Abstract
Background and aims
The stoichiometric ratio of carbon (C): phosphorus (P) acquisition is strongly correlated with soil available C:P ratio. However how the stoichiometric relationship between acquiring C and P through microbial metabolism affects bioavailable P is poorly understood in semi-arid agricultural ecosystems.
Methods
Our objective was to investigate the underlying mechanisms of the P availability in typical P-limited steppe soil from Kazakhstan in response to mineral nutrient (Na2HPO4) with and without Dactylis glomerata L. leaves addition in a 38-day incubation experiment.
Results
Four bioavailable P fractions content (CaCl2-P, Citrate-P, Enzyme-P, and HCl-P) were improved. Sole application of P fertilizer decreased the maximal velocity (Vmax) of P acquisition enzyme (phosphomonoesterase) but increased microbial C limitation, resulting in increasing the ratio of C to P acquisition but decreasing the ratio of available dissolved organic C: Olsen-P. In contrast, plant residues returning (the application of sole D. glomerata leaves and the combined application of D.glomerata and mineral P) increased Vmax of C (β-1, 4-glucosidase, β-D-cellobiosidase, β-1, 4-xylosidase) and P acquisition enzymes, however decreasing microbial C and P limitation through improving microbial metabolism. Furthermore, the spearman correlation and piecewiseSEM analysis suggested that microbial C limitation and EEAC:P had a negative effect on P availability, illustrating that the decreasing of microbial C limitation can improve soil bioavailable P.
Conclusion
The decomposition of organic residues eliminated microbial P limitation and increased P availability by allocating C and P acquisition enzymes to balance the stoichiometric ratio of microbial C and P demand.
Graphical Abstract
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
Data will be made available on request.
References
Allison SD, Vitousek PM (2005) Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biol Biochem 37(5):937–944. https://doi.org/10.1016/j.soilbio.2004.09.014
Andrino A, Guggenberger G, Sauheitl L, Burkart S, Boy J (2021) Carbon investment into mobilization of mineral and organic phosphorus by arbuscular mycorrhiza. Biol Fertil Soils 57(1):47–64. https://doi.org/10.1007/s00374-020-01505-5
Balemi T, Negisho K (2012) Management of soil phosphorus and plant adaptation mechanisms to phosphorus stress for sustainable crop production: a review. J Soil Sci Plant Nut 12(3):547–562. https://doi.org/10.4067/S0718-95162012005000015
Baligar VC, Fageria NK, He ZL (2001) Nutrient use efficiency in plants. Commun Soil Sci Plant Anal 32(7–8):921–950. https://doi.org/10.1081/CSS-100104098
Barea JM, Pozo MJ, Azcón R, Azcón-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 56(147):1716–1778. https://doi.org/10.1093/jxb/eri197
Bárta J, Šlajsová P, Tahovská K, Picek T, Šantrůčková H (2014) Different temperature sensitivity and kinetics of soil enzymes indicate seasonal shifts in C, N and P nutrient stoichiometry in acid forest soil. Biogeochemistry 117:525–537. https://doi.org/10.1007/s10533-013-9898-1
Bashan Y, Kamnev AA, de-Bashan LE (2013) A proposal for isolating and testing phosphate-solubilizing bacteria that enhance plant growth. Biol Fertil Soils 49:1–2. https://doi.org/10.1007/s00374-012-0756-4
Brookes PC, Powlson DS, Jenkinson DS (1982) Measurement of microbial biomass phosphorus in soil. Soil Biol Biochem 14(4):319–329. https://doi.org/10.1016/0038-0717(82)90001-3
Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: A rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17(6):837–842. https://doi.org/10.1016/0038-0717(85)90144-0
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. https://doi.org/10.1016/j.soilbio.2012.04.012
