Soil microbes become a major pool of biological phosphorus during the early stage of soil development with little evidence of competition for phosphorus with plants

  • Jipeng Wang
  • Yanhong WuEmail author
  • Jun Zhou
  • Haijian Bing
  • Hongyang Sun
  • Qingqing He
  • Jingji Li
  • Wolfgang Wilcke
Regular Article



We aimed to quantify the pool size of soil microbial biomass P (Pmic) during the early stage of soil development up to 125 years after glacial retreat in the Gongga Mountains, China and relate the pool size of Pmic to the plant P (Pplant) pools in the ecosystem.


We determined the pool sizes of P in soil microbes, plants and soils and the P fluxes with plant uptake and litterfall in successional ecosystems at five study sites along the 125-year Hailuogou glacial retreat chronosequence. Moreover, we estimated the flux of P cycled through microbial biomass (Pmic cycling) based on literature data. We also approached the likelihood of P competition between plants and soil microbes based on the P status of the plants, soils and soil microbes.


The size of the Pmic pools (0.2–8.3 g m−2) in the organic layer and top 10 cm of the mineral soils was comparable to that of the Pplant pools (0.3–9.1 g m−2) at all study sites along the Hailuogou chronosequence. Based on the literature, the Pmic cycling at our study site (0.3–13.5 g m−2 year−1 if estimated based on temporal fluctuations of Pmic, 5.2–268 g m−2 year−1 if estimated based on the isotope dilution method) was at least one order of magnitude larger than the Pplant uptake (not detected-0.36 g m−2 year−1) and the Pplant return by litterfall (not detected-0.16 g m−2 year−1). Although Pmic became a major pool of biological P, we did not find indications of P competition between plants and soil microbes as indicated by the positive relationships between the concentrations of Pmic and plant-available P in soils and the P-rich status of plants and soil microbes.


Soil microbial biomass already becomes a major P pool in the early stage of soil development. Our estimations based on the literature suggest that Pmic cycling is probably the largest P flux in the studied up to 125-year ecosystems. Plants likely did not suffer P competition with microbes, in part due to the preferential decomposition of the P-rich compounds from dead microbial biomass which led to net P mineralization.


Soil microbial biomass Phosphorus cycling Phosphomonoesterase Primary succession Hailuogou chronosequence 



This research was supported by the National Natural Science Foundation of China (No. 41630751, 41701288 and 41877011), Science & Technology Department of Sichuan Province (Grant No. 18YYJC0163) and the China Scholarship Council (201708515106).

Supplementary material

11104_2019_4329_MOESM1_ESM.docx (2.2 mb)
ESM 1 (DOCX 2248 kb)


