Abstract
Regular application of mineral and organic fertilizers is one of the essential components of agricultural intensification. The application of fertilizers leads to the artificial enrichment of the soil with readily available substrates and biophilic elements, which can have a significant impact on the soil and rhizosphere microbiome. We studied the impact of different fertilizer systems on the quantitative parameters of various microbial groups in a soddy-podzolic soil (Umbric Albic Retisol) and the rhizosphere of potatoes and barley. The study was carried out on a long-term field experiment, in which mineral (NPK), organic (manure), and mixed (NPK + manure) fertilizer systems had been applied since 1968. The application of organic fertilizers increased the microbial biomass carbon (Cmic) in the bulk soil and the rhizosphere by 25–100% compared to the soil without fertilizers, while the use of mineral fertilizers, on the contrary, decreased the microbial biomass by 10–30%. Basal respiration and metabolic quotient (qСО2) increased in the following order: without fertilizers < NPK < NPK + manure < manure. The gene copy numbers of bacteria, archaea, and fungi significantly increased (by 1.5–2.5 times) under organic fertilizers and decreased (2–2.5 times) under NPK. The fungi/bacteria ratios varied from 32 to 100 and from 0.10 to 0.92 according to luminescent microscopy and quantitative PCR methods, respectively. The lowest ratios were revealed for variants with NPK, and the highest fungi/bacteria ratios were in variants with manure. Thus, the applied doses of mineral fertilizers should be compensated by the addition of fresh organic matter in order to maintain the stability of the soil—microorganisms—plant system.
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REFERENCES
N. D. Ananyeva, E. A. Susyan, and E. G. Gavrilenko, “Determination of the soil microbial biomass carbon using the method of substrate-induced respiration,” Eurasian Soil Sci. 44 (11), 1215–1221 (2011).
N. D. Ananyeva, L. M. Polyanskaya, E. V. Stolnikova, and D. G. Zvyagintzev, “Fungal to bacterial biomass ratio in the forests soil profile,” Biol. Bull. (Moscow) 37 (3), 254–262 (2010).
E. V. Blagodatskaya, M. V. Semenov, and A. V. Yakushev, Activity and Biomass of Soil Microorganisms under Changing Environmental Conditions (Tov. Nauchn. Izd. KMK, Moscow, 2016) [in Russian].
I. V. Yevdokimov, “Dynamics of the rhizosphere effect in soils,” Eurasian Soil Sci. 46 (6), 676–684 (2013). https://doi.org/10.1134/S1064229313060021
B. M. Kogut, M. A. Yashin, V. M. Semenov, T. N. Avdeeva, L. G. Markina, S. M. Lukin, and S. I. Tarasov, “Distribution of transformed organic matter in structural units of loamy sandy soddy-podzolic soil,” Eurasian Soil Sci. 49 (1), 45–55 (2016). https://doi.org/10.1134/S1064229316010075
V. N. Kudeyarov and V. M. Semenov, “Problems of agrochemistry and the current state of chemicalization of agricultural production in the Russian Federation,” Agrokhimiya, No. 10, 3–17 (2014).
S. M. Lukin, E. I. Zolkina, and E. V. Marchuk, “The influence of long-term use of fertilizers on the productivity of crop rotation, the content and qualitative composition of soil organic matter,” Plodorodie 3 (120), 93–98 (2021). https://doi.org/10.25680/S19948603.2021.120.18
L. M. Polyanskaya, S. M. Lukin, and D. G. Zvyagintsev, “The change in composition of microbial biomass in cultivated soils,” Eurasian Soil Sci. 30 (2), 172–177 (1997).
V. M. Semenov, T. N. Lebedeva, N. B. Zinyakova, D. A. Sokolov, and M. V. Semenov, “Eutrophication of arable soil: a comparative effect of mineral and organic fertilizer systems,” Eurasian Soil Sci. 56 (1), 49–62 (2023).