Burns RG, DeForest JL, Marxsen J, Sinsabaugh RL, Stromberger ME, Wallenstein MD, Weintraub MN, Zoppini A (2013) Soil enzymes in a changing environment: Current knowledge and future directions. Soil Biol Biochem 58:216–234. https://doi.org/10.1016/j.soilbio.2012.11.009
Canfield DE, Glazer AN, Falkowski PG (2010) The evolution and future of earth’s nitrogen cycle. Science 330(6001):192–196. https://doi.org/10.1126/science.1186120
Caruso G (2010) Leucine aminopeptidase, β-glucosidase and alkaline phosphatase activity rates and their significance in nutrient cycles in some coastal Mediterranean sites. Mar Drugs 8(4):916–940. https://doi.org/10.3390/md8040916
Chernenok V, Barkusky D (2014) Diagnosis and Optimization of Phosphorus Nutrition Conditions of Grain Crops in Northern Kazakhstan. L. Müller et al (eds). Novel Measurement and Assessment Tools for Monitoring and Management of Land and Water Resources in Agricultural Landscapes of Central Asia. Environmental Science and Engineering, 667–679 https://doi.org/10.1007/978-3-319-01017-5
Cleveland CC, Liptzin D (2007) C:N: P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85(3):235–252. https://doi.org/10.1007/s10533-007-9132-0
Correll DL (1998) The role of phosphorus in the eutrophication of receiving waters: A review. J Environ Qual 27(2):261–266. https://doi.org/10.2134/jeq1998.00472425002700020004x
Cui Y, Fang L, Deng L, Guo X, Han F, Ju W, Wang X, Chen H, Tan W, Zhang X (2019) Patterns of soil microbial nutrient limitations and their roles in the variation of soil organic carbon across a precipitation gradient in an arid and semi-arid region. Sci Total Environ 658:1440–1451. https://doi.org/10.1016/j.scitotenv.2018.12.289
Cui Y, Zhang Y, Duan C, Wang X, Zhang X, Ju W, Chen H, Yue S, Wang Y, Fang L (2020) Ecoenzymatic stoichiometry reveals microbial phosphorus limitation decreases the nitrogen cycling potential of soils in semi-arid agricultural ecosystems. Soil Tillage Res 197:104463. https://doi.org/10.1016/j.still.2019.104463
DeLuca TH, Glanville HC, Harris M, Emmett BA, Pingree MRA, de Sosa LL, Cerdá-Moreno C, Jones DL (2015) A novel biologically-based approach to evaluating soil phosphorus availability across complex landscapes. Soil Biol Biochem 88:110–119. https://doi.org/10.1016/j.soilbio.2015.05.016
Ding W, Meng L, Yin Y, Cai Z, Zheng X (2007) CO2 emission in an intensively cultivated loam as affected by long-term application of organic manure and nitrogen fertilizer. Soil Biol Biochem 39(2):669–679. https://doi.org/10.1016/j.soilbio.2006.09.024
Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88(6):1354–1364. https://doi.org/10.1890/05-1839
Frossard E, Condron LM, Oberson A, Sinaj S, Fardeau JC (2000) Processes Governing Phosphorus Availability in Temperate Soils. J Environ Qual 29(1):15–23. https://doi.org/10.2134/jeq2000.00472425002900010003x
Gyaneshwar P, Parekh LJ, Archana G, Poole PS, Collins MD, Hutson RA, Kumar GN (1999) Involvement of a phosphate starvation inducible glucose dehydrogenase in soil phosphate solubilization by Enterobacter asburiae. FEMS Microbiol Lett 171(2):223–229. https://doi.org/10.1016/S0378-1097(99)00003-8
Harris D, Horwáth WR, van Kessel C (2001) Acid fumigation of soils to remove carbonates prior to total organic carbon or CARBON-13 isotopic analysis. Soil Sci Soc Am J 65(6):1853–1856. https://doi.org/10.2136/sssaj2001.1853
Harrison AF (1982) Labile organic phosphorus mineralization in relationship to soil properties. Soil Biol Biochem 14(4):343–351. https://doi.org/10.1016/0038-0717(82)90004-9
Harrison AF (1989) Soil Organic Phosphorus A review of world literature. Soil Sci 147(1):77
Heuck C, Weig A, Spohn M (2015) Soil microbial biomass C: N: P stoichiometry and microbial use oforganic phosphorus. Soil Biol Biochem 85:119–129. https://doi.org/10.1016/j.soilbio.2015.02.029
Hinsinger P (2001) Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: A review. Plant Soil 237:173–195. https://doi.org/10.1023/A:1013351617532
