Effects of nanoFe₃O₄ and carbon nanotubes on anaerobic decomposition of soil organic matter in paddy soil

Highlights

	● Nanoparticles inhibit anaerobic decomposition of SOM, with a more severe suppression on CO2 than CH4 production.
	● The Prolixibacteraceae in anaerobic paddy soils are sensitive to nanoparticles.
	● Microbial populations stimulated by nanoparticles probably contribute to the increase of CH4/TIC ratio in paddy soils.

Abstract

Paddy soil is frequently flooded, which leads to anaerobic decomposition of soil organic matter (SOM) to produce CO₂ and CH₄. Currently, there is limited research about the impact of nanoparticles on anaerobic SOM decomposition and CH₄ production in paddy soil. This study investigates the effects of iron oxide nanoparticles (Fe₃O₄ NPs) and multi-walled carbon nanotubes (MWCNTs) on anaerobic SOM decomposition in two paddy soils. The findings showed that addition of nanoparticles (Fe₃O₄ NPs: 0.08% and 0.3%; MWCNTs: 0.05% and 0.2%) reduced methane production by 7.48%−31.72% in Guiyang soil and 3.32%−31.24% in Fuyang soil, with decrease in SOM decomposition of 32.19%−47.87% and 19.60%−33.09%, respectively. However, the CH₄/TIC (total inorganic carbon) ratio was elevated (by 3.17% to 61.92%) after nanoparticles amendment, suggested that TIC production was more significantly suppressed than CH₄. The Prolixibacteraceae, which usually involve in organic macromolecule decomposition, decreased in relative abundance with inhibition of CH₄ production by nanoparticles in both soils, suggesting their sensitivity to nanoparticles. In contrast, the relative abundances of many microbial populations increased with the intensified inhibition of soil mineralization by nanoparticles in both soils. Especially, Sedimentibacter and Melioribacterae increased with inhibition of CH₄ by nanoparticles, and Clostridiaceae, Minicystis as well as Rhodomicrobium increased with the CH₄/TIC ratio in both soils, probably because they might provide substrates for methanogens. These results suggested that nanoparticles not only inhibit the decomposition of SOM but also change the fate of decomposed carbon through modulating microbial populations, leading to a substantial increase in the proportion of CH₄ produced from SOM decomposition.

Graphical abstract

Keywords

nanoFe₃O₄ / multi-walled carbon nanotubes / paddy soil / anaerobic decomposition / microbial community

References

[1] Ameen, F., Alsamhary, K., Alabdullatif, J.A., ALNadhari, S., 2021. A review on metal-based nanoparticles and their toxicity to beneficial soil bacteria and fungi. Ecotoxicology and Environmental Safety213, 112027.

[2] Aromokeye, D.A., Oni, O.E., Tebben, J., Yin, X.R., Richter-Heitmann, T., Wendt, J., Nimzyk, R., Littmann, S., Tienken, D., Kulkarni, A.C., Henkel, S., Hinrichs, K.U., Elvert, M., Harder, T., Kasten, S., Friedrich, M.W., 2021. Crystalline iron oxides stimulate methanogenic benzoate degradation in marine sediment-derived enrichment cultures. The ISME Journal15, 965–980.

[3] Arora, B., Attri, P., 2020. Carbon nanotubes (CNTs): a potential nanomaterial for water purification. Journal of Composites Science4, 135.

[4] Brar, S.K., Verma, M., Tyagi, R.D., Surampalli, R.Y., 2010. Engineered nanoparticles in wastewater and wastewater sludge – Evidence and impacts. Waste Management30, 504–520.

[5] Cao, J.L., Feng, Y.Z., Lin, X.G., Wang, J.H., 2016. Arbuscular mycorrhizal fungi alleviate the negative effects of iron oxide nanoparticles on bacterial community in rhizospheric soils. Frontiers in Environmental Science4, 10.

