Organic matter accelerated microbial iron reduction and available phosphorus release in reflooded paddy soils

Abstract

Organic fertilization may influence soil carbon−iron (C-Fe) cycling and enhance phosphorus (P) availability, yet the direct connection between soil organic matter molecules and iron-reducing processes in long-term fertilized paddy soils remains underexplored. In this study, we conducted a microcosm experiment using paddy soils treated with six distinct fertilization regimes involving varying P and organic matter inputs up to five years. We assessed P activation under reflooding conditions, evaluated Fe reduction, and characterized dissolved organic matter (DOM) at the molecular level using Fourier transform ion cyclotron resonance mass spectrometry (FT-ICR MS), alongside profiling soil microbial community composition via high-throughput sequencing. Our findings revealed that after 25 days of reflooding, soil Olsen-P content increased by an average of 73% compared to its initial state, showing a strong correlation with the Fe reduction process. Specifically, treatments involving pig manure application exhibited higher Fe reduction rates and enhanced P activation, highlighting the role of organic matter in facilitating Fe reduction. Examination of Fe-reducing microorganisms revealed that their relative abundance was decoupled from Fe reduction and P release rates, potentially due to limitations of lower soil organic matter content. Further analysis of DOM composition and network structures suggested that high-molecular-weight DOM, particularly lignin, acted as key resources for Fe-reducing microbes, thereby driving Fe reduction and promoting P release. Overall, our study highlights the crucial role of soil DOM in enabling microbial-driven Fe reduction and enhancing P availability, providing insights valuable for sustainable agricultural practices.

Graphical abstract

Keywords

manure application / P availability / soil biogeochemistry / microbial carbon mineralization / iron–carbon cycling / anaerobic soil

Highlight

	● Relative abundance of Fe-reducing bacteria decoupled from Fe reduction rate.
	● Soil phosphorus limitation contributed to the enrichment of Fe-reducing bacteria.
	● Microbial Fe reduction facilitated phosphorus release.
	● Lignin degradation accelerated microbial Fe reduction and P activation.

References

[1] Abboud, F.Y., Favaretto, N., Motta, A.C.V., Barth, G., Goularte, G.D., 2018. Phosphorus mobility and degree of saturation in oxisol under no-tillage after long-term dairy liquid manure application. Soil and Tillage Research177, 45–53.

[2] Ando, K., Yamaguchi, N., Kasuya, M., Oga, T., Ohashi, Y., Taki, K., 2022. Long-term (nearly a century) effects of fertilizer, lime and rice straw compost application on active aluminum and iron and available phosphorus in paddy fields. Geoderma424, 115992.

[3] 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.

[4] Bierke, A., Kaiser, K., Guggenberger, G., 2008. Crop residue management effects on organic matter in paddy soils — the lignin component. Geoderma146, 48–57.

[5] Borch, T., Fendorf, S., 2007. Chapter 12 phosphate interactions with iron (Hydr)oxides: mineralization pathways and phosphorus retention upon bioreduction. Developments in Earth and Environmental Sciences7, 321–348.

[6] Chen, H., Ersan, M.S., Tolić, N., Chu, R.K., Karanfil, T., Chow, A.T., 2022. Chemical characterization of dissolved organic matter as disinfection byproduct precursors by UV/fluorescence and ESI FT-ICR MS after smoldering combustion of leaf needles and woody trunks of pine (Pinus jeffreyi). Water Research209, 117962.

[7] Chen, S.S., Yang, Y.T., Jing, X.Y., Zhang, L.L., Chen, J., Rensing, C., Luan, T.G., Zhou, S.G., 2021. Enhanced aging of polystyrene microplastics in sediments under alternating anoxic-oxic conditions. Water Research207, 117782.

[8] Cordell, D., Drangert, J.O, White, S., 2009. The story of phosphorus: global food security and food for thought. Global Environmental Change19, 292–305.

[9] Csárdi, G., Nepusz, T., Traag, V., et al., 2023. igraph: network analysis and visualization.

[10] Dai, J., Tang, Z., Jiang, N., Kopittke, P.M., Zhao, F.J., Wang, P., 2020. Increased arsenic mobilization in the rice rhizosphere is mediated by iron-reducing bacteria. Environmental Pollution263, 114561.

[11] Damon, P.M., Bowden, B., Rose, T., Rengel, Z., 2014. Crop residue contributions to phosphorus pools in agricultural soils: a review. Soil Biology and Biochemistry74, 127–137.

