Biosolids; Community assembly process; Heavy metals; Soil microbial community; Soil Pollutants/analysis; Arbuscular mycorrhizal
Abstract :
[en] Biosolids are considered an alternative to chemical fertilizers due to their rich nutrients. However, long-term biosolids application can lead to heavy metals accumulation, which severely affects soil microbial community compositions. The factors influencing soil microbial community assembly were explored under a 16-year long-term experiment with biosolids applications. Our results indicated that biosolids application significantly increased fungal richness while not for bacterial and arbuscular mycorrhizal (AM) fungal richness. Besides, biosolids application significantly affected soil bacterial, fungal compositions and AM fungal community. Soil microorganisms were clustered into different modules with bacterial and AM fungal communities were affected by both organic matter and heavy metals, while fungal communities were affected by heavy metals (Cr, Ni, and As). The soil bacterial community assembly was dominated by stochastic processes while the fungal and AM fungal community assemblies were mainly driven by deterministic processes. Random forest analysis showed that heavy metals were identified as major drivers (Hg, Cu, Cd, and Zn for bacteria, Pb and Cr for fungi, and As and Ni for AM fungi) of the community assembly process. Overall, our study highlights the significant role of heavy metals in shaping microbial community dynamics and gives a guide for controlling biosolids application.
Research Center/Unit :
TERRA Research Centre. Plant Sciences - ULiège
Disciplines :
Environmental sciences & ecology
Author, co-author :
Sun, Tao ; Université de Liège - ULiège > TERRA Research Centre
Li, Guihua; State Key Laboratory of Efficient Utilization of Arid and Semi-arid Arable Land in Northern China, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing 100081, China
Mazarji, Mahmoud; State Key Laboratory of Efficient Utilization of Arid and Semi-arid Arable Land in Northern China, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing 100081, China
Delaplace, Pierre ; Université de Liège - ULiège > TERRA Research Centre > Plant Sciences
Yang, Xing; Key Laboratory of Agro-Forestry Environmental Processes and Ecological Regulation of Hainan Province, School of Ecology and Environment, Hainan University, Renmin Avenue, Haikou 570228, China
Zhang, Jianfeng; State Key Laboratory of Efficient Utilization of Arid and Semi-arid Arable Land in Northern China, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing 100081, China. Electronic address: zhangjianfeng@caas.cn
Pan, Junting; State Key Laboratory of Efficient Utilization of Arid and Semi-arid Arable Land in Northern China, Institute of Agricultural Resources and Regional Planning, Chinese Academy of Agricultural Sciences, Beijing 100081, China. Electronic address: panjunting@caas.cn
Language :
English
Title :
Heavy metals drive microbial community assembly process in farmland with long-term biosolids application.
NSCF - National Natural Science Foundation of China CSC - China Scholarship Council Earmarked Fund for China Agriculture Research System CAAS - Chinese Academy of Agricultural Sciences
The authors would like to thank the financial support by National Natural Science Foundation of China ( 22176215 ), the Earmarked fund for CARS ( CARS-06-14.5-A31 , CARS 23-B18 ), Agricultural Science and Technology Innovation Program of Chinese Academy of Agricultural Sciences and the China Scholarship Council (No. 202393250064 ).
Adingo, S., Yu, J.R., Xuelu, L., Li, X., Jing, S., Xiaong, Z., Variation of soil microbial carbon use efficiency (CUE) and its Influence mechanism in the context of global environmental change: a review. PeerJ, 9, 2021, e12131.
Alvarenga, P., Mourinha, C., Farto, M., Santos, T., Palma, P., Sengo, J., Cunha-Queda, C., Sewage sludge, compost and other representative organic wastes as agricultural soil amendments: benefits versus limiting factors. Waste Manag 40 (2015), 44–52.
Alvarenga, P., Palma, P., Mourinha, C., Farto, M., Dôres, J., Patanita, M., Sousa, J.P., Recycling organic wastes to agricultural land as a way to improve its quality: a field study to evaluate benefits and risks. Waste Manag 61 (2017), 582–592.
Amend, A.S., Martiny, A.C., Allison, S.D., Berlemont, R., Goulden, M.L., Lu, Y., Martiny, J.B., Microbial response to simulated global change is phylogenetically conserved and linked with functional potential. ISME J 10:1 (2016), 109–118.
Artursson, V., Finlay, R.D., Jansson, J.K., Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ Microbiol 8:1 (2006), 1–10.
