Copper; Soil health index; Soil multifunctionality; Sustainable agriculture; Zinc; Ecology; Agricultural and Biological Sciences (miscellaneous); Soil Science
Abstract :
[en] Soil fertility and nutrient cycling can be enhanced with application of biosolids; however, it can also pose risks associated with introduction of heavy metals. The balance between these beneficial and adverse effects in influencing soil health and multifunctionality remains unclear. Further, eco-friendly strategies to alleviate heavy metal accumulation in biosolids-applied soils are undetermined. With this objective, we sampled soil from an agricultural field that had been applied with biosolids for 16 years at rates of 0 t ha−1 (Control), 4.5 t ha−1 (SW1), 9 t ha−1 (SW2), 18 t ha−1 (SW3), and 36 t ha−1 (SW4). Bacterial, fungal and arbuscular mycorrhizal (AM) fungal communities were determined, and soil health index (SHI) and multifunctionality (SMF) quantified. Field experiment showed that optimal biosolids application significantly increased SHI and SMF by 3–20 % and 3–75 %, respectively, compared to the Control treatment. Bacterial and AM fungal keystone taxa abundances were positively correlated to SHI and SMF. Additionally, to corroborate these results, pot experiments were conducted to test the effect of AM fungal inoculation on soil microbial diversity and multifunctionality, and its mitigatory effect on heavy metal accumulation. AM fungal inoculation significantly increased SMF by 42–61 %, and reduced Cu and Zn contents by 7–10 % and 4–6 %, respectively. Metagenomic analyses showed that AM fungal inoculation significantly increased soil carbon, nitrogen, phosphorus and sulfur gene abundance, positively correlated to SMF. Overall, the findings underscore the benefits of judicious biosolids application combined with AM fungal bioaugmentation as a viable strategy for mitigation of heavy metal accumulation for sustainable agriculture.
Disciplines :
Agriculture & agronomy
Author, co-author :
Sun, Tao; State Key Laboratory of Efficient Utilization of Arable Land in China, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing, China ; Gembloux Agro Bio Tech, University of Liège, Belgium
Delaplace, Pierre ; Université de Liège - ULiège > Département GxABT > Plant Sciences
Li, Guihua; State Key Laboratory of Efficient Utilization of Arable Land in China, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing, China
James, Anina; State Key Laboratory of Efficient Utilization of Arable Land in China, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing, China
Pan, Junting; State Key Laboratory of Efficient Utilization of Arable Land in China, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing, China
Zhang, Jianfeng; State Key Laboratory of Efficient Utilization of Arable Land in China, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing, China ; Institute of Special Animal and Plant Sciences, Chinese Academy of Agricultural Sciences, Changchun, China
Language :
English
Title :
Arbuscular mycorrhizal fungi bioaugmentation improves soil health in long-term biosolids-amended farmland
CSC - China Scholarship Council NSCF - National Natural Science Foundation of China
Funding text :
This study was supported by the National Natural Science Foundation of China ( 22176215 ), the Shandong Provincial Key Research and Development Program ( 2023TZXD087 ), and the China Scholarship Council (No. 202393250064 ).
Abdu, N., Abdullahi, A.A., Abdulkadir, A., 2017. Heavy metals and soil microbes. Environmental Chemistry Letters. 15(1), 65-84.
Adewara, O.A., Adebayo-Olajide, T.C., Ayedun, J.S., Kotun, B.C., Adeleke, A.J., Brown, A.D., Ogunbanwo, S.T., 2024. Soil formation, soil health and soil biodiversity. In Prospects for soil regeneration and its impact on environmental protection (pp. 95-121). Cham: Springer Nature Switzerland.
Ahmad, A.M., Ugya, A.Y., Isah, H.A., Imam, T.S., 2019. Mineralization and mobilization of biosolids phosphorus in soil: A concise review. J. Appl. Biol. Biotech. 7(05), 98-106.
Alengebawy, A., Abdelkhalek, S.T., Qureshi, S.R., Wang, M.Q., 2021. Heavy metals and pesticides toxicity in agricultural soil and plants: Ecological risks and human health implications. Toxics. 9(3), 42.
Andrés-Abellán, M., Wic-Baena, C., López-Serrano, F.R., et al., 2019. A soil-quality index for soil from Mediterranean forests. European Journal of Soil Science. 70(5), 1001-1011.