[6] Chai, M.W., Shi, F.C., Li, R.L., Liu, L.M., Liu, Y.M., Liu, F.C., 2013. Interactive effects of cadmium and carbon nanotubes on the growth and metal accumulation in a halophyte Spartina alterniflora (Poaceae). Plant Growth Regulation71, 171–179.

[7] Chen, X.T., Cui, Z.J., Zhao, Y.H., Zhu, N., Liu, Y., Hu, Z.H., Yuan, X.F., 2024. Synergistic mechanism of substrate hydrolysis and methanogenesis under “gradient anaerobic digestion” process. Energy Conversion and Management309, 118443.

[8] Conrad, R., 2009. The global methane cycle: recent advances in understanding the microbial processes involved. Environmental Microbiology Reports1, 285–292.

[9] De Volder, M.F., Tawfick, S.H., Baughman, R.H., Hart, A.J., 2013. Carbon nanotubes: present and future commercial applications. Science339, 535–539.

[10] Denisse, V.G.J., Roberto, S.C.C., Hermes, P.H., Patricio, T.G.A., Andrea, P.M., Fabián, F.L., 2021. Influence of nanoparticles on the physical, chemical, and biological properties of soils. In: Amrane, A., Mohan, D., Nguyen, T.A., Assadi, A.A., Yasin, G., eds. Nanomaterials for Soil Remediation. Amsterdam: Elsevier, 151–182.

[11] Dinesh, R., Anandaraj, M., Srinivasan, V., Hamza, S., 2012. Engineered nanoparticles in the soil and their potential implications to microbial activity. Geoderma 173–174, 173–174.

[12] Dwivedi, A.D., Dubey, S.P., Sillanpää, M., Kwon, Y.N., Lee, C., Varma, R.S., 2015. Fate of engineered nanoparticles: implications in the environment. Coordination Chemistry Reviews287, 64–78.

[13] Fadare, O.O., Wan, B., Guo, L.H., Xin, Y., Qin, W.P., Yang, Y., 2019. Humic acid alleviates the toxicity of polystyrene nanoplastic particles to Daphnia magna. Environmental Science: Nano6, 1466–1477.

[14] Faisal, S., Salama, E.S., Malik, K., Lee, S.H., Li, X.K., 2020. Anaerobic digestion of cabbage and cauliflower biowaste: impact of iron oxide nanoparticles (IONPs) on biomethane and microbial communities alteration. Bioresource Technology Reports12, 100567.

[15] García-Gómez, C., Fernández, M.D., García, S., Obrador, A.F., Letón, M., Babín, M., 2018. Soil pH effects on the toxicity of zinc oxide nanoparticles to soil microbial community. Environmental Science and Pollution Research25, 28140–28152.

[16] Gladkov, G.V., Kimeklis, A.K., Afonin, A.M., Lisina, T.O., Orlova, O.V., Aksenova, T.S., Kichko, A.A., Pinaev, A.G., Andronov, E.E., 2022. The structure of stable cellulolytic consortia isolated from natural lignocellulosic substrates. International Journal of Molecular Sciences23, 10779.

[17] Glissmann, K., Conrad, R., 2000. Fermentation pattern of methanogenic degradation of rice straw in anoxic paddy soil. FEMS Microbiology Ecology31, 117–126.

[18] Hahnke, S., Langer, T., Koeck, D.E., Klocke, M., 2016. Description of Proteiniphilum saccharofermentans sp. nov., Petrimonas mucosa sp. nov. and Fermentimonas caenicola gen. nov., sp. nov., isolated from mesophilic laboratory-scale biogas reactors, and emended description of the genus Proteiniphilum. International Journal of Systematic and Evolutionary Microbiology 66, 1466–1475.

[19] Harwood, C.S., 2020. Iron-only and vanadium nitrogenases: fail-safe enzymes or something more? Annual Review of Microbiology 74, 247–266.