  1. 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 158:163–172CrossRefGoogle Scholar
  2. 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 42:2231–2240CrossRefGoogle Scholar
  3. Allen AP, Gillooly JF (2009) Towards an integration of ecological stoichiometry and the metabolic theory of ecology to better understand nutrient cycling. Ecol Lett 12:369–384CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bernasconi SM et al (2011) Chemical and biological gradients along the Damma glacier soil chronosequence, Switzerland. Vadose Zone J 10:867–883CrossRefGoogle Scholar
  5. Bol R et al (2016) Dissolved and colloidal phosphorus fluxes in forest ecosystems—an almost blind spot in ecosystem research. J Plant Nutr Soil Sci 179:425–438CrossRefGoogle Scholar
  6. Bowman WD, Bahn L, Damm M (2003) Alpine landscape variation in foliar nitrogen and phosphorus concentrations and the relation to soil nitrogen and phosphorus availability. Arct Antarct Alp Res 35:144–149CrossRefGoogle Scholar
  7. Brandtberg P-O, Bengtsson J, Lundkvist H (2004) Distributions of the capacity to take up nutrients by Betula spp. and Picea abies in mixed stands. For Ecol Manag 198:193–208CrossRefGoogle Scholar
  8. Chadwick OA, Derry LA, Vitousek PM, Huebert BJ, Hedin LO (1999) Changing sources of nutrients during four million years of ecosystem development Nature 397:491Google Scholar
  9. Chapin FS, Walker LR, Fastie CL, Sharman LC (1994) Mechanisms of primary succession following deglaciation at Glacier Bay, Alaska. Ecol Monogr 64:149–175CrossRefGoogle Scholar
  10. 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 Manag 177:539–557CrossRefGoogle Scholar
  11. Clarholm M (1993) Microbial biomass P, labile P, and acid phosphatase activity in the humus layer of a spruce forest, after repeated additions of fertilizers. Biol Fertil Soils 16:287–292CrossRefGoogle Scholar
  12. Clemmensen KE et al (2013) Roots and associated Fungi drive long-term carbon sequestration in boreal Forest. Science 339:1615–1618CrossRefPubMedPubMedCentralGoogle Scholar
  13. Cleveland CC, Liptzin D (2007) C: N: P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85:235–252CrossRefGoogle Scholar
  14. Cotrufo MF, Wallenstein MD, Boot CM, Denef K, Paul E (2013) The microbial efficiency-matrix stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter? Glob Chang Biol 19:988–995CrossRefPubMedPubMedCentralGoogle Scholar
  15. Courchesne F, Turmel MC (2008) Extractable Al, Fe, Mn, and Si. In: Cartery MR, Gregorich EG (eds) Soil sampling and methods of analysis, second edition. CRC Press, Boca Raton Taylor & Francis Group, LLC, pp 307–315Google Scholar
  16. Darcy JL, Schmidt SK, Knelman JE, Cleveland CC, Castle SC, Nemergut DR (2018) Phosphorus, not nitrogen, limits plants and microbial primary producers following glacial retreat science. Advances 4:eaaq0942Google Scholar
  17. Egli M, Filip D, Mavris C, Fischer B, Götze J, Raimondi S, Seibert J (2012) Rapid transformation of inorganic to organic and plant-available phosphorous in soils of a glacier forefield. Geoderma 189–190:215–226CrossRefGoogle Scholar
  18. Elser JJ, Dobberfuhl DR, MacKay NA, Schampel JH (1996) Organism size, life history, and N: P stoichiometry. Bioscience 46:674–684CrossRefGoogle Scholar
  19. Göransson H, Olde Venterink H, Bååth E (2011) Soil bacterial growth and nutrient limitation along a chronosequence from a glacier forefield. Soil Biol Biochem 43:1333–1340CrossRefGoogle Scholar
  20. Hacker N et al (2015) Plant diversity shapes microbe-rhizosphere effects on P mobilisation from organic matter in soil. Ecol Lett 18:1356–1365CrossRefPubMedPubMedCentralGoogle Scholar
  21. Hedley M, Stewart J (1982) Method to measure microbial phosphate in soils. Soil Biol Biochem 14:377–385CrossRefGoogle Scholar