Begum, N., Qin, C., Ahanger, M. A., Raza, S., Khan, M. I., Ashraf, M., Zhang, L., 2019. Role of arbuscular mycorrhizal fungi in plant growth regulation: implications in abiotic stress tolerance. Frontiers in Plant Science. 10, 1068.
Bell, C.W., Fricks, B.E., Rocca, J.D., Steinweg, J.M., McMahon, S.K., Wallenstein, M. D., 2013. High-throughput Fluorometric Measurement of Potential Soil Extracellular Enzyme Activities. Jove-Journal of Visualized Experiments. 81.
Bhantana, P., Rana, M.S., Sun, X.C., Moussa, M.G., Saleem, M.H., Syaifudin, M., Hu, C.X., 2021. Arbuscular mycorrhizal fungi and its major role in plant growth, zinc nutrition, phosphorous regulation and phytoremediation. Symbiosis. 84, 19-37.
Bharti, R., Sharma, R., 2022. Effect of heavy metals: An overview. Materials Today: Proceedings. 51, 880-885.
Caracciolo, A.B., Topp, E., Grenni, P., 2015. Pharmaceuticals in the environment: biodegradation and effects on natural microbial communities. A review. Journal of Pharmaceutical and Biomedical Analysis. 106, 25-36.
Cardoso, E.J.B.N., Vasconcellos, R.L.F., Bini, D., Miyauchi, M.Y.H., Santos, C.A.D., Alves, P.R.L., Nogueira, M.A., 2013. Soil health: looking for suitable indicators. What should be considered to assess the effects of use and management on soil health? Scientia Agricola. 70, 274-289.
Clarke, B.O., Smith, S.R., 2011. Review of ‘emerging’ organic contaminants in biosolids and assessment of international research priorities for the agricultural use of biosolids. Environment International. 37(1), 226-247.
Cycoń, M., Mrozik, A., Piotrowska-Seget, Z., 2019. Antibiotics in the soil environment—degradation and their impact on microbial activity and diversity. Frontiers in Microbiology. 10, 338.
Das, S., Dash, H.R., Chakraborty, J., 2016. Genetic basis and importance of metal resistant genes in bacteria for bioremediation of contaminated environments with toxic metal pollutants. Applied Microbiology and Biotechnology. 100, 2967-2984.
Delgado-Baquerizo, M., Maestre, F.T., Reich, P.B., Jeffries, T.C., Gaitan, J.J., Encinar, D., Singh, B.K., 2016. Microbial diversity drives multifunctionality in terrestrial ecosystems. Nature Communications. 7(1), 10541.
Devi, R., Kaur, T., Kour, D., Rana, K.L., Yadav, A., Yadav, A.N., 2020. Beneficial fungal communities from different habitats and their roles in plant growth promotion and soil health. Microbial Biosystems. 5(1), 21-47.
Dhalaria, R., Kumar, D., Kumar, H., Nepovimova, E., Kuča, K., Torequl Islam, M., Verma, R., 2020. Arbuscular mycorrhizal fungi as potential agents in ameliorating heavy metal stress in plants. Agronomy. 10(6), 815.
Dong, Z., Li, H., Xiao, J., Sun, J., Liu, R., Zhang, A., 2022. Soil multifunctionality of paddy field is explained by soil pH rather than microbial diversity after 8-years of repeated applications of biochar and nitrogen fertilizer. Science of the Total Environment. 853, 158620.
Elgarahy, A.M., Eloffy, M.G., Priya, A.K., Yogeshwaran, V., Yang, Z., Elwakeel, K.Z., Lopez-Maldonado, E.A., 2024. Biosolids management and utilizations: A review. Journal of Cleaner Production. 141974.
Eshaghi, A., Bommersbach, C., Zittermann, S., Burnham, C.A.D., Patel, R., Schuetz, A.N., Kus, J.V., 2021. Phenotypic and genomic profiling of Staphylococcus argenteus in Canada and the United States and recommendations for clinical result reporting. Journal of Clinical Microbiology. 59(6), 10-1128.
Etesami, H., 2018. Bacterial mediated alleviation of heavy metal stress and decreased accumulation of metals in plant tissues: mechanisms and future prospects. Ecotoxicology and Environmental Safety. 147, 175-191.
Fall, A.F., Nakabonge, G., Ssekandi, J., Founoune-Mboup, H., Apori, S.O., Ndiaye, A., Ngom, K., 2022. Roles of arbuscular mycorrhizal fungi on soil fertility: contribution in the improvement of physical, chemical, and biological properties of the soil. Frontiers in Fungal Biology. 3, 723892.