[20] He, C., Song, H., Hou, T.T., Jiao, Y.Z., Li, G., Litti, Y.V., Zhang, Q.G., Liu, L., 2023. Simultaneous addition of CO₂-nanobubble water and iron nanoparticles to enhance methane production from anaerobic digestion of corn straw. Bioresource Technology377, 128947.

[21] Hu, T., Wang, X.J., Zhen, L.S., Gu, J., Song, Z.L., Sun, W., Xie, J., 2021. Succession of diazotroph community and functional gene response to inoculating swine manure compost with a lignocellulose-degrading consortium. Bioresource Technology337, 125469.

[22] Huang, Z.Z., Zeng, Z.T., Song, Z.X., Chen, A.W., Zeng, G.M., Xiao, R., He, K., Yuan, L., Li, H., Chen, G.Q., 2020. Antimicrobial efficacy and mechanisms of silver nanoparticles against Phanerochaete chrysosporium in the presence of common electrolytes and humic acid. Journal of Hazardous Materials383, 121153.

[23] Jiang, H., Yang, B.S., Wang, H., Chen, Q.L., Cao, X.L., Gao, Y.C., Zhao, C.H., Yin, K.X., 2021. Insights on the effects of ZnO nanoparticle exposure on soil heterotrophic respiration as revealed by soil microbial communities and activities. Journal of Soils and Sediments21, 2315–2326.

[24] Jones, D.L., Willett, V.B., 2006. Experimental evaluation of methods to quantify dissolved organic nitrogen (DON) and dissolved organic carbon (DOC) in soil. Soil Biology and Biochemistry38, 991–999.

[25] Keller, A.A., Lazareva, A., 2014. Predicted releases of engineered nanomaterials: from global to regional to local. Environmental Science & Technology Letters1, 65–70.

[26] Khan, M.R., Akram, M., 2020. Nanoparticles and their fate in soil ecosystem. In: Ghorbanpour, M., Bhargava, P., Varma, A., Choudhary, D.K., eds. Biogenic Nano-Particles and Their Use in Agro-Ecosystems. Singapore: Springer, 221–245.

[27] Khatoon, H., Solanki, P., Narayan, M., Tewari, L., Rai, J.P.N., 2017. Role of microbes in organic carbon decomposition and maintenance of soil ecosystem. International Journal of Chemical Studies5, 1648–1656.

[28] Leschine, S.B., 1995. Cellulose degradation in anaerobic environments. Annual Review of Microbiology49, 399–426.

[29] Lin, J.J., Ma, K.Y., Chen, H.H., Chen, Z.L., Xing, B.S., 2022. Influence of different types of nanomaterials on soil enzyme activity: a global meta-analysis. Nano Today42, 101345.

[30] Lin, J.J., Ma, K.Y., Chen, H.H., Chen, Z.L., Xing, B.S., 2022. Influence of different types of nanomaterials on soil enzyme activity: a global meta-analysis. Nano Today42, 101345.

[31] Lin, L.M., Ju, F., 2023. Evaluation of different 16S rRNA gene hypervariable regions and reference databases for profiling engineered microbiota structure and functional guilds in a swine wastewater treatment plant. Interface Focus13, 20230012.

[32] Liu, D., Iqbal, S., Gui, H., Xu, J.C., An, S.S., Xing, B.S., 2023. Nano-iron oxide (Fe₃O₄) mitigates the effects of microplastics on a ryegrass soil–microbe–plant system. ACS Nano17, 24867–24882.

[33] Llamas, M., Greses, S., Tomás-Pejó, E., González-Fernández, C., 2022. Carboxylic acids production via anaerobic fermentation: microbial communities’ responses to stepwise and direct hydraulic retention time decrease. Bioresource Technology344, 126282.

[34] Pan, B., Li, S.L., Peng, H.B., Ao, C.H., Wei, Z., Xing, B.S., 2023. Advances in understanding the processes and cycling of nanoparticles in the terrestrial environment. Advances in Agronomy182, 1–79.