  22. Heuck C, Weig A, Spohn M (2015) Soil microbial biomass C:N:P stoichiometry and microbial use of organic phosphorus. Soil Biol Biochem 85:119–129CrossRefGoogle Scholar
  23. Hoppe H-G, Ullrich S (1999) Profiles of ectoenzymes in the Indian Ocean: phenomena of phosphatase activity in the mesopelagic zone. Aquat Microb Ecol 19:139–148CrossRefGoogle Scholar
  24. Jenkinson DS, Brookes PC, Powlson DS (2004) Measuring soil microbial biomass. Soil Biol Biochem 36:5–7CrossRefGoogle Scholar
  25. Jiang Y, Lei Y, Yang Y, Korpelainen H, Niinemets Ü, Li C (2018) Divergent assemblage patterns and driving forces for bacterial and fungal communities along a glacier forefield chronosequence. Soil Biol Biochem 118:207–216CrossRefGoogle Scholar
  26. Johnson AH, Frizano J, Vann DR (2003) Biogeochemical implications of labile phosphorus in forest soils determined by the Hedley fractionation procedure. Oecologia 135:487–499CrossRefPubMedPubMedCentralGoogle Scholar
  27. Jonard M, Augusto L, Morel C, Achat DL, Saur E (2009) Forest floor contribution to phosphorus nutrition: experimental data. Ann For Sci 66:510–510CrossRefGoogle Scholar
  28. Kirkby CA, Kirkegaard JA, Richardson AE, Wade LJ, Blanchard C, Batten G (2011) Stable soil organic matter: a comparison of C:N:P:S ratios in Australian and other world soils. Geoderma 163:197–208CrossRefGoogle Scholar
  29. Kouno K, Wu J, Brookes P (2002) Turnover of biomass C and P in soil following incorporation of glucose or ryegrass. Soil Biol Biochem 34:617–622CrossRefGoogle Scholar
  30. Lang F et al (2016) Phosphorus in forest ecosystems: new insights from an ecosystem nutrition perspective. J Plant Nutr Soil Sci 179:129–135CrossRefGoogle Scholar
  31. Li W, Cheng G, Luo J, Lu R, Liao X (2004) Features of the natural runoff of Hailuo ravine in Mt. Gongga Journal of Mountain Research 22:698–701Google Scholar
  32. Li X, Xiong SF (1995) Vegetation primary succession on glacier foreland in Hailuogou, Mt. Gongga. Mountain Research 12:109–115Google Scholar
  33. Liang C, Schimel JP, Jastrow JD (2017) The importance of anabolism in microbial control over soil carbon storage. Nat Microbiol 2:17105CrossRefPubMedPubMedCentralGoogle Scholar
  34. Liebisch F, Keller F, Huguenin-Elie O, Frossard E, Oberson A, Bünemann E (2014) Seasonal dynamics and turnover of microbial phosphorusin a permanent grassland. Biol Fertil Soils 50:465–475CrossRefGoogle Scholar
  35. Liu E, Shen J, Zhang E, Wu Y, Yang L (2010) A geochemical record of recent anthropogenic nutrient loading and enhanced productivity in Lake Nansihu. China J Paleolimnol 44:15–24CrossRefGoogle Scholar
  36. Luo J, Chen Y, Wu Y, Shi P, She J, Zhou P (2012) Temporal-spatial variation and controls of soil respiration in different primary succession stages on glacier forehead in Gongga Mountain. China PLoS One 7Google Scholar
  37. Luo J, Cheng GW, Li W, He ZW (2005) Characteristics of nutrient biocycling of natural forests on the Gongga Mountain. Journal of Beijing Forestry University 27:13–17Google Scholar
  38. Margalef O et al (2017) Global patterns of phosphatase activity in natural soils. Sci Rep 7:1337CrossRefPubMedPubMedCentralGoogle Scholar
  39. Maynard DG, Curran MP (2008) Soil density measurement in forest soils. In: Cartery MR, Gregorich EG (eds) Soil sampling and methods of analysis, second edition. CRC Press, Boca Raton Taylor & Francis Group, LLC, pp 863–869Google Scholar
  40. McGill WB, Cole CV (1981) Comparative aspects of cycling of organic C, N, S and P through soil organic-matter. Geoderma 26:267–286CrossRefGoogle Scholar
  41. Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36CrossRefGoogle Scholar
  42. Myers RG, Thien SJ, Pierzynski GM (1999) Using an ion sink to extract microbial phosphorus from soil. Soil Sci Soc Am J 63:1229–1237CrossRefGoogle Scholar