[12] Ding, L.J., Su, J.Q., Xu, H.J., Jia, Z.J., Zhu, Y.G., 2015. Long-term nitrogen fertilization of paddy soil shifts iron-reducing microbial community revealed by RNA-13C-acetate probing coupled with pyrosequencing. The ISME Journal9, 721–734.

[13] Dong, H.L., Zeng, Q., Sheng, Y.Z., Chen, C.M., Yu, G.H., Kappler, A., 2023. Coupled iron cycling and organic matter transformation across redox interfaces. Nature Reviews Earth & Environment4, 659–673.

[14] Fritzsche, A., Bosch, J., Sander, M., Schröder, C., Byrne, J.M., Ritschel, T., Joshi, P., Maisch, M., Meckenstock, R.U., Kappler, A., Totsche, K.U., 2021. Organic matter from redoximorphic soils accelerates and sustains microbial Fe(III) reduction. Environmental Science & Technology55, 10821–10831.

[15] Golbeck, J., 2013. Chapter 3 - network structure and measures. In: Golbeck, J., ed. Analyzing the Social Web. Amsterdam: Elsevier, 25–44.

[16] Graves, S., Piepho, H.P., with help from Dorai-Raj, S., 2019. multcompView: visualizations of paired comparisons.

[17] He, C., Zhang, Y.H., Li, Y.Y., Zhuo, X.C., Li, Y.G., Zhang, C.L., Shi, Q., 2020. In-house standard method for molecular characterization of dissolved organic matter by FT-ICR mass spectrometry. ACS Omega5, 11730–11736.

[18] He, J.Z., Qu, D., 2008. Dissimilatory Fe(III) reduction characteristics of paddy soil extract cultures treated with glucose or fatty acids. Journal of Environmental Sciences20, 1103–1108.

[19] Jindo, K., Audette, Y., Olivares, F.L., Canellas, L.P., Smith, D.S., Paul Voroney, R., 2023. Biotic and abiotic effects of soil organic matter on the phytoavailable phosphorus in soils: a review. Chemical and Biological Technologies in Agriculture10, 29.

[20] Jr, F.E.H., 2023. Hmisc: Harrell miscellaneous. available at the website of Harrell Miscellaneous.

[21] Kappler, A., Bryce, C., Mansor, M., Lueder, U., Byrne, J.M., Swanner, E.D., 2021. An evolving view on biogeochemical cycling of iron. Nature Reviews Microbiology19, 360–374.

[22] Khan, I., Fahad, S., Wu, L., Zhou, W., Xu, P., Sun, Z., Salam, A., Imran, M., Jiang, M.D., Kuzyakov, Y., Hu, R.G., 2019. Labile organic matter intensifies phosphorous mobilization in paddy soils by microbial iron (III) reduction. Geoderma352, 185–196.

[23] Koch, B.P., Dittmar, T., 2006. From mass to structure: an aromaticity index for high-resolution mass data of natural organic matter. Rapid Communications in Mass Spectrometry20, 926–932.

[24] Kögel-Knabner, I., Amelung, W., Cao, Z.H., Fiedler, S., Frenzel, P., Jahn, R., Kalbitz, K., Kölbl, A., Schloter, M., 2010. Biogeochemistry of paddy soils. Geoderma157, 1–14.

[25] Kuczynski, J., Stombaugh, J., Walters, W.A., González, A., Caporaso, J.G., Knight, R., 2011. Using QIIME to analyze 16S rRNA gene sequences from microbial communities. Current Protocols in Bioinformatics36, 10.7.1–10.7.20.

[26] Li, J., Zhang, X.C., Luo, J.F., Lindsey, S., Zhou, F., Xie, H.T., Li, Y., Zhu, P., Wang, L.C., Shi, Y.L., He, H.B., Zhang, X.D., 2020a. Differential accumulation of microbial necromass and plant lignin in synthetic versus organic fertilizer-amended soil. Soil Biology and Biochemistry149, 107967.

[27] Li, K.J., Bi, Q.F., Liu, X.P., Wang, H.B., Sun, C.L., Zhu, Y.G., Lin, X.Y., 2022. Unveiling the role of dissolved organic matter on phosphorus sorption and availability in a 5-year manure amended paddy soil. Science of the Total Environment838, 155892.

[28] Li, L.N., Jia, R., Qu, Z., Li, T.L., Shen, W.S., Qu, D., 2020b. Coupling between nitrogen-fixing and iron(III)-reducing bacteria as revealed by the metabolically active bacterial community in flooded paddy soils amended with glucose. Science of the Total Environment716, 137056.

[29] Li, X.M., Sun, G.X., Chen, S.C., Fang, Z., Yuan, H.Y., Shi, Q., Zhu, Y.G., 2018. Molecular chemodiversity of dissolved organic matter in paddy soils. Environmental Science & Technology52, 963–971.