Bastida, F., Eldridge, D.J., García, C., Kenny Png, G., Bardgett, R.D., Delgado-Baquerizo, M., Soil microbial diversity–biomass relationships are driven by soil carbon content across global biomes. ISME J 15:7 (2021), 2081–2091.
Bennett, A.E., Groten, K., The costs and benefits of plant–arbuscular mycorrhizal fungal interactions. Annu Rev Plant Biol 73 (2022), 649–672.
Cabral, L., Soares, C.R.F.S., Giachini, A.J., Siqueira, J.O., Arbuscular mycorrhizal fungi in phytoremediation of contaminated areas by trace elements: mechanisms and major benefits of their applications. World J Microbiol Biotechnol 31 (2015), 1655–1664.
Chen, J., He, F., Zhang, X., Sun, X., Zheng, J., Zheng, J., Heavy metal pollution decreases microbial abundance, diversity and activity within particle-size fractions of a paddy soil. FEMS Microbiol Ecol 87:1 (2014), 164–181.
Cheng, Z., Zheng, Q., Shi, J., He, Y., Yang, X., Huang, X., Xu, J., Metagenomic and machine learning-aided identification of biomarkers driving distinctive Cd accumulation features in the root-associated microbiome of two rice cultivars. ISME Commun, 3(1), 2023, 14.
Cui, G., Ai, S., Chen, K., Wang, X., Arbuscular mycorrhiza augments cadmium tolerance in soybean by altering accumulation and partitioning of nutrient elements, and related gene expression. Ecotoxicol Environ Saf 171 (2019), 231–239.
Dhalaria, R., Kumar, D., Kumar, H., Nepovimova, E., Kuča, K., Torequl Islam, M., Verma, R., Arbuscular mycorrhizal fungi as potential agents in ameliorating heavy metal stress in plants. Agronomy, 10(6), 2020, 815.
Drigo, B., Kowalchuk, G.A., Van Veen, J.A., Climate change goes underground: effects of elevated atmospheric CO2 on microbial community structure and activities in the rhizosphere. Biol Fertil Soils 44 (2008), 667–679.
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.
Evans, S., Martiny, J.B., Allison, S.D., Effects of dispersal and selection on stochastic assembly in microbial communities. ISME J 11:1 (2017), 176–185.
Ghori, N.H., Ghori, T., Hayat, M.Q., Imadi, S.R., Gul, A., Altay, V., Ozturk, M., Heavy metal stress and responses in plants. Int J Environ Sci Technol 16 (2019), 1807–1828.
Giller, K.E., Witter, E., Mcgrath, S.P., Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol Biochem 30:10-11 (1998), 1389–1414.
Green, G.B., Williams, M.B., Chehade, S.B., Morrow, C.D., Watts, S.A., Bej, A.K., 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 Brief, 42, 2022, 108313.
Hu, Y., Pang, S., Yang, J., Zhao, X., Cao, J., Changes in soil microbial community structure following amendment of biosolids for seven years. Environ Pollut Bioavailab 31:1 (2019), 24–31.
Jia, J., Hu, G., Ni, G., Xie, M., Li, R., Wang, G., Zhang, J., Bacteria drive soil multifunctionality while fungi are effective only at low pathogen abundance. Sci Total Environ, 906, 2024, 167596.
Jia, J., Zhang, J., Li, Y., Koziol, L., Podzikowski, L., Delgado-Baquerizo, M., Zhang, J., Relationships between soil biodiversity and multifunctionality in croplands depend on salinity and organic matter. Geoderma, 429, 2023, 116273.
Kasemodel, M.C., Sakamoto, I.K., Varesche, M.B.A., Rodrigues, V.G.S., Potentially toxic metal contamination and microbial community analysis in an abandoned Pb and Zn mining waste deposit. Sci Total Environ 675 (2019), 367–379.
Kirchmann, H., Börjesson, G., Kätterer, T., Cohen, Y., From agricultural use of sewage sludge to nutrient extraction: a soil science outlook. Ambio 46 (2017), 143–154.
Koupaie, E.H., Eskicioglu, C., Health risk assessment of heavy metals through the consumption of food crops fertilized by biosolids: a probabilistic-based analysis. J Hazard Mater 300 (2015), 855–865.
Kürsten, D., Möller, F., Gross, G.A., Lenk, C., Visaveliya, N., Schüler, T., Köhler, J.M., Identification of response classes from heavy metal‐tolerant soil microbial communities by highly resolved concentration‐dependent screenings in a microfluidic system. Methods Ecol Evol 6:5 (2015), 600–609.
