Abstract
Globally, heavy metal (HM) pollution of soil is a serious problem that can lead to long-term toxic effects on soil. In this milieu, the present study investigated the eco-toxicological effects of three trace elements, e.g., cadmium (Cd), copper (Cu), and lead (Pb), on enzyme activities and microbial function and structural diversity in phaeozem and red soil samples. Hormesis effects of Cd, Cu, and Pb on catalase and invertase activities were observed in phaeozem soil, while for red soil, there was an inhibitory effect on the activities of catalase and invertase under Cu- and Pb-contaminated soils. The utilization of carbon sources was inhibited in Cd- and Pb-treated phaeozem soil, but higher utilization of polymers and amines exhibited in Cu-contaminated soil. Although the substrates under the contamination of Cd, Cu, and Pb had high average well color development values across incubation time, the utilization of various substrates did not exhibit a regular trend under different treatments with HMs. The denaturing gradient gel electrophoresis (DGGE) analysis showed that the HMs led to marginal changes in the number and species of soil microbes, while the similarity indices decreased in HM-treated samples, varying from 66.2 to 77.3% in phaeozem soil and from 62.8 to 66.7% in red soil. However, the sequence analysis showed that there existed metal-resistant microbial communities such as Bacillales, Bacillus, and Massilia and so on under the stress of HMs.
Similar content being viewed by others
Abbreviations
- HM:
-
Heavy metal
- AWCD:
-
Average well color development
- CLPP:
-
Community-level physiological profile
- DGGE:
-
Denaturing gradient gel electrophoresis
- MARA:
-
Ministry of Agriculture and Rural Affairs
References
Abicht, H. K., Kumar, R., Mancini, S., Solioz, M., & Fischermeier, E. (2016). Copper resistance and its regulation in the sulfate reducing bacterium Desulfosporosinus sp. OT. Microbiology, 162, 684–693.
Ai, C., Liang, G., Sun, J., He, P., Tang, S., Yang, S., Zhou, W., & Wang, X. (2015). The alleviation of acid soil stress in rice by inorganic or organic ameliorants is associated with changes in soil enzyme activity and microbial community composition. Biology and Fertility of Soils, 51, 465–477.
Allard, S., Enurah, A., Strain, E., Millner, P., Rideout, S. L., Brown, E. W., & Zhen, J. (2014). In situ evaluation of Paenibacillus alvei in reducing carriage of Salmonella enterica serovar Newport on whole tomato plants. Applied & Environmental Microbiology, 80, 3842–3850.
Aslam, A., Thomas-Hall, S. R., Mughal, T., Zaman, Q. U., & Schenk, P. M. (2019). Heavy metal bioremediation of coal–fired flue gas using microalgae under different CO2 concentrations. Journal of Environmental Management, 241, 243–250.
Bååth, E. (1989). Effects of heavy metals in soil on microbial processes and populations (a review). Water, Air, and Soil Pollution, 47, 335–379.
Basta, N. T., Gradwohl, R., Snethen, K. L., & Schroder, J. L. (2001). Chemical immobilization of lead, zinc, and cadmium in smelter-contaminated soils using biosolids and rock phosphate. Journal of Environmental Quality, 30, 1222–1230.
Calvarro, L. M., Santiago-Martín, A. D., Gómez, J. Q., González-Huecas, C., Quintana, J. R., Vázquez, A., Lafuente, A. L., Fernández, T. M. R., & Vera, R. R. (2014). Biological activity in metal–contaminated calcareous agricultural soils: the role of the organic matter composition and the particle size distribution. Environmental Science & Pollution Research International, 21, 6176–6187.
Chen, J., He, F., Zhang, X., Sun, X., Zheng, J., & Zheng, J. (2014). Heavy metal pollution decreases microbial abundance, diversity and activity within particle-size fractions of a paddy soil. FEMS Microbiology Ecology, 87, 164–181.
Ciarkowska, K., Sołek-Podwika, K., & Wieczorek, J. (2014). Enzyme activity as an indicator of soil-rehabilitation processes at a zinc and lead ore mining and processing area. Journal of Environmental Management, 132, 250–256.
Deng, A. H., Sun, Z. P., Zhang, G. Q., Wu, J., & Wen, T. Y. (2012). Rapid discrimination of newly isolated Bacillales with industrial applications using Raman spectroscopy. Laser Physics Letters, 9, 636–642.
Ding, Z., Wu, J., You, A., Huang, B., & Cao, C. (2017). Effects of heavy metals on soil microbial community structure and diversity in the rice (Oryza sativa L. subsp. Japonica) rhizosphere. Soil Science & Plant Nutrition, 63, 75–83.
Dror, B., Jurkevitch, E., & Cytryn, E. (2020). State-of-the-art methodologies to identify antimicrobial secondary metabolites in soil bacterial communities—a review. Soil Biology and Biochemistry, 147, 107838.
E.F.S.A. (2009). Scientific opinion of the panel on contaminants in the food chain on a request from the European Commission on cadmium in food. The EFSA Journal, 980, 1–139.
Epelde, L., Lanzén, A., Blanco, F., Urich, T., & Garbisu, C. (2015). Adaptation of soil microbial community structure and function to chronic metal contamination at an abandoned Pb-Zn mine. FEMS Microbiology Ecology, 91, 1–11.