[30] Liang, Q.B., Chen, T., Wang, Y.X., Gao, L., Hou, L., 2022. Seasonal variation in release characteristics and mechanisms of sediment phosphorus to the overlying water in a free water surface wetland, Southwest China. Environmental Pollution308, 119612.

[31] Liu, X.P., Bi, Q.F., Qiu, L.L., Li, K.J., Yang, X.R., Lin, X.Y., 2019a. Increased risk of phosphorus and metal leaching from paddy soils after excessive manure application: insights from a mesocosm study. Science of the Total Environment666, 778–785.

[32] Liu, Y.L., Dong, Y.Q., Ge, T.D., Hussain, Q., Wang, P., Wang, J.K., Li, Y., Guggenberger, G., Wu, J.S., 2019b. Impact of prolonged rice cultivation on coupling relationship among C, Fe, and Fe-reducing bacteria over a 1000-year paddy soil chronosequence. Biology and Fertility of Soils55, 589–602.

[33] Long, J.M., Liu, F.S., Ouyang, L.Z., Chen, C.L., Han, N., Tan, Y.T., Xiao, Y., Zhou, D.S., 2024. Biochar changes iron-reducing bacteria community in paddy soils and promotes the bacterial iron reduction. Journal of Soils and Sediments24, 3656–3667.

[34] Ma, T., Yang, Z.Y., Shi, B.W., Gao, W.J., Li, Y.F., Zhu, J.X., He, J.S., 2023. Phosphorus supply suppressed microbial necromass but stimulated plant lignin phenols accumulation in soils of alpine grassland on the Tibetan Plateau. Geoderma431, 116376.

[35] Merino, C., Kuzyakov, Y., Godoy, K., Jofré, I., Nájera, F., Matus, F., 2021. Iron-reducing bacteria decompose lignin by electron transfer from soil organic matter. Science of the Total Environment761, 143194.

[36] Oksanen, J., Simpson, G.L., Blanchet, F.G., et al., 2022. vegan: community ecology package.

[37] Penn, C.J., Camberato, J.J., 2019. A critical review on soil chemical processes that control how soil pH affects phosphorus availability to plants. Agriculture9, 120.

[38] Qiu, C.P., Feng, Y.Z., Wu, M., Liu, M., Li, W.T., Li, Z.P., 2019. NanoFe₃O₄ accelerates methanogenic straw degradation by improving energy metabolism. Bioresource Technology292, 121930.

[39] Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., Glöckner, F.O., 2013. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research41, D590–D596.

[40] Rivas-Ubach, A., Liu, Y.N., Bianchi, T.S., Tolić, N., Jansson, C., Paša-Tolić, L., 2018. Moving beyond the van Krevelen Diagram: a new stoichiometric approach for compound classification in organisms. Analytical Chemistry90, 6152–6160.

[41] Sambrook, J., Russell, D.W., 2006. The Condensed Protocols from Molecular Cloning: A Laboratory Manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.

[42] Takahashi, Y., Katoh, M., 2022. Root response and phosphorus uptake with enhancement in available phosphorus level in soil in the presence of water-soluble organic matter deriving from organic material. Journal of Environmental Management322, 116038.

[43] Tfaily, M.M., Hamdan, R., Corbett, J.E., Chanton, J.P., Glaser, P.H., Cooper, W.T., 2013. Investigating dissolved organic matter decomposition in northern peatlands using complimentary analytical techniques. Geochimica et Cosmochimica Acta112, 116–129.

[44] Veneklaas, E.J., Lambers, H., Bragg, J., Finnegan, P.M., Lovelock, C.E., Plaxton, W.C., Price, C.A., Scheible, W.R., Shane, M.W., White, P.J., Raven, J.A., 2012. Opportunities for improving phosphorus-use efficiency in crop plants. New Phytologist195, 306–320.

[45] Wang, C.Q., Thielemann, L., Dippold, M.A., Guggenberger, G., Kuzyakov, Y., Banfield, C.C., Ge, T.D., Guenther, S., Bork, P., Horn, M.A., Dorodnikov, M., 2022. Microbial iron reduction compensates for phosphorus limitation in paddy soils. Science of the Total Environment837, 155810.

[46] Wang, H.B., Liu, X.P., Jin, B.J., Shu, Y.C., Sun, C.L., Zhu, Y.G., Lin, X.Y., 2024a. High-molecular-weight dissolved organic matter enhanced phosphorus availability in paddy soils: evidence from field and microcosm experiments. Soil and Tillage Research240, 106099.

