Organic fertilizers shape the bacterial communities harboring pqqC and phoD genes by altering organic acids, leading to improved phosphorus utilization

Abstract

The management of phosphorus (P) is challenged by the disruption of the soil natural phosphorus cycle, primarily due to over-fertilization. However, less research has been done on how fertilization affects organic acids secreted by roots, which in turn affects bacteria harboring the pqqC and phoD genes. Employing high-throughput sequencing and quantitative PCR, we analyzed the impact of various fertilizer treatments on these bacterial communities. Our research reveals that both organic and inorganic fertilizers alter soil pH, a change that is closely linked to changes in oxalic, gluconic, and succinic acids in the soil. These secretions subsequently modify the composition of pqqC and phoD-harboring bacterial communities, thereby enhancing P solubilization. Our findings suggest that while inorganic fertilizers can increase P-solubilizing bacterial populations by elevating soil pH, organic fertilizers not only boost these bacterial communities but also maintain the P content in the soil, thereby directly supporting P utilization. After the application of organic fertilizers, the content of lactic acid and gluconic acid can not only indirectly affect the abundance of P solubilizing bacteria by increasing soil pH, but also directly increase the effective P content of the soil. Additionally, the introduction of nitrogen (N) and potassium (K) alongside P fertilization appears to fine-tune this microbial-plant interaction, paving the way for more efficient P use in agriculture. Consequently, our research provides sustainable strategies for enhancing agricultural productivity amid P management challenges.

Graphical abstract

Keywords

phosphate fertilizer / P solubilization / plant root exudates / phoD-harboring bacteria / pqqC-harboring bacteria / fertilizer treatments

Highlight

	● Root secretions interact with microbes during fertilizer application.
	● Inorganic fertilizers boost phosphorus-solubilizing bacteria abundance by raising pH.
	● Organic fertilizers directly affect soil’s available phosphorus.
	● Lactic acid post-fertilization alters pH, affecting phosphorus bacteria.

References

[1] Adeleke, R., Nwangburuka, C., Oboirien, B., 2017. Origins, roles and fate of organic acids in soils: a review. South African Journal of Botany108, 393–406.

[2] Bi, Q.F., Li, K. J., Zheng, B.X., Liu, X.P., Li, H.Z., Jin, B.J., Ding, K., Yang, X.R., Lin, X.Y., Zhu, Y.G., 2020. Partial replacement of inorganic phosphorus (P) by organic manure reshapes phosphate mobilizing bacterial community and promotes P bioavailability in a paddy soil. Science of the Total Environment703, 134977.

[3] Buchfink, B., Xie, C., Huson, D.H., 2015. Fast and sensitive protein alignment using DIAMOND. Nature Methods12, 59–60.

[4] Chen, W.J., Zhan, Y.B., Zhang, X.J., Shi, X., Wang, Z.G., Xu, S.Q., Chang, Y., Ding, G.C., Li, J., Wei, Y.Q., 2022. Influence of carbon-to-phosphorus ratios on phosphorus fractions transformation and bacterial community succession in phosphorus-enriched composting. Bioresource Technology362, 127786.

[5] Colwell, J.D., 1963. The estimation of the phosphorus fertilizer requirements of wheat in southern New South Wales by soil analysis. Australian Journal of Experimental Agriculture and Animal Husbandry3, 190–197.

[6] Cordell, D., White, S., 2014. Life's bottleneck: sustaining the world's phosphorus for a food secure future. Annual Review of Environment and Resources39, 161–188.

[7] Dai, Z.M., Liu, G.F., Chen, H.H., Chen, C.R., Wang, J.K., Ai, S.Y., Wei, D., Li, D.M., Ma, B., Tang, C.X., Brookes, P.C., Xu, J.M., 2020. Long-term nutrient inputs shift soil microbial functional profiles of phosphorus cycling in diverse agroecosystems. The ISME Journal14, 757–770.

[8] de Oliveira Mendes, G., Murta, H.M., Valadares, R.V., da Silveira, W.B., da Silva, I.R., Costa, M.D., 2020. Oxalic acid is more efficient than sulfuric acid for rock phosphate solubilization. Minerals Engineering155, 106458.

[9] Dotaniya, M.L., Datta, S.C., Biswas, D.R., Meena, B.P., 2013. Effect of solution phosphorus concentration on the exudation of oxalate ions by wheat (Triticum aestivum L. ). Proceedings of the National Academy of Sciences, India Section B: Biological Sciences83, 305–309.

