MR, Saur E, Pellerin S, Augusto L, Morel C (2010) Quantifying gross mineralisation of P in dead soil organic matter: testing an isotopic dilution method. Geoderma 158:163–172

    Article  CAS  Google Scholar 

  • Achat DL, Augusto L, Gallet-Budynek A, Bakker MR (2012) Drying-induced changes in phosphorus status of soils with contrasting soil organic matter contents—implications for laboratory approaches. Geoderma 187–188:41–48

    Article  Google Scholar 

  • Alef K (1995) Sterilisation of soil and inhibition of microbial activity. In: Alef K, Nannipieri P (eds) Methods of applied soil microbiology and biochemistry. Acad Press, London, pp 52–54

    Google Scholar 

  • Alekseeva T, Alekseev A, Maher BA, Demkin V (2007) Late Holocene climate reconstructions for the Russian steppe, based on mineralogical and magnetic properties of buried palaeosols. Pelaegeog Palaeoclim Palaeoecol 249:103–127

    Article  Google Scholar 

  • Azam F, Mulvaney RL, Stevenson FJ (1989) Synthesis of 15N labelled microbial biomass in soil in situ and extraction of biomass N. Biol Fertil Soils 7:180–185

    Article  Google Scholar 

  • Baon JB, Smith SE, Alston AM (1994) Phosphorus uptake and growth of barley as affected by soil temperature and mycorrhizal infection. J Plant Nutr 17:479–492

    Article  Google Scholar 

  • Bargett RD, McAlister E (1999) The measurement of soil bacterial: fungal biomass ratios as an indicator of self-regulation in temperate meadow grassland. Biol Fertil Soils 29:282–290

    Article  Google Scholar 

  • Blackwell MSA, Brookes PC, 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

    Article  CAS  Google Scholar 

  • Blagodatsky SA, Yevdokimov IV (1998) Extractability of microbial N as influenced by C:N ratio in the flush after drying or fumigation. Biol Fertil Soils 28:5–11

    Article  CAS  Google Scholar 

  • Borken W, Matzner E (2009) Reappraisal of drying and wetting effects on C and N mineralisation and fluxes in soils. Glob Change Biol 15:808–824

    Article  Google Scholar 

  • Brookes PC, Powlson DS, Jenkinson DS (1982) Measurement of microbial biomass phosphorus in soil. Soil Biol Biochem 14:319–329

    Article  CAS  Google Scholar 

  • Bünemann EK (2015) Assessment of gross and net mineralization rates of soil organic phosphorus—a review. Soil Biol Biochem 89:82–98

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Bünemann EK, Oberson A, Liebisch F, Keller F, Annaheim KE, Huguenin-Elie O, Frossard E (2012) Rapid microbial phosphorus immobilisation dominates gross phosphorus fluxes in a grassland soil with low inorganic phosphorus availability. Soil Biol Biochem 51:84–95

    Article  Google Scholar 

  • Bünemann EK, Keller B, Hoop D, Jud K, Boivin P, Frossardet E (2013) Increased availability of phosphorus after drying and rewetting of a grassland soil: processes and plant use. Plant Soil 370:511–526

    Article  Google Scholar 

  • Butterly CR, Bünemann EK, McNeill AM, Baldock JA, Marschner P (2009) Carbon pulses but not phosphorus pulses are related to decreases in microbial biomass during repeated drying and rewetting of soils. Soil Biol Biochem 41:1406–1416

    Article  CAS  Google Scholar 

  • Butterly CR, McNeill AM, Baldock JA, Marschner P (2011) Changes in water content of two agricultural soils does not alter labile P and C pools. Plant Soil 348:185–201

    Article  CAS  Google Scholar 

  • Cheesman AW, Turner BL, Reddy KR (2010) Interaction of phosphorus compounds with anion-exchange membranes: implications for soil analysis. Soil Sci Soc Am J 74:1607–1612

    Article  CAS  Google Scholar 

  • d’Angelo E, Crutchfield J, Vandiviere M (2001) Rapid, sensitive, microscale determination of phosphate in water and soil. J Environ Qual 30:2206–2209