[47] Wang, H.B., Liu, X.P., Shu, Y.C., Li, G., Sun, C.L., Jones, D., Zhu, Y.G., Lin, X.Y., 2024b. Molecular composition of exogenous dissolved organic matter regulates dissimilatory iron reduction and carbon emissions in paddy soil. Preprints.org Environmental Science DO1: 10.20944/preprints202409.0323.v1.

[48] Wang, Q.Q., Huang, Q., Wang, J.X., Khan, M.A., Guo, G.M., Liu, Y., Hu, S., Jin, F.M., Wang, J.F., Yu, Y.B., 2021. Dissolved organic carbon drives nutrient cycling via microbial community in paddy soil. Chemosphere285, 131472.

[49] Wang, R., Wang, X.X., Li, H., Wang, X.M., Ning, Z.P., Liu, C.S., Zhou, L.X., Zheng, G.Y., 2024c. Phase transformation of schwertmannite changes microbial iron and sulfate-reducing processes in flooded paddy soil and decreases arsenic accumulation in rice (Oryza sativa L. ). Soil Biology and Biochemistry199, 109600.

[50] Wang, S.X., Huang, Y.X., Wu, Q.F., Yao, W., Lu, Y.Y., Huang, B.C., Jin, R.C., 2024d. A review of the application of iron oxides for phosphorus removal and recovery from wastewater. Critical Reviews in Environmental Science and Technology54, 405–423.

[51] Weber, K.A., Achenbach, L.A., Coates, J.D., 2006. Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction. Nature Reviews Microbiology4, 752–764.

[52] Wilfert, P., Kumar, P.S., Korving, L., Witkamp, G.J., van Loosdrecht, M.C.M., 2015. The relevance of phosphorus and iron chemistry to the recovery of phosphorus from wastewater: a review. Environmental Science & Technology49, 9400–9414.

[53] Xu, Z.X., Lei, P., Zhai, R., Wen, Z.Q., Jin, M.J., 2019. Recent advances in lignin valorization with bacterial cultures: microorganisms, metabolic pathways, and bio-products. Biotechnology for Biofuels12, 32.

[54] Yan, M.R., Zhang, X.Z., Liu, K.L., Lou, Y.L., Wang, Y.D., 2022. Particle size primarily shifts chemical composition of organic matter under long-term fertilization in paddy soil. European Journal of Soil Science73, e13170.

[55] Yang, Y.J., Zhang, H.P., Qian, X.Q., Duan, J.N., Wang, G.L., 2017. Excessive application of pig manure increases the risk of P loss in calcic cinnamon soil in China. Science of the Total Environment609, 102–108.

[56] Yao, Y., Wang, L.L., Hemamali Peduruhewa, J., Van Zwieten, L., Gong, L.X., Tan, B.C., Zhang, G.L., 2023. The coupling between iron and carbon and iron reducing bacteria control carbon sequestration in paddy soils. CATENA223, 106937.

[57] Zhang, Z.C., Masuda, Y., Xu, Z.X., Shiratori, Y., Ohba, H., Senoo, K., 2023. Active nitrogen fixation by iron-reducing bacteria in rice paddy soil and its further enhancement by iron application. Applied Sciences13, 8156.

[58] Zheng, B.X., Ding, K., Yang, X.R., Wadaan, M.A.M., Hozzein, W.N., Peñuelas, J., Zhu, Y.G., 2019. Straw biochar increases the abundance of inorganic phosphate solubilizing bacterial community for better rape (Brassica napus) growth and phosphate uptake. Science of the Total Environment647, 1113–1120.

[59] Zhou, J.Z., Wu, L.Y., Deng, Y., Zhi, X.Y., Jiang, Y.H., Tu, Q.C., Xie, J.P., Van Nostrand, J.D., He, Z.L., Yang, Y.F., 2011. Reproducibility and quantitation of amplicon sequencing-based detection. The ISME Journal5, 1303–1313.

[60] Zhou, Y., Zhang, J.W., Xu, L., Nadeem, M.Y., Li, W.W., Jiang, Y., Ding, Y.F., Liu, Z.H., Li, G.H., 2022. Long-term fertilizer postponing promotes soil organic carbon sequestration in paddy soils by accelerating lignin degradation and increasing microbial necromass. Soil Biology and Biochemistry175, 108839.

[61] Zhu, J., Li, M., Whelan, M., 2018. Phosphorus activators contribute to legacy phosphorus availability in agricultural soils: a review. Science of the Total Environment612, 522–537.

RIGHTS & PERMISSIONS

Higher Education Press