M. V. Semenov, D. A. Nikitin, A. L. Stepanov, and V. M. Semenov, “The structure of bacterial and fungal communities in the rhizosphere and root-free loci of gray forest soil,” Eurasian Soil Sci. 52 (3), 319–332 (2019). https://doi.org/10.1134/S1064229319010137
M. V. Semenov, “Metabarcoding and metagenomics in soil ecology research: achievements, challenges, and prospects,” Biol. Bull. Rev. 11 (1), 40–53 (2021). https://doi.org/10.1134/S2079086421010084
C. Ai, G. Liang, J. Sun, X. Wang, P. He, W. Zhou, and X. He, “Reduced dependence of rhizosphere microbiome on plant-derived carbon in 32-year long-term inorganic and organic fertilized soils,” Soil Biol. Biochem. 80, 70–78 (2015). https://doi.org/10.1016/j.soilbio.2014.09.028
M. N. Ashraf, C. Hu, L. Wu, Y. Duan, W. Zhang, T. Aziz, A. Cai, M. M. Abrar, and M. Xu, “Soil and microbial biomass stoichiometry regulate soil organic carbon and nitrogen mineralization in rice-wheat rotation subjected to long-term fertilization,” J. Soils Sediments 20, 3103–3113 (2020). https://doi.org/10.1007/s11368-020-02642-y
V. L. Bailey, J. L. Smith, and H. Bolton Jr., “Fungal-to-bacterial ratios in soils investigated for enhanced C sequestration,” Soil Biol. Biochem. 34, 997–1007 (2002). https://doi.org/10.1016/S0038-0717(02)00033-0
D. P. Bebber and V. R. Richards, “A meta-analysis of the effect of organic and mineral fertilizers on soil microbial diversity,” Appl. Soil Ecol. 175, 104450 (2022). https://doi.org/10.1016/j.apsoil.2022.104450
R. L. Berendsen, C. M. Pieterse, and P. A. Bakker, “The rhizosphere microbiome and plant health,” Trends Plant Sci. 17, 478–486 (2012). https://doi.org/10.1016/j.tplants.2012.04.001
B. S. Brar, J. Singh, G. Singh, and G. Kaur, “Effects of long-term application of inorganic and organic fertilizers on soil organic carbon and physical properties in maize–wheat rotation,” Agronomy 5, 220–238 (2015). https://doi.org/10.3390/agronomy5020220
L. G. Carvalheiro, J. C. Biesmeijer, M. Franzén, J. Aguirre-Gutiérrez, L. A. Garibaldi, A. Helm, D. Michez, J. Pöyry, M. Reemer, O. Schweiger, L. van den Berg, M. Wallisdevries, and W. E. Kunin, “Soil eutrophication shaped the composition of pollinator assemblages during the past century,” Ecography 43, 209–221 (2020). https://doi.org/10.1111/ecog.04656
C. Chenu, D. A. Angers, P. Barré, D. Derrien, D. Arrouays, and J. Balesdent, “Increasing organic stocks in agricultural soils: knowledge gaps and potential innovations,” Soil Tillage Res. 188, 41–52 (2019). https://doi.org/10.1016/j.still.2018.04.011
P. Dang, C. Li, C. Lu, M. Zhang, T. Huang, C. Wan, H. Wang, Y. Chen, X. Qin, Y. Liao, and K. H. M. Siddique, “Effect of fertilizer management on the soil bacterial community in agroecosystems across the globe,” Agric., Ecosyst. Environ. 326, 107795 (2022). https://doi.org/10.1016/j.agee.2021.107795
M. Diacono and F. Montemurro, “Long-term effects of organic amendments on soil fertility. a review,” Agron. Sustainable Dev. 30, 401–422 (2010). https://doi.org/10.1007/978-94-007-0394-0_34
L. C. Dincă, P. Grenni, C. Onet, and A. Onet, “Fertilization and soil microbial community: a review,” Appl. Sci. 12, 1198 (2022). https://doi.org/10.3390/app12031198
J. Ding, X. Jiang, D. Guan, B. Zhao, M. Ma, B. Zhou, F. Cao, X. Yang, L. Li, and J. Li, “Influence of inorganic fertilizer and organic manure application on fungal communities in a long-term field experiment of Chinese Mollisols,” Appl. Soil Ecol. 111, 114–122 (2017). https://doi.org/10.1016/j.apsoil.2016.12.003
W. Y. Dong, X. Y. Zhang, X. Q. Dai, X. L. Fu, F. T. Yang, X. Y. Liu, and S. Schaeffer, “Changes in soil microbial community composition in response to fertilization of paddy soils in subtropical China,” Appl. Soil Ecol. 84, 140–147 (2014). https://doi.org/10.1016/j.apsoil.2014.06.007
N. Fierer, “Embracing the unknown: disentangling the complexities of the soil microbiome,” Nat. Rev. Microbiol. 15, 579–590 (2017). https://doi.org/10.1038/nrmicro.2017.87
G. Ge, Z. Li, F. Fan, G. Chu, Z. Hou, and Y. Liang, “Soil biological activity and their seasonal variations in response to long-term application of organic and inorganic fertilizers,” Plant Soil 326, 31–44 (2010). https://doi.org/10.1007/s11104-009-0186-8