Gianico, A., Braguglia, C.M., Gallipoli, A., Montecchio, D., Mininni, G., 2021. Land application of biosolids in Europe: possibilities, constraints and future perspectives. Water. 13(1), 103.
Green, G.B., Williams, M.B., Chehade, S.B., Morrow, C.D., Watts, S.A., Bej, A.K., 2022. High-throughput amplicon sequencing datasets of the metacommunity DNA of the gut microbiota of Zebrafish Danio rerio fed diets with differential quantities of protein and fat contents. Data in Brief. 42, 108313.
Gupta, P., Diwan, B., 2017. Bacterial exopolysaccharide mediated heavy metal removal: a review on biosynthesis, mechanism and remediation strategies. Biotechnology Reports. 13, 58-71.
Hale, R.C., King, A.E., Ramirez, J. M., La Guardia, M., Nidel, C., 2022. Durable plastic goods: a source of microplastics and chemical additives in the built and natural environments. Environmental Science & Technology Letters. 9(10), 798-807.
Han, S., Delgado-Baquerizo, M., Luo, X., Liu, Y., Van Nostrand, J.D., Chen, W., Huang, Q., 2021. Soil aggregate size-dependent relationships between microbial functional diversity and multifunctionality. Soil Biology and Biochemistry. 154, 108143.
Hartmann, M., Six, J., 2023. Soil structure and microbiome functions in agroecosystems. Nature Reviews Earth & Environment. 4(1), 4-18.
Hooker, J.E., Black, K.E., 1995. Arbuscular mycorrhizal fungi as components of sustainable soil-plant systems. Critical Reviews in Biotechnology. 15(3-4), 201-212.
Huang, W., Zong, M., Fan, Z., Feng, Y., Li, S., Duan, C., Li, H., 2021. Determining the impacts of deforestation and corn cultivation on soil quality in tropical acidic red soils using a soil quality index. Ecol. Indicat. 125, 107580
Hung, W.C., Miao, Y., Truong, N., Jones, A., Mahendra, S., Jay, J., 2022. Tracking antibiotic resistance through the environment near a biosolid spreading ground: resistome changes, distribution, and metal (loid) co-selection. Science of the Total Environment. 823, 153570.
Jia, J., Hu, G., Ni, G., Xie, M., Li, R., Wang, G., Zhang, J., 2024. Bacteria drive soil multifunctionality while fungi are effective only at low pathogen abundance. Science of the Total Environment. 906, 167596.
Jia, J., de Goede, R., Li, Y., Zhang, J., Wang, G., Zhang, J., Creamer, R., 2025. Unlocking soil health: Are microbial functional genes effective indicators? Soil Biology and Biochemistry. 109768.
Jia, J., Zhang, J., Li, Y., Koziol, L., Podzikowski, L., Delgado-Baquerizo, M., Wang, G., Zhang, J., 2023. Relationships between soil biodiversity and multifunctionality in croplands depend on salinity and organic matter. Geoderma. 429, 116273.
Jian, Z., Zeng, L., Xu, T., Sun, S., Yan, S., Yang, L., Dou, T., 2021. Antibiotic resistance genes in bacteria: Occurrence, spread, and control. Journal of Basic Microbiology. 61(12), 1049-1070.
Jiao, S., Lu, Y., Wei, G., 2022. Soil multitrophic network complexity enhances the link between biodiversity and multifunctionality in agricultural systems. Global Change Biology. 28(1), 140-153.
Keesstra, S., Nunes, J., Novara, A., Finger, D., Avelar, D., Kalantari, Z., Cerdà, A., 2018. The superior effect of nature based solutions in land management for enhancing ecosystem services. Science of the Total Environment. 610, 997-1009.
Kumar, S., Prasad, S., Yadav, K.K., Shrivastava, M., Gupta, N., Nagar, S., Malav, L.C., 2019. Hazardous heavy metals contamination of vegetables and food chain: Role of sustainable remediation approaches-A review. Environmental Research. 179, 108792.
Kumar, V., Chopra, A.K., Kumar, A., 2017. A review on sewage sludge (Biosolids) a resource for sustainable agriculture. Archives of Agriculture and Environmental Science. 2(4), 340-347.
Law, A., Solano, O., Brown, C.J., Hunter, S.S., Fagnan, M., Top, E.M., Stalder, T., 2021. Biosolids as a source of antibiotic resistance plasmids for commensal and pathogenic bacteria. Frontiers in Microbiology. 12, 606409.