Hofmann K, Heuck C, Spohn M (2016) Phosphorus resorption by young beech trees and soil phosphatase activity as dependent on phosphorus availability. Oecologia 181(2):369–379. https://doi.org/10.1007/s00442-016-3581-x
Johnston AE, Poulton PR, Fixen PE, Curtin D (2014) Phosphorus. Its Efficient Use in Agriculture. In Adv Agron 123:177–228. https://doi.org/10.1016/B978-0-12-420225-2.00005-4
Kumar A, Kuzyakov Y, Pausch J (2016) Maize rhizosphere priming: field estimates using 13C natural abundance. Plant Soil 409:87–97. https://doi.org/10.1007/s11104-016-2958-2
Liu A, Hamel C, Spedding T, Zhang TQ, Mongeau R, Lamarre GR, Tremblay G (2008) Soil microbial carbon and phosphorus as influenced by phosphorus fertilization and tillage in a maize-soybean rotation in south-western Quebec. Can J Soil Sci 88(1):21–30. https://doi.org/10.4141/CJSS07016
Liu Y, Wei X, Wei L, Zhu Z, Ge T, Zhang Y, Lu S, Wu J (2018a) Responses of extracellular enzymes to carbon and phosphorus additions in Rice Rhizosphere and bulk soil. Scientia Agricultura Sinica 51(9):1653–1663. https://doi.org/10.3864/j.issn.0578-1752.2018.09.004
Liu Y, Zang H, Ge T, Bai J, Lu S, Zhou P, Peng P, Shibistova O, Zhu Z, Wu J, Guggenberger G (2018b) Intensive fertilization (N, P, K, Ca, and S) decreases organic matter decomposition in paddy soil. Appl Soil Ecol 127:51–57. https://doi.org/10.1016/j.apsoil.2018.02.012
Liu Y, Shahbaz M, Ge T, Zhu Z, Liu S, Chen L, Wu X, Deng Y, Lu S, Wu J (2020) Effects of root exudate stoichiometry on CO2 emission from paddy soil. Euro J Soil Biol 101:103247. https://doi.org/10.1016/j.ejsobi.2020.103247
Liu Y, Shahbaz M, Fang Y, Li B, Wei X, Zhu Z, Lynn TM, Lu S, Shibistova O, Wu J, Guggenberger G, Ge T (2021) Stoichiometric theory shapes enzyme kinetics in paddy bulk soil but not in rhizosphere soil. Land Degrad Dev 33:246–256. https://doi.org/10.1002/ldr.4141
Manzoni S, Trofymow JA, Jackson RB, Porporato A (2010) Stoichiometric controls on carbon, nitrogen, and phosphorus dynamics in decomposing litter. Ecol Monogr 80(1):89–106. https://doi.org/10.1890/09-0179.1
Merchant SS, Helmann JD (2012) Elemental Economy. Microbial Strategies for Optimizing Growth in the Face of Nutrient Limitation. In Adv Micro Physiol 60:91–210. https://doi.org/10.1016/B978-0-12-398264-3.00002-4
Moorhead DL, Rinkes ZL, Sinsabaugh RL, Weintraub MN (2013) Dynamic relationships between microbial biomass, respiration, inorganic nutrients and enzyme activities: Informing enzyme-based decomposition models. Front Microbiol 4:1–12. https://doi.org/10.3389/fmicb.2013.00223
Moorhead DL, Sinsabaugh RL, Hill BH, Weintraub MN (2016) Vector analysis of ecoenzyme activities reveal constraints on coupled C, N and P dynamics. Soil Biol Biochem 93:1–7. https://doi.org/10.1016/j.soilbio.2015.10.019
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. Soil Biology, Springer, Berlin, Heidelberg 26 https://doi.org/10.1007/978-3-642-15271-9_9
Nezat CA, Blum JD, Yanai RD, Park BB (2008) Mineral sources of calcium and phosphorus in soils of the northeastern United States. Soil Sci Soc Am J 72(6):1786–1794. https://doi.org/10.2136/sssaj2007.0344
Ng EL, Patti AF, Rose MT, Schefe CR, Wilkinson K, Cavagnaro TR (2014) Functional stoichiometry of soil microbial communities after amendment with stabilised organic matter. Soil Biol Biochem 76:170–178. https://doi.org/10.1016/j.soilbio.2014.05.016
Nottingham AT, Turner BL, Whitaker J, Ostle N, Bardgett RD, McNamara NP, Salinas N, Meir P (2016) Temperature sensitivity of soil enzymes along an elevation gradient in the Peruvian Andes. Biogeochemistry 127(2–3):217–230. https://doi.org/10.1007/s10533-015-0176-2
Olsen S, Cole C, Watanabe F, Dean L (1954) Estimation of available phosphorous in soils by extraction with sodium carbonate US Department of Agriculture Circular no. 939.