Y. Ge, J. B. Zhang, L. M. Zhang, M. Yang, and J. Z. He, “Long-term fertilization regimes affect bacterial community structure and diversity of an agricultural soil in northern China,” J. Soils Sediments 8, 43–50 (2008). https://doi.org/10.1065/jss2008.01.270
D. Geisseler and K. M. Scow, “Long-term effects of mineral fertilizers on soil microorganisms – a review,” Soil Biol. Biochem. 75, 54–63 (2014). https://doi.org/10.1016/j.soilbio.2014.03.023
Z. Guo, “Fertilization regime has a greater effect on soil microbial community structure than crop rotation and growth stage in an agroecosystems,” Appl. Soil Ecol. 149, 103510 (2020). https://doi.org/10.1016/j.apsoil.2020.103510
M. Hartmann, B. Frey, J. Mayer, P. Mäder, and F. Widmer, “Distinct soil microbial diversity under long-term organic and conventional farming,” ISME J. 9, 1177–1194 (2015). https://doi.org/10.1038/ismej.2014.210
J. Hu, X. Lin, J. Wang, J. Dai, R. Chen, J. Zhang, and M. H. Wong, “Microbial functional diversity, metabolic quotient, and invertase activity of a sandy loam soil as affected by long-term application of organic amendment and mineral fertilizer,” J. Soils Sediments 11, 271–280 (2011). https://doi.org/10.1007/s11368-010-0308-1
R. Huang, S. P. McGrath, P. R. Hirsch, I. M. Clark, J. Storkey, L. Wu, J. Zhou, and Y. Liang, “Plant–microbe networks in soil are weakened by century-long use of inorganic fertilizers,” Microb. Biotechnol. 12, 1464–1475 (2019). https://doi.org/10.1111/1751-7915.13487
Y. Kuzyakov and E. Blagodatskaya, “Microbial hotspots and hot moments in soil: concept & review,” Soil Biol. Biochem. 83, 184–199 (2015). https://doi.org/10.1016/j.soilbio.2015.01.025
C. L. Lauber, M. Hamady, R. Knight, and N. Fierer, “Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale,” Appl. Environ. Microbiol. 75 (15), 5111–5120 (2009). https://doi.org/10.1128/AEM.00335-09
C. Lazcano, M. Gómez-Brandón, P. Revilla, and J. Domínguez, “Short-term effects of organic and inorganic fertilizers on soil microbial community structure and function,” Biol. Fertil. Soils 49, 723–733 (2013). https://doi.org/10.1007/s00374-012-0761-7
L. Liu, C. Li, S. Zhu, Y. Xu, H. Li, X. Zheng, and R. Shi, “Combined application of organic and inorganic nitrogen fertilizers affects soil prokaryotic communities compositions,” Agronomy 10, 132 (2020). https://doi.org/10.3390/agronomy10010132
S. Liu, J. Wang, S. Pu, E. Blagodatskaya, Y. Kuzyakov, and B. Razavi, “Impact of manure on soil biochemical properties: a global synthesis,” Sci. Total Environ., 141003 (2020). https://doi.org/10.1016/j.scitotenv.2020.141003
H. Luan, W. Gao, S. Huang, J. Tang, M. Li, H. Zhang, and D. Masiliūnas, “Substitution of manure for chemical fertilizer affects soil microbial community diversity structure and function in greenhouse vegetable production systems,” PLoS One 15, e0214041 (2020). https://doi.org/10.1371/journal.pone.0214041
Q. Ma, Y. Wen, D. Wang, X. Sun, P. W. Hill, A. Macdonald, D. R. Chadwick, L. Wu, and D. L. Jones, “Farmyard manure applications stimulate soil carbon and nitrogen cycling by boosting microbial biomass rather than changing its community composition,” Soil Biol. Biochem. 144, 107760 (2020). https://doi.org/10.1016/j.soilbio.2020.107760
A. A. Malik, S. Chowdhury, V. Schlager, A. Oliver, J. Puissant, P. G. Vazquez, N. Jehmlich, M. Bergen, R. I. Griffiths, G. Gleixner, and G. Gleixner, “Soil fungal: bacterial ratios are linked to altered carbon cycling,” Front. Microbiol. 7, 1247 (2016). https://doi.org/10.3389/fmicb.2016.01247
R. Mendes, P. Garbeva, and J. M. Raaijmakers, “The rhizosphere microbiome: significance of plant beneficial plant pathogenic and human pathogenic microorganisms,” FEMS Microbiol. Rev. 37, 634–663 (2013). https://doi.org/10.1111/1574-6976.12028
J. Pöyry, L. G. Carvalheiro, R. K. Heikkinen, I. Kühn, M. Kuussaari, O. Schweiger, P. M. van Bodegom, A. Valtonen, M. Franzén, “The effects of soil eutrophication propagate to higher trophic levels,” Global Ecol. Biogeogr. 26, 18–30 (2017). https://doi.org/10.1111/geb.12521
K. S. Ramirez, C. L. Lauber, R. Knight, M. A. Bradford, and N. Fierer, “Consistent effects of nitrogen fertilization on soil bacterial communities in contrasting systems,” Ecology 91, 3463–3470 (2010). https://doi.org/10.1890/10-0426.1