[35] Park, J.H., Kang, H.J., Park, K.H., Park, H.D., 2018. Direct interspecies electron transfer via conductive materials: a perspective for anaerobic digestion applications. Bioresource Technology254, 300–311.

[36] Qi, L.Q., Liu, X., Miao, Y.J., Chatzisymeon, E., Yang, P., Lu, H.Y., Pang, L.N., 2021. Response of cattle manure anaerobic digestion to zinc oxide nanoparticles: methane production, microbial community, and functions. Journal of Environmental Chemical Engineering9, 106704.

[37] Qiu, C.P., Feng, Y.Z., Wu, M., Zhang, J.W., Chen, X.F., Li, Z.P., 2019. NanoFe₃O₄ accelerates methanogenic straw degradation in paddy soil enrichments. Applied Soil Ecology144, 155–164.

[38] Rajput, V.D., Minkina, T., Sushkova, S., Tsitsuashvili, V., Mandzhieva, S., Gorovtsov, A., Nevidomskyaya, D., Gromakova, N., 2018. Effect of nanoparticles on crops and soil microbial communities. Journal of Soils and Sediments18, 2179–2187.

[39] Sampaio, D.S., Almeida, J.R.B., de Jesus, H.E., Rosado, A.S., Seldin, L., Jurelevicius, D., 2017. Distribution of anaerobic hydrocarbon-degrading bacteria in soils from king George Island, maritime Antarctica. Microbial Ecology74, 810–820.

[40] Schellenberger, S., Kolb, S., Drake, H.L., 2010. Metabolic responses of novel cellulolytic and saccharolytic agricultural soil Bacteria to oxygen. Environmental Microbiology12, 845–861.

[41] Schnell, S., Ratering, S., Jansen, K.H., 1998. Simultaneous determination of iron(III), iron(II), and manganese(II) in environmental samples by ion chromatography. Environmental Science & Technology32, 1530–1537.

[42] Shrestha, B., Acosta-Martinez, V., Cox, S.B., Green, M.J., Li, S.B., Cañas-Carrell, J.E., 2013. An evaluation of the impact of multiwalled carbon nanotubes on soil microbial community structure and functioning. Journal of Hazardous Materials261, 188–197.

[43] Simonin, M., Richaume, A., 2015. Impact of engineered nanoparticles on the activity, abundance, and diversity of soil microbial communities: a review. Environmental Science and Pollution Research22, 13710–13723.

[44] Tripathi, G.D., Javed, Z., Gattupalli, M., Dashora, K., 2023. Impact of nanomaterials accumulation on the organic carbon associated enzymatic activities in soil. Soil and Sediment Contamination: An International Journal32, 538–556.

[45] Vyas, T.K., Vala, A.K., 2020. The impact of magnetic nanoparticles on microbial community structure and function in rhizospheric soils. In: Thomas, S., Nochehdehi, A.R., eds. Handbook of Magnetic Hybrid Nanoalloys and Their Nanocomposites. Cham: Springer, 1–25.

[46] Wu, H.X., Jiang, X.H., Tong, J.H., Wang, J., Shi, J.Y., 2023. Effects of Fe₃O₄ nanoparticles and nano hydroxyapatite on Pb and Cd stressed rice (Oryza sativa L.) seedling. Chemosphere329, 138686.

[47] Xin, X.P., Zhao, F.L., Zhao, H.M., Goodrich, S.L., Hill, M.R., Sumerlin, B.S., Stoffella, P.J., Wright, A.L., He, Z.L., 2020. Comparative assessment of polymeric and other nanoparticles impacts on soil microbial and biochemical properties. Geoderma367, 114278.

[48] Yamini, V., Shanmugam, V., Rameshpathy, M., Venkatraman, G., Ramanathan, G., Al Garalleh, H., Hashmi, A., Brindhadevi, K., Rajeswari, V.D., 2023. Environmental effects and interaction of nanoparticles on beneficial soil and aquatic microorganisms. Environmental Research236, 116776.