Palpurina S, Chytrý M, Hölzel N, Tichý L, Wagner V, Horsák M, Hájková P, Freitag M, Lososová Z, Mathar W, Tzonev R, Danihelka J, Dřevojan P (2019) The type of nutrient limitation affects the plant species richness–productivity relationship: Evidence from dry grasslands across Eurasia. J Ecol 107(3):1038–1050. https://doi.org/10.1111/1365-2745.13084
Pritsch K, Raidl S, Marksteiner E, Blaschke H, Agerer R, Schloter M, Hartmann A (2004) A rapid and highly sensitive method for measuring enzyme activities in single mycorrhizal tips using 4-methylumbelliferone-labelled fluorogenic substrates in a microplate system. J Microbiol Methods 58(2):233–241. https://doi.org/10.1016/j.mimet.2004.04.001
Razavi BS, Zarebanadkouki M, Blagodatskaya E, Kuzyakov Y (2016) Rhizosphere shape of lentil and maize: Spatial distribution of enzyme activities. Environ Model Softw 96:229–237. https://doi.org/10.1016/j.soilbio.2016.02.020
Sanaullah M, Razavi BS, Blagodatskaya E, Kuzyakov Y (2016) Spatial distribution and catalytic mechanisms of β-glucosidase activity at the root-soil interface. Biol Fertil Soils 52:505–514. https://doi.org/10.1007/s00374-016-1094-8
Scott JT, Cotner JB, LaPara TM (2012) Variable stoichiometry and homeostatic regulation of bacterial biomass elemental composition. Front Microbiol 3:42. https://doi.org/10.3389/fmicb.2012.00042
Shahbaz M, Kuzyakov Y, Sanaullah M, Heitkamp F, Zelenev V, Kumar A, Blagodatskaya E (2017) Microbial decomposition of soil organic matter is mediated by quality and quantity of crop residues: mechanisms and thresholds. Biol Fertil Soils 53:287–301. https://doi.org/10.1007/s00374-016-1174-9
Sharpley AN (1995) Soil phosphorus dynamics: agronomic and environmental impacts. Ecol Eng 5(2–3):261–279. https://doi.org/10.1016/0925-8574(95)00027-5
Sinsabaugh RL, Follstad Shah JJ (2012) Ecoenzymatic Stoichiometry and Ecological Theory. Annu Rev Ecol Evol Syst 43(1):313–343. https://doi.org/10.1146/annurev-ecolsys-071112-124414
Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME, Gartner TB, Hobbie SE, Holland K, Keeler BL, Powers JS, Stursova M, Takacs-Vesbach C, Waldrop MP, Wallenstein MD, Zak DR, Zeglin LH (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11(11):1252–1264. https://doi.org/10.1111/j.1461-0248.2008.01245.x
Sinsabaugh RL, Hill BH, Follstad Shah JJ (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462(7274):795–798. https://doi.org/10.1038/nature08632
Soong JL, Marañon-Jimenez S, Cotrufo MF, Boeckx P, Bodé S, Guenet B, Peñuelas J, Richter A, Stahl C, Verbruggen E, Janssens IA (2018) Soil microbial CNP and respiration responses to organic matter and nutrient additions: Evidence from a tropical soil incubation. Soil Biol Biochem 122:141–149. https://doi.org/10.1016/j.soilbio.2018.04.011
Spohn M, Kuzyakov Y (2013) Distribution of microbial- and root-derived phosphatase activities in the rhizosphere depending on P availability and C allocation - Coupling soil zymography with 14C imaging. Soil Biol Biochem 67:103–113. https://doi.org/10.1016/j.soilbio.2013.08.015
Spohn M, Ermak A, Kuzyakov Y (2013) Microbial gross organic phosphorus mineralization can be stimulated by root exudates - A 33P isotopic dilution study. Soil Biol Biochem 65:254–263. https://doi.org/10.1016/j.soilbio.2013.05.028