Li, K., Wang, C., Zhang, H., Zhang, J., Jiang, R., Feng, G., Yu, B., 2022. Evaluating the effects of agricultural inputs on the soil quality of smallholdings using improved indices. Catena. 209, 105838.
Liang, L., Liu, W., Sun, Y., Huo, X., Li, S., Zhou, Q., 2017. Phytoremediation of heavy metal contaminated saline soils using halophytes: current progress and future perspectives. Environmental Reviews. 25(3), 269-281.
Liu, C., Cui, Y., Li, X., Yao, M., 2021. microeco: an R package for data mining in microbial community ecology. FEMS Microbiology Ecology, 97(2), fiaa255.
Lu, Q., He, Z.L., Stoffella, P.J., 2012. Land application of biosolids in the USA: a review. Applied and Environmental Soil Science. 2012(1), 201462.
Luo, G., Rensing, C., Chen, H., Liu, M., Wang, M., Guo, S., Shen, Q., 2018. Deciphering the associations between soil microbial diversity and ecosystem multifunctionality driven by long-term fertilization management. Functional Ecology. 32(4), 1103-1116.
Maestre F.T., Castillo-Monroy A.P., Bowker M.A., Ochoa-Hueso R., 2012. Species richness effects on ecosystem multifunctionality depend on evenness, composition and spatial pattern. Journal of Ecology. 100, 317-330.
Mahajan, G., Das, B., Morajkar, S., Desai, A., Murgaokar, D., Kulkarni, R., Sale, R., Patel, K., 2020. Soil quality assessment of coastal salt-affected acid soils of India. Environ. Sci. Pollut. Res. 27, 26221–26238
Marchuk, S., Tait, S., Sinha, P., Harris, P., Antille, D.L., McCabe, B.K., 2023. Biosolids-derived fertilisers: A review of challenges and opportunities. Science of the Total Environment. 875, 162555.
Mohajerani, A., Karabatak, B., 2020. Microplastics and pollutants in biosolids have contaminated agricultural soils: An analytical study and a proposal to cease the use of biosolids in farmlands and utilise them in sustainable bricks. Waste Management. 107, 252-265.
Mohapatra, D.P., Cledón, M., Brar, S.K., Surampalli, R.Y., 2016. Application of wastewater and biosolids in soil: occurrence and fate of emerging contaminants. Water, Air, & Soil Pollution. 227, 1-14.
Morgan, B.S., Tian, G., Oladeji, O.O., Cox, A.E., Granato, T.C., Zhang, H., Podczerwinski, E.W., 2024. Analysis of effects and factors linked to soil microbial populations and nitrogen cycling under long-term biosolids application. Science of The Total Environment. 934, 173216.
Olaniran, A.O., Balgobind, A., Pillay, B., 2013. Bioavailability of heavy metals in soil: impact on microbial biodegradation of organic compounds and possible improvement strategies. International Journal of Molecular Sciences. 14(5), 10197-10228.
Olesen, J. M., Bascompte, J., Dupont, Y. L., Jordano, P., 2007. The modularity of pollination networks. Proceedings of the national academy of sciences, 104(50), 19891-19896.
Oliveira, A., Pampulha, M.E., 2006. Effects of long-term heavy metal contamination on soil microbial characteristics. Journal of Bioscience and Bioengineering. 102(3), 157-161.
Op De Beeck, M., Lievens, B., Busschaert, P., Declerck, S., Vangronsveld, J., Colpaert, J.V., 2014. Comparison and validation of some ITS primer pairs useful for fungal metabarcoding studies. PloS One. 9(6), e97629.
Öpik, M., Vanatoa, A., Vanatoa, E., Moora, M., Davison, J., Kalwij, J.M., Zobel, M., 2010. The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytologist. 188(1), 223-241.
Pandao, M.R., Thakare, A.A., Choudhari, R.J., Navghare, N.R., Sirsat, D.D., Rathod, S.R., 2024. Soil health and nutrient management. International Journal of Plant and Soil Science. 36(5), 873-883.
Pathma, J., Sakthivel, N., 2012. Microbial diversity of vermicompost bacteria that exhibit useful agricultural traits and waste management potential. SpringerPlus, 1, 1-19.
Pérez-de-Mora, A., Burgos, P., Madejón, E., Cabrera, F., Jaeckel, P., Schloter, M., 2006. Microbial community structure and function in a soil contaminated by heavy metals: effects of plant growth and different amendments. Soil Biology and Biochemistry. 38(2), 327-341.