[10] Edgar, R.C., 2018. Updating the 97% identity threshold for 16S ribosomal RNA OTUs. Bioinformatics34, 2371–2375.

[11] Edwards, J., Johnson, C., Santos-Medellín, C., Lurie, E., Podishetty, N.K., Bhatnagar, S., Eisen, J.A., Sundaresan, V., 2015. Structure, variation, and assembly of the root-associated microbiomes of rice. Proceedings of the National Academy of Sciences of the United States of America112, E911–E920.

[12] Fadrosh, D.W., Ma, B., Gajer, P., Sengamalay, N., Ott, S., Brotman, R.M., Ravel, J., 2014. An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform. Microbiome2, 6.

[13] Falkowski, P.G., Fenchel, T., Delong, E.F., 2008. The microbial engines that drive Earth's biogeochemical cycles. Science320, 1034–1039.

[14] George, T.S., Giles, C.D., Menezes-Blackburn, D., Condron, L.M., Gama-Rodrigues, A.C., Jaisi, D., Lang, F., Neal, A.L., Stutter, M.I., Almeida, D.S., Bol, R., Cabugao, K.G., Celi, L., Cotner, J.B., Feng, G., Goll, D.S., Hallama, M., Krueger, J., Plassard, C., Rosling, A., Darch, T., Fraser, T., Giesler, R., Richardson, A.E., Tamburini, F., Shand, C.A., Lumsdon, D.G., Zhang, H., Blackwell, M.S.A., Wearing, C., Mezeli, M.M., Almås, Å.R., Audette, Y., Bertrand, I., Beyhaut, E., Boitt, G., Bradshaw, N., Brearley, C.A., Bruulsema, T.W., Ciais, P., Cozzolino, V., Duran, P.C., Mora, M.L., De Menezes, A.B., Dodd, R.J., Dunfield, K., Engl, C., Frazão, J.J., Garland, G., González Jiménez, J.L., Graca, J., Granger, S.J., Harrison, A.F., Heuck, C., Hou, E.Q., Johnes, P. J., Kaiser, K., Kjær, H.A., Klumpp, E., Lamb, A.L., Macintosh, K.A., Mackay, E.B., Mcgrath, J., Mcintyre, C., Mclaren, T., Mészáros, E., Missong, A., Mooshammer, M., Negrón, C.P., Nelson, L.A., Pfahler, V., Poblete-Grant, P., Randall, M., Seguel, A., Seth, K., Smith, A.C., Smits, M.M., Sobarzo, J.A., Spohn, M., Tawaraya, K., Tibbett, M., Voroney, P., Wallander, H., Wang, L., Wasaki, J., Haygarth, P.M., 2018. Organic phosphorus in the terrestrial environment: a perspective on the state of the art and future priorities. Plant and Soil427, 191–208.

[15] Hasegawa, S., Ryan, M.H., Power, S.A., 2023. CO₂ concentration and water availability alter the organic acid composition of root exudates in native Australian species. Plant and Soil485, 507–524.

[16] Honvault, N., Houben, D., Nobile, C., Firmin, S., Lambers, H., Faucon, M.P., 2021. Tradeoffs among phosphorus-acquisition root traits of crop species for agroecological intensification. Plant and Soil461, 137–150.

[17] Hu, X.J., Gu, H.D., Liu, J.J., Wei, D., Zhu, P., Cui, X.A., Zhou, B.K., Chen, X.L., Jin, J., Liu, X.B., Wang, G.H., 2023. Metagenomic strategies uncover the soil bioavailable phosphorus improved by organic fertilization in Mollisols. Agriculture, Ecosystems & Environment349, 108462.

[18] Jiang, N., Wei, K., Pu, J.H., Huang, W.J., Bao, H.X., Chen, L.J., 2021. A balanced reduction in mineral fertilizers benefits P reserve and inorganic P-solubilizing bacterial communities under residue input. Applied Soil Ecology159, 103833.

[19] Jiao, S., Chen, W.M., Wang, J.L., Du, N.N., Li, Q.P., Wei, G.H., 2018. Soil microbiomes with distinct assemblies through vertical soil profiles drive the cycling of multiple nutrients in reforested ecosystems. Microbiome6, 146.

[20] Jin, J., Krohn, C., Franks, A.E., Wang, X.J., Wood, J.L., Petrovski, S., McCaskill, M., Batinovic, S., Xie, Z.H., Tang, C.X., 2022. Elevated atmospheric CO₂ alters the microbial community composition and metabolic potential to mineralize organic phosphorus in the rhizosphere of wheat. Microbiome10, 12.