[49] Yang, Z.F., Xu, Z.N., Geng, L.S., Shu, W.J., Zhu, T., 2020. Effect of multi-walled carbon nanotubes on extractability of Sb and Cd in contaminated soil. Ecotoxicology and Environmental Safety205, 111316.

[50] Yang, Z.M., Guo, R.B., Shi, X.S., Wang, C.S., Wang, L., Dai, M., 2016. Magnetite nanoparticles enable a rapid conversion of volatile fatty acids to methane. RSC Advances6, 25662–25668.

[51] Yang, Z.M., Shi, X.S., Wang, C.S., Wang, L., Guo, R.B., 2015. Magnetite nanoparticles facilitate methane production from ethanol via acting as electron acceptors. Scientific Reports5, 16118.

[52] You, T.T., Liu, D.D., Chen, J., Yang, Z.Z., Dou, R.Z., Gao, X., Wang, L., 2018. Effects of metal oxide nanoparticles on soil enzyme activities and bacterial communities in two different soil types. Journal of Soils and Sediments18, 211–221.

[53] Yuan, Q., Hernández, M., Dumont, M.G., Rui, J.P., Scavino, A.F., Conrad, R., 2018. Soil bacterial community mediates the effect of plant material on methanogenic decomposition of soil organic matter. Soil Biology and Biochemistry116, 99–109.

[54] Zhan, H., Bian, Y.N., Yuan, Q., Ren, B.Z., Hursthouse, A., Zhu, G.C., 2018. Preparation and potential applications of super paramagnetic nano-Fe₃O₄. Processes6, 33.

[55] Zhang, J.C., Xia, X.X., Li, S.L., Ran, W., 2018. Response of methane production via propionate oxidation to carboxylated multiwalled carbon nanotubes in paddy soil enrichments. PeerJ6, e4267.

[56] Zhang, J.Y., Zhou, H., Gu, J.F., Huang, F., Yang, W.J., Wang, S.L., Yuan, T.Y., Liao, B.H., 2020. Effects of nano-Fe₃O₄-modified biochar on iron plaque formation and Cd accumulation in rice (Oryza sativa L.). Environmental Pollution260, 113970.

[57] Zhang, Y.R., Xu, R., Xiang, Y.P., Lu, Y., Jia, M.Y., Huang, J., Xu, Z.Y., Cao, J., Xiong, W.P., Yang, Z.H., 2021. Addition of nanoparticles increases the abundance of mobile genetic elements and changes microbial community in the sludge anaerobic digestion system. Journal of Hazardous Materials405, 124206.

[58] Zhang, Z.Z., Wang, Z.J., Zhang, T., Yin, B.S., Li, R.J., Sheng, Z.P., Li, S., 2024. Variations in soil microbial communities in different saline soils under typical Populus spp. vegetation in alpine region of the Qaidam Basin, NW China. Ecotoxicology and Environmental Safety282, 116747.

[59] Zhou, D.M., Jin, S.Y., Wang, Y.J., Wang, P., Weng, N.Y., Wang, Y., 2012. Assessing the impact of iron-based nanoparticles on pH, dissolved organic carbon, and nutrient availability in soils. Soil and Sediment Contamination: An International Journal21, 101–114.

[60] Zuo, Y.T., Zeng, W.Z., Huang, J.S., 2024. Effects of exposure to carbon nanomaterials on soil microbial communities: a global meta-analysis. Land Degradation & Development35, 238–248.

Competing interests

The authors declare no conflicts of interest in the authorship and publication of this document.

Funding

This study was financially supported by the National Natural Science Foundation of China (Grant No. 42177116); by complementary fund from the Guizhou Provincial Department of Science and Technology; by Guizhou Provincial 2021 Science and Technology Subsidies (Grant No. GZ2021SIG); by the Chinese Academy of Sciences “Light of West China” Program.

Electronic supplementary material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s42832-025-0331-1 and is accessible for authorized users.

RIGHTS & PERMISSIONS

2025 Higher Education Press