    Article  PubMed  Google Scholar 

  • Dijkstra FA, He M, Johansen MP, Harrison JJ, Keitel C (2015) Plant and microbial uptake of nitrogen and phosphorus affected by drought using 15N and 32P tracers. Soil Biol Biochem 82:135–142

    Article  CAS  Google Scholar 

  • Fierer N, Schimel JP (2002) Effects of drying-rewetting frequency on soil carbon and nitrogen transformations. Soil Biol Biochem 34:777–787

    Article  CAS  Google Scholar 

  • Fierer N, Schimel JP (2003) A proposed mechanism for the pulse in carbon dioxide production commonly observed following the rapid rewetting of a dry soil. Soil Sci Soc Am J 67:798–805

    Article  CAS  Google Scholar 

  • Frossard E, Condron LM, Oberson A, Sinaj S, Fardeau JC (2000) Processes governing phosphorus availability in temperate soils. J Environ Qual 29:15–23

    Article  CAS  Google Scholar 

  • Frossard E, Achat DL, Bernasconi SM, Bünemann EK, Fardeau J-C, Jansa J, Morel C, Rabeharisoa L, Randriamanantsoa L, Sinaj S, Tamburini F, Oberson A (2011) The use of tracers to investigate phosphate cycling in soil–plant systems. In: Bünemann EK, Oberson A, Frossard E (eds) Phosphorus in action: biological processes in soil phosphorus cycling, vol 26, Soil biology. Springer, Heidelberg. doi:10.1007/978-3-642-15271-9_3

    Chapter  Google Scholar 

  • Hedley MJ, Stewart JWB (1982) Method to measure microbial phosphate in soils. Soil Biol Biochem 14:377–385

    Article  CAS  Google Scholar 

  • IPCC (2014) Climate Change 2014: Synthesis Report. In: Core Writing Team, Pachauri RK, Meyer LA (eds) Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva, p 151

    Google Scholar 

  • IUSS Working Group WRB (2006) World reference base for soil resources 2006, 2nd ed. In: FAO (ed) World Soil Resources Reports No. 103, Rome

  • Jenkinson DS (1988) Determination of microbial biomass carbon and nitrogen in soil. In: Wilson JR (ed) Advances in nitrogen cycling in agriculture ecosystems. CAB International, Wallingford, pp 368–386

    Google Scholar 

  • Kaiser V, Kleber M, Berhe AA (2015) How air-drying and rewetting modify soil organic matter characteristics: an assessment to improve data interpretation and inference. Soil Biol Biochem 80:324–340

    Article  CAS  Google Scholar 

  • Kouno K, Tuchiya Y, Ando T (1995) Measurement of soil microbial biomass phosphorus by an anion exchange membrane method. Soil Biol Biochem 27:353–1357

    Article  Google Scholar 

  • Liebisch F, Keller F, Huguenin-Elie O, Frossard E, Oberson A, Bünemann EK (2014) Seasonal dynamics and turnover of microbial phosphorus in a permanent grassland. Biol Fertil Soils 50:465–475

    Article  CAS  Google Scholar 

  • Lukas S, Abbas SJ, Karlovsky P, Potthoff M, Joergensen RG (2014) Substrate use and survival of fungal plant pathogens on maize residues at winter temperatures around freezing point. Soil Biol Biochem 77:141–149

    Article  CAS  Google Scholar 

  • McKeague JA, Day JH (1966) Dithionite-and oxalate-extractable Fe and Al as aids in differentiating various classes of soils. Can J Soil Sci 46:13–22

    Article  CAS  Google Scholar 

  • McLaughlin MJ, Alston AM, Martin JK (1988) Phosphorus cycling in wheat-pasture rotations. II.* The role of the microbial biomass in phosphorus cycling. Aust J Soil Res 26:333–342

    Article  Google Scholar 

  • Mehra OP, Jackson ML (1960) Iron oxide removal from soils and clay by a dithionite citrate system buffered with sodium bicarbonate. Clay Clay Miner 7:317–327