  43. Nannipieri P, Giagnoni L, Landi L, Renella G (2011) Role of phosphatase enzymes in soil. In: Bünemann E, Oberson A, Frossard E (eds) Phosphorus in action: biological processes in soil phosphorus cycling. Springer Berlin Heidelberg, Berlin, Heidelberg, pp 215–243Google Scholar
  44. Oberson A, Joner EJ (2005) Microbial turnover of phosphorus in soil organic phosphorus in the environment CABI. Wallingford:133–164Google Scholar
  45. Prietzel J, Dümig A, Wu Y, Zhou J, Klysubun W (2013) Synchrotron-based P K-edge XANES spectroscopy reveals rapid changes of phosphorus speciation in the topsoil of two glacier foreland chronosequences. Geochim Cosmochim Acta:154–171Google Scholar
  46. Richardson AE, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability update on microbial phosphorus. Plant Physiol 156:989–996CrossRefPubMedPubMedCentralGoogle Scholar
  47. Richardson SJ, Peltzer DA, Allen RB, McGlone MS, Parfitt RL (2004) Rapid development of phosphorus limitation in temperate rainforest along the Franz Josef soil chronosequence. Oecologia 139:267–276CrossRefPubMedPubMedCentralGoogle Scholar
  48. Rosinger C, Rousk J, Sandén H (2019) Can enzymatic stoichiometry be used to determine growth-limiting nutrients for microorganisms?-a critical assessment in two subtropical soils. Soil Biol Biochem 128:115–126CrossRefGoogle Scholar
  49. Sinsabaugh RL, Hill BH, Shah JJF (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462:795–798CrossRefPubMedPubMedCentralGoogle Scholar
  50. Sinsabaugh RL, Manzoni S, Moorhead DL, Richter A (2013) Carbon use efficiency of microbial communities: stoichiometry, methodology and modelling. Ecol Lett 16:930–939CrossRefPubMedPubMedCentralGoogle Scholar
  51. Sinsabaugh RL, Shah JJF (2012) Ecoenzymatic stoichiometry and ecological theory annual review of ecology. Evolution, and Systematics 43:313–343CrossRefGoogle Scholar
  52. Sohrt J, Lang F, Weiler M (2017) Quantifying components of the phosphorus cycle in temperate forests Wiley Interdisciplinary Reviews: Water e1243Google Scholar
  53. Spohn M, Kuzyakov Y (2013) Phosphorus mineralization can be driven by microbial need for carbon. Soil Biol Biochem 61:69–75CrossRefGoogle Scholar
  54. Tabatabai M (1994) Soil enzymes. In: Hart SC, Stark JM, Davidson EA, Firestone MK (eds) Methods of soil analysis. Part 2 microbiological and biochemical properties, vol 2. vol 2. Soil Science Society of America, Madison, Wisconsin, USA, pp 775–833Google Scholar
  55. Tamburini F, Pfahler V, Buenemann EK, Guelland K, Bernasconi SM, Frossard E (2012) Oxygen isotopes unravel the role of microorganisms in phosphate cycling in soils. Environ Sci Technol 46:5956–5962CrossRefPubMedPubMedCentralGoogle Scholar
  56. Tiessen H, Moir J (1993) Characterization of available P by sequential extraction. in: Carter MR (ed) Soil sampling and methods of analysis. Canadian Society of Soil Science, Lewis, Boca Raton, Fla, pp 75–86Google Scholar
  57. Turner BL, Condron LM, Richardson SJ, Peltzer DA, Allison VJ (2007) Soil organic phosphorus transformations during pedogenesis. Ecosystems 10:1166–1181CrossRefGoogle Scholar
  58. Turner BL, Lambers H, Condron LM, Cramer MD, Leake JR, Richardson AE, Smith SE (2013) Soil microbial biomass and the fate of phosphorus during long-term ecosystem development. Plant Soil:1–10Google Scholar
  59. Vincent AG, Vestergren J, Grobner G, Persson P, Schleucher J, Giesler R (2013) Soil organic phosphorus transformations in a boreal forest chronosequence. Plant Soil 367:149–162CrossRefGoogle Scholar
  60. Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecol Appl 20:5–15CrossRefPubMedPubMedCentralGoogle Scholar
  61. Walker T, Syers J (1976) The fate of phosphorus during pedogenesis. Geoderma 15:1–19CrossRefGoogle Scholar