Lian, M., Wang, J., Ma, Y., Li, J., Zeng, X., Influence of DOM and its subfractions on the mobilization of heavy metals in rhizosphere soil solution. Sci Rep, 12(1), 2022, 14082.
Lin, Y., Ye, Y., Hu, Y., Shi, H., The variation in microbial community structure under different heavy metal contamination levels in paddy soils. Ecotoxicol Environ Saf 180 (2019), 557–564.
Liu, C., Cui, Y., Li, X., Yao, M., microeco: an R package for data mining in microbial community ecology. FEMS Microbiol Ecol, 97(2), 2021, fiaa255.
Marchuk, S., Tait, S., Sinha, P., Harris, P., Antille, D.L., McCabe, B.K., Biosolids-derived fertilizers: a review of challenges and opportunities. Sci Total Environ, 875, 2023, 162555.
Mossa, A.W., Bailey, E.H., Usman, A., Young, S.D., Crout, N.M., The impact of long-term biosolids application (> 100 years) on soil metal dynamics. Sci Total Environ, 720, 2020, 137441.
Mossa, A.W., Dickinson, M.J., West, H.M., Young, S.D., Crout, N.M., The response of soil microbial diversity and abundance to long-term application of biosolids. Environ Pollut 224 (2017), 16–25.
Nemergut, D.R., Schmidt, S.K., Fukami, T., O'Neill, S.P., Bilinski, T.M., Stanish, L.F., Ferrenberg, S., Patterns and processes of microbial community assembly. Microbiol Mol Biol Rev 77:3 (2013), 342–356.
Op De Beeck, M., Lievens, B., Busschaert, P., Declerck, S., Vangronsveld, J., Colpaert, J.V., Comparison and validation of some ITS primer pairs useful for fungal metabarcoding studies. PloS One, 9(6), 2014, e97629.
Öpik, M., Vanatoa, A., Vanatoa, E., Moora, M., Davison, J., Kalwij, J.M., Zobel, M., The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). N Phytol 188:1 (2010), 223–241.
Pasqualetti, M., Mulas, B., Canzonetti, G., Benedetti, A., Tempesta, S., Effects of long-term heavy metal contamination on soil fungi in the Mediterranean area. Cryptogam, Mycol 33:1 (2012), 43–57.
Piotrowska-Seget, Z., Cycoń, M., Kozdroj, J., Metal-tolerant bacteria occurring in heavily polluted soil and mine spoil. Appl Soil Ecol 28:3 (2005), 237–246.
Priyadarshini, E., Priyadarshini, S.S., Cousins, B.G., Pradhan, N., Metal-fungus interaction: review on cellular processes underlying heavy metal detoxification and synthesis of metal nanoparticles. Chemosphere, 274, 2021, 129976.
Qin, X., Zhai, L., Khoshnevisan, B., Pan, J., Liu, H., Restriction of biosolids returning to land: fate of antibiotic resistance genes in soils after long-term biosolids application. Environ Pollut, 301, 2022, 119029.
Riaz, M., Kamran, M., Fang, Y., Wang, Q., Cao, H., Yang, G., Wang, X., Arbuscular mycorrhizal fungi-induced mitigation of heavy metal phytotoxicity in metal contaminated soils: a critical review. J Hazard Mater, 402, 2021, 123919.
Sanchez-Monedero, M.A., Cayuela, M.L., Roig, A., Jindo, K., Mondini, C., Bolan, N.J.B.T., Role of biochar as an additive in organic waste composting. Bioresour Technol 247 (2018), 1155–1164.
Schlatter, D.C., Schillinger, W.F., Bary, A.I., Sharratt, B., Paulitz, T.C., Biosolids and conservation tillage: impacts on soil fungal communities in dryland wheat-fallow cropping systems. Soil Biol Biochem 115 (2017), 556–567.
Shahid, M., Khalid, S., Abbas, G., Shahid, N., Nadeem, M., Sabir, M., Dumat, C., Heavy metal stress and crop productivity. Crop Prod Glob Environ Issues, 2015, 1–25.
Shen, Y., Li, H., Liu, Y., Gao, T., Li, G., Zuo, M., Zhang, W., Variations of fungal communities in lead–zinc tailings located in Northwestern China. Hum Ecol Risk Assess Int J 29:2 (2023), 390–409.