    Article  Google Scholar 

  • Nannipieri P, Johnson RL, Paul EA (1978) Criteria for measurement of microbial growth and activity in soil. Soil Biol Biochem 10:223–229

    Article  CAS  Google Scholar 

  • Nannipieri P, Giagnoni L, Renella G, Puglisi E, Ceccanti B, Masciandaro G, Fornasier F, Moscatelli MC, Marinari S (2012) Soil enzymology: classical and molecular approaches. Biol Fertil Soils 48:743–762

    Article  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • Oberson A, Friesen DK, Rao IM, Bühler S, Frossard E (2001) Phosphorus transformations in an Oxisol under contrasting land-use systems: the role of the soil microbial biomass. Plant Soil 237:197–210

    Article  CAS  Google Scholar 

  • Oehl F, Oberson A, Sinaj S, Frossard E (2001) Organic phosphorus mineralisation studies using isotopic dilution techniques. Soil Sci Soc Am J 65:780–787

    Article  CAS  Google Scholar 

  • Orlov DS (1992) Soil chemistry. A.A. Balkema Publishers, Rotterdam, p 390

    Google Scholar 

  • Qian P, Schoenau JJ (2002) Practical applications of ion exchange resins in agricultural and environmental soil research. Can J Soil Sci 82:9–21

    Article  CAS  Google Scholar 

  • Rennenberg H, Dannenmann M, Gessler A, Kreuzwieser J, Simon J, Papen H (2009) Nitrogen balance in forest soils: nutritional limitation of plants under climate change stresses. Plant Biol 11:4–23

    Article  CAS  PubMed  Google Scholar 

  • Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecol 88:1386–1394

    Article  Google Scholar 

  • Sparling GP, West AW (1989) Importance of soil water content when estimating soil microbial C, N and P by the fumigation-extraction methods. Soil Biol Biochem 21:245–253

    Article  CAS  Google Scholar 

  • Susyan EA, Ananyeva ND, Blagodatskaya EV (2005) The antibiotic-aided distinguishing of fungal and bacterial substrate-induced respiration in various soil ecosystems. Microbiology 74:336–342

    Article  CAS  Google Scholar 

  • Suzina NE, Mulyukin AL, Kozlova AN, Shorokhova AP, Dmitriev VV, Barinova ES, Mokhova ON, El’-Registan GI, Duda VI (2004) Ultrastructure of resting cells of some non-spore-forming bacteria. Microbiology 73:435–447

    Article  CAS  Google Scholar 

  • Thiet RH, Frey SD, Six J (2006) Do growth yield efficiencies differ between soil microbial communities differing in fungal:bacterial ratios? Reality check and methodological issues. Soil Biol Biochem 38:837–844

    Article  CAS  Google Scholar 

  • Tolpeshta II, Sokolova TA (2010) Mobile aluminum compounds in soils of the Southern Taiga (soils of the Central Forest Reserve as an example). Eurasian Soil Sci 43:893–904

    Article  Google Scholar 

  • Turner BL, Driessen JP, Haygarth PM, Mckelviea ID (2003) Potential contribution of lysed bacterial cells to phosphorus solubilisation in two rewetted Australian pasture soils. Soil Biol Biochem 35:187–189

    Article  CAS  Google Scholar 

  • Wang B, Funakoshi D, Dalpé Y, Hamel C (2002) Phosphorus-32 absorption and translocation to host plants by arbuscular mycorrhizal fungi at low root-zone temperature. Mycorrhiza 12:93–96

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful to the Russian Science Foundation (project 14-14-00625) for financial support. Also, we are thankful to the editor and two anonymous reviewers for very helpful suggestions and improvements. Besides, we thank Prof. Dr Yakov Kuzyakov for valuable discussion of the MS.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ilya Yevdokimov.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yevdokimov, I., Larionova, A. & Blagodatskaya, E. Microbial immobilisation of phosphorus in soils exposed to drying-rewetting and freeze-thawing cycles. Biol Fertil Soils 52, 685–696 (2016). https://doi.org/10.1007/s00374-016-1112-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-016-1112-x

Keywords

Navigation