  62. Wang J, Wu Y, Zhou J, Bing H, Sun H (2016) Carbon demand drives microbial mineralization of organic phosphorus during the early stage of soil development. Biol Fertil Soils 52:825–839CrossRefGoogle Scholar
  63. Wang J, Wu Y, Zhou J, Bing H, Sun H, Luo J, Pu S (2017) Air-drying changes the distribution of Hedley phosphorus pools in forest soils. Pedosphere (in press).
  64. Wardle DA, Walker LR, Bardgett RD (2004) Ecosystem Properties and Forest Decline in Contrasting Long-Term Chronosequences. Science 305 (5683):509-513Google Scholar
  65. Wu J, He ZL, Wei WX, O'Donnell AG, Syers JK (2000) Quantifying microbial biomass phosphorus in acid soils. Biol Fertil Soils 32:500–507CrossRefGoogle Scholar
  66. Wu Y, Li W, Zhou J, Cao Y (2013) Temperature and precipitation variations at two meteorological stations on eastern slope of Gongga Mountain, SW China in the past two decades. J Mt Sci 10:370–377CrossRefGoogle Scholar
  67. Wu Y, Ma B, Zhou L, Wang H, Xu J, Kemmitt S, Brookes PC (2009) Changes in the soil microbial community structure with latitude in eastern China, based on phospholipid fatty acid analysis. Appl Soil Ecol 43:234–240CrossRefGoogle Scholar
  68. Wu Y, Zhou J, Bing H, Sun H, Wang J (2015) Rapid loss of phosphorus during early pedogenesis along a glacier retreat choronosequence, Gongga Mountain (SW China). PeerJ 3:e1377CrossRefPubMedPubMedCentralGoogle Scholar
  69. Xu X, Thornton PE, Post WM (2013) A global analysis of soil microbial biomass carbon, nitrogen and phosphorus in terrestrial ecosystems. Glob Ecol Biogeogr 22:737–749CrossRefGoogle Scholar
  70. Yang L, Wang G, Yang Y, Yang Y (2012) Responses of leaf functional traits and nitrogen and phosphorus stoichiometry in Abies fabiri seedlings in Gongga Mountain to simulated nitrogen deposition. Chinese Journal of Ecology 31:44–50Google Scholar
  71. Yang Z et al (2015) Variation of mineral composition along the soil chronosequence at the Hailuogou glacier foreland of Gongga Mountain. Acta Pedol Sin 52:507–516Google Scholar
  72. Zederer DP, Talkner U, Spohn M, Joergensen RG (2017) Microbial biomass phosphorus and C/N/P stoichiometry in forest floor and a horizons as affected by tree species. Soil Biol Biochem 111:166–175CrossRefGoogle Scholar
  73. Zhou J (2014) Weathering, pedogenesis and changes of soil phosphorus speciation of Hailuogou Glacier foreland chronosequence. PhD thesis, University of Chinese Academy of Sciences, Beijing, China, pp 76Google Scholar
  74. Zhou J, Bing H, Wu Y, Sun H, Wang J (2018a) Weathering of primary mineral phosphate in the early stages of ecosystem development in the Hailuogou glacier foreland chronosequence. Eur J Soil Sci 69:450–461CrossRefGoogle Scholar
  75. Zhou J et al (2016) Rapid weathering processes of a 120-year-old chronosequence in the Hailuogou glacier foreland, Mt. Gongga, SW China. Geoderma 267:78–91CrossRefGoogle Scholar
  76. Zhou J, Sun H, Wang J, He Q, Bing H, Wu Y (2018b) Comments on “unravelling community assemblages through multi-element stoichiometry in plant leaves and roots across primary successional stages in a glacier retreat area” by Jiang et al. Plant Soil 433:1–5CrossRefGoogle Scholar
  77. Zhou J et al (2013) Changes of soil phosphorus speciation along a 120-year soil chronosequence in the Hailuogou glacier retreat area (Gongga Mountain, SW China). Geoderma 195:251–259CrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.College of Ecology and EnvironmentChengdu University of TechnologyChengduChina
  2. 2.Key Laboratory of Mountain Surface Processes and Ecological Regulation, Institute of Mountain Hazards and EnvironmentChinese Academy of SciencesChengduChina
  3. 3.Institute of Geography and GeoecologyKarlsruhe Institute of Technology (KIT)KarlsruheGermany
  4. 4.University of Chinese Academy of SciencesBeijingChina

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