Shukla, P.K., Misra, P., Maurice, N., Ramteke, P.W., Heavy metal toxicity and possible functional aspects of microbial diversity in heavy metal-contaminated sites. Microb Genom Sustain Agroecosystems Volume 2 (2019), 255–317.
Silva, J.L.A., Souza, A.F., Jardim, J.G., Goto, B.T., Community assembly in harsh environments: the prevalence of ecological drift in the heath vegetation of South America. Ecosphere 6:7 (2015), 1–18.
Stegen, J.C., Lin, X., Fredrickson, J.K., Konopka, A.E., Estimating and mapping ecological processes influencing microbial community assembly. Front Microbiol, 6, 2015, 370.
Sullivan, T.S., Stromberger, M.E., Paschke, M.W., Ippolito, J.A., Long-term impacts of infrequent biosolids applications on chemical and microbial properties of a semi-arid rangeland soil. Biol Fertil Soils 42 (2006), 258–266.
Tang, B., Xu, H., Song, F., Ge, H., Yue, S., Effects of heavy metals on microorganisms and enzymes in soils of lead–zinc tailing ponds. Environ Res, 207, 2022, 112174.
Urra, J., Alkorta, I., Garbisu, C., Potential benefits and risks for soil health derived from the use of organic amendments in agriculture. Agronomy, 9(9), 2019, 542.
Van Der Heijden, M.G., Bardgett, R.D., Van Straalen, N.M., The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:3 (2008), 296–310.
Van Geel, M., Busschaert, P., Honnay, O., Lievens, B., Evaluation of six primer pairs targeting the nuclear rRNA operon for characterization of arbuscular mycorrhizal fungal (AMF) communities using 454 pyrosequencing. J Microbiol Methods 106 (2014), 93–100.
Vardanyan, A., Vyrides, I., Acidophilic bioleaching at high dissolved organic compounds: inhibition and strategies to counteract this. Miner Eng, 143, 2019, 105943.
Walters, W., Hyde, E.R., Berg-Lyons, D., Ackermann, G., Humphrey, G., Parada, A., Knight, R., Improved bacterial 16S rRNA gene (V4 and V4-5) and fungal internal transcribed spacer marker gene primers for microbial community surveys. Msystems 1:1 (2016), e00009–e00015.
Wang, M., Xue, J., Horswell, J., Kimberley, M.O., Huang, Z., Long-term biosolids application alters the composition of soil microbial groups and nutrient status in a pine plantation. Biol Fertil Soils 53 (2017), 799–809.
Wang, P., Li, S.P., Yang, X., Zhou, J., Shu, W., Jiang, L., Mechanisms of soil bacterial and fungal community assembly differ among and within islands. Environ Microbiol 22:4 (2020), 1559–1571.
Wang, Q., Jiang, X., Guan, D., Wei, D., Zhao, B., Ma, M., Li, J., Long-term fertilization changes bacterial diversity and bacterial communities in the maize rhizosphere of Chinese Mollisols. Appl Soil Ecol 125 (2018), 88–96.
Wood, S.A., Gilbert, J.A., Leff, J.W., Fierer, N., D'Angelo, H., Bateman, C., McGuire, K.L., Consequences of tropical forest conversion to oil palm on soil bacterial community and network structure. Soil Biol Biochem 112 (2017), 258–268.
Xu, M., Cui, Y., Beiyuan, J., Wang, X., Duan, C., Fang, L., Heavy metal pollution increases soil microbial carbon limitation: evidence from ecological enzyme stoichiometry. Soil Ecol Lett 3:3 (2021), 230–241.
Zarei, M., Hempel, S., Wubet, T., Schäfer, T., Savaghebi, G., Jouzani, G.S., Buscot, F., Molecular diversity of arbuscular mycorrhizal fungi in relation to soil chemical properties and heavy metal contamination. Environ Pollut 158:8 (2010), 2757–2765.
Zeng, X.Y., Li, S.W., Leng, Y., Kang, X.H., Structural and functional responses of bacterial and fungal communities to multiple heavy metal exposure in arid loess. Sci Total Environ, 723, 2020, 138081.
Zhang, M., Zhang, T., Zhou, L., Lou, W., Zeng, W., Liu, T., Meng, D., Soil microbial community assembly model in response to heavy metal pollution. Environ Res, 213, 2022, 113576.
Zhong, X., Chen, Z., Ding, K., Liu, W.S., Baker, A.J., Fei, Y.H., Qiu, R., Heavy metal contamination affects the core microbiome and assembly processes in metal mine soils across Eastern China. J Hazard Mater, 443, 2023, 130241.