[21] Jones, D.L., Oburger, E., 2011. Solubilization of phosphorus by soil microorganisms. In: Bünemann, E., Oberson, A., Frossard, E., eds. Phosphorus in Action. Berlin: Springer, 169–198.

[22] Kour, D., Rana, K.L., Kaur, T., Yadav, N., Yadav, A.N., Kumar, M., Kumar, V., Dhaliwal, H.S., Saxena, A.K., 2021. Biodiversity, current developments and potential biotechnological applications of phosphorus-solubilizing and -mobilizing microbes: a review. Pedosphere31, 43–75.

[23] Li, L., Zhang, L.Z., Zhang, F.S., 2013. Crop mixtures and the mechanisms of overyielding. In: Levin, S.A., ed. Encyclopedia of Biodiversity. 2nd ed. Amsterdam: Academic Press, 382–395.

[24] Ling, N., Wang, T.T., Kuzyakov, Y., 2022. Rhizosphere bacteriome structure and functions. Nature Communications13, 836.

[25] Liu, E.K., Yan, C.R., Mei, X.R., He, W.Q., Bing, S.H., Ding, L.P., Liu, Q., Liu, S., Fan, T.L., 2010. Long-term effect of chemical fertilizer, straw, and manure on soil chemical and biological properties in northwest China. Geoderma158, 173–180.

[26] Liu, J.S., Ma, Q., Hui, X.L., Ran, J.Y., Ma, Q.X., Wang, X.S., Wang, Z.H., 2020. Long-term high-P fertilizer input decreased the total bacterial diversity but not phoD-harboring bacteria in wheat rhizosphere soil with available-P deficiency. Soil Biology and Biochemistry149, 107918.

[27] Luo, G.W., Ling, N., Nannipieri, P., Chen, H., Raza, W., Wang, M., Guo, S.W., Shen, Q.R., 2017. Long-term fertilisation regimes affect the composition of the alkaline phosphomonoesterase encoding microbial community of a vertisol and its derivative soil fractions. Biology and Fertility of Soils53, 375–388.

[28] Meyer, J.B., Frapolli, M., Keel, C., Maurhofer, M., 2011. Pyrroloquinoline quinone biosynthesis gene pqqC, a novel molecular marker for studying the phylogeny and diversity of phosphate-solubilizing pseudomonads. Applied and Environmental Microbiology77, 7345–7354.

[29] Penuelas, J., Janssens, I.A., Ciais, P., Obersteiner, M., Sardans, J., 2020. Anthropogenic global shifts in biospheric N and P concentrations and ratios and their impacts on biodiversity, ecosystem productivity, food security, and human health. Global Change Biology26, 1962–1985.

[30] Peñuelas, J., Poulter, B., Sardans, J., Ciais, P., van der Velde, M., Bopp, L., Boucher, O., Godderis, Y., Hinsinger, P., Llusia, J., Nardin, E., Vicca, S., Obersteiner, M., Janssens, I.A., 2013. Human-induced nitrogen-phosphorus imbalances alter natural and managed ecosystems across the globe. Nature Communications4, 2934.

[31] Pu, J.H., Jiang, N., Zhang, Y.L., Guo, L.L., Huang, W.J., Chen, L.J., 2023. Effects of various straw incorporation strategies on soil phosphorus fractions and transformations. Global Change Biology15, 88–98.

[32] Richardson, A.E., Barea, J.M., McNeill, A.M., Prigent-Combaret, C., 2009. Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant and Soil321, 305–339.

[33] Richardson, A.E., Lynch, J.P., Ryan, P.R., Delhaize, E., Smith, F.A., Smith, S.E., Harvey, P.R., Ryan, M.H., Veneklaas, E.J., Lambers, H., Oberson, A., Culvenor, R.A., Simpson, R.J., 2011. Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant and Soil349, 121–156.

[34] Richardson, A.E., Simpson, R.J., 2011. Soil microorganisms mediating phosphorus availability update on microbial phosphorus. Plant Physiology156, 989–996.

[35] Sharma, S.B., Sayyed, R.Z., Trivedi, M.H., Gobi, T.A., 2013. Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. SpringerPlus2, 587.