Ploughe, L.W., Akin-Fajiye, M., Gagnon, A., Gardner, W.C., Fraser, L.H., 2021. Revegetation of degraded ecosystems into grasslands using biosolids as an organic amendment: A meta-analysis. Applied Vegetation Science. 24(1), e12558.
Popoola, L.T., Olawale, T.O., Salami, L., 2023. A review on the fate and effects of contaminants in biosolids applied on land: Hazards and government regulatory policies. Heliyon. 9(10).
Pritchard, D.L., Penney, N., McLaughlin, M.J., Rigby, H., Schwarz, K., 2010. Land application of sewage sludge (biosolids) in Australia: risks to the environment and food crops. Water Science and Technology. 62(1), 48-57.
Riaz, M., Kamran, M., Fang, Y., Wang, Q., Cao, H., Yang, G., Wang, X., 2021. Arbuscular mycorrhizal fungi-induced mitigation of heavy metal phytotoxicity in metal contaminated soils: A critical review. Journal of Hazardous Materials. 402, 123919.
Rigby, H., Clarke, B.O., Pritchard, D. L., Meehan, B., Beshah, F., Smith, S.R., Porter, N.A., 2016. A critical review of nitrogen mineralization in biosolids-amended soil, the associated fertilizer value for crop production and potential for emissions to the environment. Science of the Total Environment. 541, 1310-1338.
Rizwan, M., Ali, S., ur Rehman, M.Z., Rinklebe, J., Tsang, D.C., Bashir, A., Ok, Y.S., 2018. Cadmium phytoremediation potential of Brassica crop species: a review. Science of the Total Environment. 631, 1175-1191.
Safronova, V.I., Piluzza, G., Bullitta, S., Belimov, A.A., 2011. Use of legume-microbe symbioses for phytoremediation of heavy metal polluted soils: advantages and potential problems. Handbook for Phytoremediation. 443.
Santaella, C., Plancot, B., 2020. Interactions of nanoenabled agrochemicals with soil microbiome. Nanopesticides: From Research and Development to Mechanisms of Action and Sustainable Use in Agriculture. 137-163.
Shao, G., Ai, J., Sun, Q., Hou, L., Dong, Y., 2020. Soil quality assessment under different forest types in the Mount Tai, central Eastern China. Ecol. Indicat. 115, 106439.
Shuaib, M., Azam, N., Bahadur, S., Romman, M., Yu, Q., Xuexiu, C., 2021. Variation and succession of microbial communities under the conditions of persistent heavy metal and their survival mechanism. Microbial Pathogenesis. 150, 104713.
Sun, T., Delaplace, P., Li, G., James, A., Pan, J., Zhang, J., 2025. Novel insights into the effect of arbuscular mycorrhizal fungi inoculation in soils under long-term biosolids application: emphasis on antibiotic and metal resistance genes, and mobile genetic elements. Environmental Pollution. 125846.
Sun, T., Li, G., Mazarji, M., Delaplace, P., Yang, X., Zhang, J., Pan, J., 2024. Heavy metals drive microbial community assembly process in farmland with long-term biosolids application. Journal of Hazardous Materials. 468, 133845.
Sun, W., Shahrajabian, M.H., 2023. The application of arbuscular mycorrhizal fungi as microbial biostimulant, sustainable approaches in modern agriculture. Plants. 12(17), 3101.
Teague, R., Kreuter, U., 2020. Managing grazing to restore soil health, ecosystem function, and ecosystem services. Frontiers in Sustainable Food Systems. 4, 534187.
Van Geel, M., Busschaert, P., Honnay, O., Lievens, B., 2014. Evaluation of six primer pairs targeting the nuclear rRNA operon for characterization of arbuscular mycorrhizal fungal (AMF) communities using 454 pyrosequencing. Journal of Microbiological Methods. 106, 93-100.
Wahab, A., Muhammad, M., Munir, A., Abdi, G., Zaman, W., Ayaz, A., Reddy, S.P.P., 2023. Role of arbuscular mycorrhizal fungi in regulating growth, enhancing productivity, and potentially influencing ecosystems under abiotic and biotic stresses. Plants. 12(17), 3102.
Walters, W., Hyde, E.R., Berg-Lyons, D., et al., 2016. Improved bacterial 16S rRNA gene (V4 and V4-5) and fungal internal transcribed spacer marker gene primers for microbial community surveys. Msystems. 1(1), e00009-15.