Takata H, Uchiyama S, Nakamura N, Nakashima S, Kobayashi S, Sone T, Kimura S, Lahmers S, Granzier H, Labeit S, Matsunaga S, Fukui K (2007) A comparative proteome analysis of human metaphase chromosomes isolated from two different cell lines reveals a set of conserved chromosome-associated proteins. Genes Cells 12(3):269–284. https://doi.org/10.1111/j.1365-2443.2007.01051.x
Tischer A, Blagodatskaya E, Hamer U (2015) Microbial community structure and resource availability drive the catalytic efficiency of soil enzymes under land-use change conditions. Soil Biol Biochem 89:226–237. https://doi.org/10.1016/j.soilbio.2015.07.011
Turner BL, Cade-Menun BJ, Westermann DT (2003) Organic Phosphorus Composition and Potential Bioavailability in Semi-Arid Arable Soils of the Western United States. Soil Sci Soc Am J 67(4):1168–1179. https://doi.org/10.2136/sssaj2003.1168
Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19(6):703–707. https://doi.org/10.1016/0038-0717(87)90052-6
Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: Critical adaptations by plants for securing a nonrenewable resource. New Phytol 157:423–447. https://doi.org/10.1046/j.1469-8137.2003.00695.x
Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: Mechanisms, implications, and nitrogen-phosphorus interactions. Ecol Appl 20(1):5–15. https://doi.org/10.1890/08-0127.1
Wang D, Zhu Z, Shahbaz M, Chen L, Liu S, Inubushi K, Wu J, Ge T (2019) Split N and P addition decreases straw mineralization and the priming effect of a paddy soil: a 100-day incubation experiment. Biol Fertil Soils 55(7):701–7012. https://doi.org/10.1007/s00374-019-01383-6
Wei X, Hu Y, Peng P, Zhu Z, Atere CT, O’Donnell AG, Wu J, Ge T (2017) Effect of P stoichiometry on the abundance of nitrogen-cycle genes in phosphorus-limited paddy soil. Biol Fertil Soils 53(7):767–776. https://doi.org/10.1007/s00374-017-1221-1
Wei X, Razavi BS, Hu Y, Xu X, Zhu Z, Liu Y, Wu J, Ge T (2019b) C/P stoichiometry of dying rice root defines the spatial distribution and dynamics of enzyme activities in root-detritusphere. Biol Fertil Soils 55(3):251–263. https://doi.org/10.1007/s00374-019-01345-y
Wei L, Razavi BS, Wang W, Zhu Z, Liu S, Wu J, Kuzyakov Y, Ge T (2019c) Labile carbon matters more than temperature for enzyme activity in paddy soil. Soil Biol Biochem 135:134–143. https://doi.org/10.1016/j.soilbio.2019.04.016
Wei X, Zhu Z, Liu Y, Luo Y, Deng Y, Xu X, Liu S, Richter A, Shibistova O, Guggenberger G, Wu J, Ge T (2020) C:N: P stoichiometry regulates soil organic carbon mineralization and concomitant shifts in microbial community composition in paddy soil. Biol Fertil Soils 56(8):1093–1107. https://doi.org/10.1007/s00374-020-01468-7
Wei X, Ge T, Zhu Z, Hu Y, Liu S, Li Y, Wu J, Razavi BS (2019a) Expansion of rice enzymatic rhizosphere: temporal dynamics in response to phosphorus and cellulose application. Plant Soil 169–181 https://doi.org/10.1007/s11104-018-03902-0
Wu J, Huang M, Xiao HA, Su YR, Tong CL, Huang DY, Syers JK (2007) Dynamics in microbial immobilization and transformations of phosphorus in highly weathered subtropical soil following organic amendments. Plant Soil 290:333–342. https://doi.org/10.1007/s11104-006-9165-5