J. Rousk, E. Bååth, P. C. Brookes, C. L. Lauber, C. Lozupone, J. G. Caporaso, et al., “Soil bacterial and fungal communities across a pH gradient in an arable soil,” ISME J. 4, 1340–1351 (2010). https://doi.org/10.1038/ismej.2010.58
M. V. Semenov, G. S. Krasnov, V. M. Semenov, and A. H. van Bruggen, “Long-term fertilization rather than plant species shapes rhizosphere and bulk soil prokaryotic communities in agroecosystems,” Appl. Soil Ecol. 154, 103641 (2020). https://doi.org/10.1016/j.apsoil.2020.103641
M. V. Semenov, G. S. Krasnov, V. M. Semenov, N. Ksenofontova, N. B. Zinyakova, and A. H. van Bruggen, “Does fresh farmyard manure introduce surviving microbes into soil or activate soil-borne microbiota?,” J. Environ. Manage. 294, 113018 (2021). https://doi.org/10.1016/j.jenvman.2021.113018
M. V. Semenov, G. S. Krasnov, V. M. Semenov, and A. van Bruggen, “Mineral and organic fertilizers distinctly affect fungal communities in the crop rhizosphere,” J. Fungi 8, 251 (2022). https://doi.org/10.3390/jof8030251
J. Six, S. D. Frey, R. K. Thiet, and K. M. Batten, “Bacterial and fungal contributions to carbon sequestration in agroecosystems,” Soil Sci. Soc. Am. J. 70, 555–569 (2006). https://doi.org/10.2136/sssaj2004.0347
M. Soares and J. Rousk, “Microbial growth and carbon use efficiency in soil: Links to fungal-bacterial dominance, SOC-quality and stoichiometry,” Soil Biol. Biochem. 131, 195–205 (2019). https://doi.org/10.1016/j.soilbio.2019.01.010
J. F. Toljander, J. C. Santos-González, A. Tehler, and R. D. Finlay, “Community analysis of arbuscular mycorrhizal fungi and bacteria in the maize mycorrhizosphere in a long-term fertilization trial,” FEMS Microbiol. Ecol. 65, 323–338 (2008). https://doi.org// j.1574-6941.2008.00512.xhttps://doi.org/10.1111/j.1574-6941.2008.00512.x10.1111
D. L. Valentine, “Adaptations to energy stress dictate the ecology and evolution of the Archaea,” Nat. Rev. Microbiol. 5, 316–323 (2007). https://doi.org/10.1038/nrmicro1619
L. van Overbeek and J. D. Van Elsas, “Effects of plant genotype and growth stage on the structure of bacterial communities associated with potato (Solanum tuberosum L.),” FEMS Microbiol. Ecol. 64, 283–296 (2008). https://doi.org/6941.2008.00469.xhttps://doi.org/10.1111/j.1574-6941.2008.00469.x10.1111/j.1574
L. Wang, F. E. Y. Yang, J. Yuan, W. Raza, Q. Huang, and Q. Shen, “Long-term application of bioorganic fertilizers improved soil biochemical properties and microbial communities of an apple orchard soil,” Front. Microbiol. 7, 1893 (2016). https://doi.org/10.3389/fmicb.2016.01893
J. Wu, C. Sha, M. Wang, C. Ye, P. Li, and S. Huang, “Effect of organic fertilizer on soil bacteria in maize fields,” Land 10, 328 (2021). https://doi.org/10.3390/land10030328
X. Xiang, J. Liu, J. Zhang, D. Li, C. Xu, and Y. Kuzyakov, “Divergence in fungal abundance and community structure between soils under long-term mineral and organic fertilization,” Soil Tillage Res. 196, 104491 (2020). https://doi.org/10.1016/j.still.2019.104491
X. Zhang, W. Dong, X. Dai, S. Schaeffer, F. Yang, M. Radosevich, L. Xu, X. Liu, and X. Sun, “Responses of absolute and specific soil enzyme activities to long term additions of organic and mineral fertilizer,” Sci. Total Environ. 536, 59–67 (2015). https://doi.org/10.1016/j.scitotenv.2015.07.043
Z. Zhou, C. Wang, and Y. Luo, “Meta-analysis of the impacts of global change factors on soil microbial diversity and functionality,” Nat. Commun. 11, 1–10 (2020). https://doi.org/10.1038/s41467-020-16881-7
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This study was supported by the Russian Science Foundation, project no. 21-76-10025 (https://rscf.ru/en/project/ 21-76-10025/).
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Semenov, M.V., Ksenofontova, N.A., Nikitin, D.A. et al. Microbiological Parameters of Soddy-Podzolic Soil and Its Rhizosphere in a Half-Century Field Experiment with Different Fertilizer Systems. Eurasian Soil Sc. 56, 756–768 (2023). https://doi.org/10.1134/S1064229323600070
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DOI: https://doi.org/10.1134/S1064229323600070