Wang, F., Zhang, L., Zhou, J., Rengel, Z., George, T.S., Feng, G., 2022a. Exploring the secrets of hyphosphere of arbuscular mycorrhizal fungi: processes and ecological functions. Plant and Soil. 481(1), 1-22.
Wang, H.R., Zhao, X.Y., Zhang, J.M., Lu, C., Feng, F.J., 2022b. Arbuscular mycorrhizal fungus regulates cadmium accumulation, migration, transport, and tolerance in Medicago sativa. Journal of Hazardous Materials. 435, 129077.
Wijesekara, H., Bolan, N.S., Thangavel, R., Seshadri, B., Surapaneni, A., Saint, C., Vithanage, M., 2017. The impact of biosolids application on organic carbon and carbon dioxide fluxes in soil. Chemosphere. 189, 565-573.
Wijesekara, H., Colyvas, K., Rippon, P., Hoang, S.A., Bolan, N.S., Manna, M.C., Kirkham, M.B., 2021. Carbon sequestration value of biosolids applied to soil: A global meta-analysis. Journal of Environmental Management. 284, 112008.
Wipf, D., Krajinski, F., van Tuinen, D., Recorbet, G., Courty, P.E., 2019. Trading on the arbuscular mycorrhiza market: from arbuscules to common mycorrhizal networks. New Phytologist. 223(3), 1127-1142.
Wright, S F., Upadhyaya, A., 1996. Extraction of an abundant and unusual protein from soil and comparison with hyphal protein of arbuscular mycorrhizal fungi. Soil Science. 161(9), 575-586.
Wright, S.F., Upadhyaya, A., Buyer, J.S., 1998. Comparison of N-linked oligosaccharides of glomalin from arbuscular mycorrhizal fungi and soils by capillary electrophoresis. Soil Biology and Biochemistry. 30(13), 1853-1857.
Wu, Y., Li, X., Yu, L., Wang, T., Wang, J., Liu, T., 2022. Review of soil heavy metal pollution in China: Spatial distribution, primary sources, and remediation alternatives. Resources, Conservation and Recycling. 181, 106261.
Wu, Y., Zeng, J., Zhu, Q., Zhang, Z., Lin, X., 2017. pH is the primary determinant of the bacterial community structure in agricultural soils impacted by polycyclic aromatic hydrocarbon pollution. Scientific Reports. 7(1), 40093.
Yu, P., Han, D., Liu, S., Wen, X., Huang, Y., Jia, H., 2018. Soil quality assessment under different land uses in an alpine grassland. Catena. 171, 280–287.
Zeng, W., Li, F., Wu, C., Yu, R., Wu, X., Shen, L., Li, J., 2020. Role of extracellular polymeric substance (EPS) in toxicity response of soil bacteria Bacillus sp. S3 to multiple heavy metals. Bioprocess and Biosystems Engineering. 43, 153-167.
Zhang, G., Bai, J., Xi, M., Zhao, Q., Lu, Q., Jia, J., 2016. Soil quality assessment of coastal wetlands in the Yellow River Delta of China based on the minimum data set. Ecol. Indicat. 66, 458–466.
Zhang, J., Li, Y., Jia, J., Liao, W., Amsili, J.P., Schneider, R.L., van Es, H.M., Li, Y., Zhang, J., 2023. Applicability of soil health assessment for wheat-maize cropping systems in smallholders'’ farmlands. Agriculture, Ecosystems & Environment. 353, 108558.
Zhang, R., Xu, Q., Song, Z., Wu, J., Chen, H., Bai, X., Huang, D., 2024. Manipulating soil microbial community assembly by the cooperation of exogenous bacteria and biochar for establishing an efficient and healthy CH4 biofiltration system. Chemosphere. 352, 141319.
Zheng, H., Feng, N., Yang, T., Shi, M., Wang, X., Zhang, Q., Xing, B., 2021. Individual and combined applications of biochar and pyroligneous acid mitigate dissemination of antibiotic resistance genes in agricultural soil. Science of the Total Environment, 796, 148962.
Zhu, L., Zhao, Y., Zhang, W., Zhou, H., Chen, X., Li, Y., Wei, Z., 2019. Roles of bacterial community in the transformation of organic nitrogen toward enhanced bioavailability during composting with different wastes. Bioresource Technology. 285, 121326.
Zou, Y. N., Wu, Q. S., Kuča, K., 2021. Unravelling the role of arbuscular mycorrhizal fungi in mitigating the oxidative burst of plants under drought stress. Plant Biology. 23, 50-57.