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(6):737–749. https://doi.org/10.1111/geb.12029
Yapiyev V, Sagintayev Z, Verhoef A, Kassymbekova A, Baigaliyeva M, Zhumabayev D, Malgazhdar D, Abudanash D, Ongdas N, Jumassultanova S (2017) The changing water cycle: Burabay National Nature Park, Northern Kazakhstan. Wiley Interdisc Rev: Water 4(5):e1227. https://doi.org/10.1002/wat2.1227
Yuan H, Liu S, Razavi BS, Zhran M, Wang J, Zhu Z, Wu J, Ge T (2019) Differentiated response of plant and microbial C: N: P stoichiometries to phosphorus application in phosphorus-limited paddy soil. Euro J Soil Biol 95:103122. https://doi.org/10.1016/j.ejsobi.2019.103122
Zang H, Wang J, Kuzyakov Y (2016) N fertilization decreases soil organic matter decomposition in the rhizosphere. Appl Soil Ecol 108:47–53. https://doi.org/10.1016/j.apsoil.2016.07.021
Zhang L, Ding X, Chen S, He X, Zhang F, Feng G (2014) Reducing carbon: Phosphorus ratio can enhance microbial phytin mineralization and lessen competition with maize for phosphorus. J Plant Interact 9(1):850–856. https://doi.org/10.1080/17429145.2014.977831
Zhang SB, Fang YY, Kawasaki A, Tavakkoli E, Cai YJ, Wang HL, Ge TD, Zhou JS, Yu B, Li YF (2023) Biochar significantly reduced nutrient-induced positive priming in a subtropical forest soil. Biol Fertil Soils. https://doi.org/10.1007/s00374-023-01723-7
Zhu Z, Zeng G, Ge T, Hu Y, Tong C, Shibistova O, He X, Wang J, Guggenberger G, Wu J (2016) Fate of rice shoot and root residues, rhizodeposits, and microbe-assimilated carbon in paddy soil - Part 1: Decomposition and priming effect. Biogeosciences 13(15):4481–4489. https://doi.org/10.5194/bg-13-4481-2016
Zhu Z, Ge T, Liu S, Hu Y, Ye R, Xiao M, Tong C, Kuzykov Y, Wu J (2018a) Rice rhizodeposits affect organic matter priming in paddy soil: The role of N fertilization and plant growth for enzyme activities, CO2 and CH4 emissions. Soil Biol Biochem 116:369–377. https://doi.org/10.1016/j.soilbio.2017.11.001
Zhu Z, Ge T, Luo Y, Liu S, Xu X, Tong C, Shibistova O, Guggenberger G, Wu J (2018b) Microbial stoichiometric flexibility regulates rice straw mineralization and its priming effect in paddy soil. Soil Biol Biochem 121:67–76. https://doi.org/10.1016/j.soilbio.2018.03.003
Acknowledgements
We gratefully acknowledge the German Ministry of Education and Science (BMBF) for funding the study in the framework of the CLIENT II program within the project ReKKS (funding number 01LZ1704A). Yuhuai Liu is grateful for financial support by the Chinese National Study Abroad Fund. We thank Institute of Soil Science, Leibniz University Hannover for technical assistance.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Yuhuai Liu and Leopold Sauheitl. The first draft of the manuscript was written by Yuhuai Liu and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Competing interests
The authors have no relevant financial or non-financial interests to disclose.
Additional information
Responsible Editor: Hans Lambers.
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Liu, Y., Shibistova, O., Cai, G. et al. Microbial response on changing C:P stoichiometry in steppe soils of Northern Kazakhstan. Plant Soil 493, 375–389 (2023). https://doi.org/10.1007/s11104-023-06235-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-023-06235-9