[36] Shi, J.Y., Gong, J.R., Li, X.B., Zhang, Z.H., Zhang, W.Y., Li, Y., Song, L.Y., Zhang, S.Q., Dong, J.J., Baoyin, T.T., 2023. Phosphorus application promoted the sequestration of orthophosphate within soil microorganisms and regulated the soil solution P supply in a temperate grassland in northern China: a ³¹P NMR study. Soil and Tillage Research227, 105612.

[37] Shi, W.H., Xing, Y.J., Zhu, Y., Gao, N., Ying, Y.Q., 2022. Diverse responses of pqqC- and phoD-harbouring bacterial communities to variation in soil properties of Moso bamboo forests. Microbial Biotechnology15, 2097–2111.

[38] Tan, H., Barret, M., Mooij, M.J., Rice, O., Morrissey, J.P., 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. Biology and Fertility of Soils49, 661–672.

[39] Tian, Y., Shi, C.P., Malo, C.U., Kwatcho Kengdo, S., Heinzle, J., Inselsbacher, E., Ottner, F., Borken, W., Michel, K., Schindlbacher, A., Wanek, W., 2023. Long-term soil warming decreases microbial phosphorus utilization by increasing abiotic phosphorus sorption and phosphorus losses. Nature Communications14, 864.

[40] Wagg, C., Bender, S.F., Widmer, F., van der Heijden, M.G.A., 2014. Soil biodiversity and soil community composition determine ecosystem multifunctionality. Proceedings of the National Academy of Sciences of the United States of America111, 5266–5270.

[41] Wang, L., Wang, J., Yuan, J., Tang, Z.H., Wang, J.D., Zhang, Y.C., 2023a. Long-term organic fertilization strengthens the soil phosphorus cycle and phosphorus availability by regulating the pqqC- and phoD-harboring bacterial communities. Microbial Ecology86, 2716–2732.

[42] Wang, Y., Huang, Y.Y., Song, L., Yuan, J.H., Li, W., Zhu, Y.G., Chang, S.X., Luo, Y.Q., Ciais, P., Peñuelas, J., Wolf, J., Cade-Menun, B.J., Hu, S.J., Wang, L., Wang, D.J., Yuan, Z.W., Wang, Y.J., Zhang, J.S., Tao, Y., Wang, S.Q., Liu, G., Yan, X.Y., Zhu, C.W., 2023b. Reduced phosphorus availability in paddy soils under atmospheric CO₂ enrichment. Nature Geoscience16, 162–168.

[43] Wu, X.J., Peng, J.J., Liu, P.F., Bei, Q.C., Rensing, C., Li, Y., Yuan, H. M., Liesack, W., Zhang, F.S., Cui, Z.L., 2021. Metagenomic insights into nitrogen and phosphorus cycling at the soil aggregate scale driven by organic material amendments. Science of the Total Environment785, 147329.

[44] Xiao, Z.F., Han, R.X., Su, J.Q., Zhu, Z., Zhao, Y., Chen, Q.L., Zhao, J.Y., Li, G., Zhu, Y.G., 2023. Application of earthworm and silicon can alleviate antibiotic resistance in soil-Chinese cabbage system with ARGs contamination. Environmental Pollution319, 120900.

[45] Xiao, Z.F., Li, G., Zhao, Y., Xiao, K.Q., Chen, Q.L., Bao, P., Tang, J.F., Ruan, T., Zama, E.F., Xu, Y.Y., 2021. Bacterioplankton richness and composition in a seasonal Urban River. Frontiers in Environmental Science9, 731227.

[46] Yang, L., Du, L.L., Li, W.J., Wang, R., Guo, S.L., 2023. Divergent responses of phoD- and pqqC-harbouring bacterial communities across soil aggregates to long fertilization practices. Soil and Tillage Research228, 105634.

[47] Zeng, F.R., Chen, S., Miao, Y., Wu, F.B., Zhang, G.P., 2008. Changes of organic acid exudation and rhizosphere pH in rice plants under chromium stress. Environmental Pollution155, 284–289.

[48] Zheng, B.X., Zhang, D.P., Wang, Y., Hao, X.L., Wadaan, M.A.M., Hozzein, W.N., Peñuelas, J., Zhu, Y.G., Yang, X.R., 2019. Responses to soil pH gradients of inorganic phosphate solubilizing bacteria community. Scientific Reports9, 25.

[49] Zou, T., Zhang, X., Davidson, E.A., 2022. Global trends of cropland phosphorus use and sustainability challenges. Nature611, 81–87.

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