Fang, L. C., Liu, Y. Q., Tian, H. X., Chen, H. S., Wang, Y. Q., & Huang, M. (2017). Proper land use for heavy metal–polluted soil based on enzyme activity analysis around a Pb–Zn mine in Feng County, China. Environmental Science & Pollution Research, 24, 1–13.
Fei, W., Yao, J., Yang, S., Chen, H., Russel, M., Ke, C., Qian, Y., Zaray, G., & Bramanti, E. (2010). Short–time effect of heavy metals upon microbial community activity. Journal of Hazardous Materials, 173, 510–516.
Feris, K. P., Ramsey, P. W., Frazar, C., Rillig, M., Moore, J. N., Gannon, J. E., & Holben, W. E. (2004). Seasonal dynamics of shallow–hyporheic–zone microbial community structure along a heavy–metal contamination gradient. Applied and Environmental Microbiology, 70, 2323–2331.
Foley, M. E., Sigler, V., & Gruden, C. L. (2007). A multiphasic characterization of the impact of the herbicide acetochlor on freshwater bacterial communities. The ISME Journal, 2, 56–66.
Freedman, A. J., Tan, B., & Thompson, J. R. (2017). Microbial potential for carbon and nutrient cycling in a geogenic supercritical carbon dioxide reservoir. Environmental Microbiology, 19, 2228–2245.
Gao, Y., Zhou, P., Mao, L., Zhi, Y. E., & Shi, W. J. (2010). Assessment of effects of heavy metals combined pollution on soil enzyme activities and microbial community structure: modified ecological dose–response model and PCR-RAPD. Environmental Earth Sciences, 60, 603–612.
Gao, J., Song, P., Wang, G., Wang, J., Zhu, L., & Wang, J. (2018). Responses of atrazine degradation and native bacterial community in soil to Arthrobacter sp. strain hb-5. Ecotoxicology & Environmental Safety, 159, 317–323.
Garau, G., Castaldi, P., Santona, L., Deiana, P., & Melis, P. (2007). Influence of red mud, zeolite and lime on heavy metal immobilization, culturable heterotrophic microbial populations and enzyme activities in a contaminated soil. Geoderma, 142, 47–57.
García-Ruiz, R., Ochoa, V., Vinegla, B., Hinojosa, M., Pena-Santiago, R., Liébanas, G., Linares, J., & Carreira, J. (2009). Soil enzymes, nematode community and selected physico–chemical properties as soil quality indicators in organic and conventional olive oil farming: influence of seasonality and site features. Applied Soil Ecology, 41, 305–314.
Gillan, D. C., Danis, B., Pernet, P., Joly, G., & Dubois, P. (2005). Structure of sediment-associated microbial communities along a heavy-metal contamination gradient in the marine environment. Applied & Environmental Microbiology, 71, 679–690.
Gomez, E., & Garland, J. L. (2012). Effects of tillage and fertilization on physiological profiles of soil microbial communities. Applied Soil Ecology, 61, 327–332.
Gryta, A., Frąc, M., & Oszust, K. (2014). The application of the Biolog EcoPlate approach in ecotoxicological evaluation of dairy sewage sludge. Applied Biochemistry and Biotechnology, 174, 1434–1443.
Gu, Y., Wang, P., & Kong, C. (2009). Urease, invertase, dehydrogenase and polyphenoloxidase activities in paddy soil influenced by allelopathic rice variety. European Journal of Soil Biology, 45, 436–441.
Guo, J. H., Li, H. P., & Zhu, H. H. (2010). Analysis of dominant species of microbial community in heavy metals contaminated soil from Dabaoshan Area. Journal of South China Agricultural University, 31, 56–48.
Guo, D., Fan, Z., Lu, S., Ma, Y., Nie, X., Tong, F., & Peng, X. W. (2019). Changes in rhizosphere bacterial communities during remediation of heavy metal–accumulating plants around the Xikuangshan mine in southern China. Scientific Reports, 9, 1947.
Gupta, N., Khan, D., & Santra, S. (2012). Heavy metal accumulation in vegetables grown in a long–term wastewater-irrigated agricultural land of tropical India. Environmental Monitoring and Assessment, 184, 6673–6682.
Hassanshahian, M., Bayat, Z., Cappello, S., Smedile, F., & Yakimov, M. (2016). Comparison the effects of bioaugmentation versus biostimulation on marine microbial community by PCR–DGGE: a mesocosm scale. Journal of Environmental Sciences, 43, 136–146.
Hong, C., Si, Y., Xing, Y., & Li, Y. (2015). Illumina MiSeq sequencing investigation on the contrasting soil bacterial community structures in different iron mining areas. Environmental Science & Pollution Research, 22, 10788–10799.
Hu, J., Lin, X., Wang, J., Dai, J., Chen, R., Zhang, J., & Wong, M. H. (2011). Microbial functional diversity, metabolic quotient, and invertase activity of a sandy loam soil as affected by long–term application of organic amendment and mineral fertilizer. Journal of Soils and Sediments, 11, 271–280.
Hu, B., Liang, D., Liu, J., Lei, L., & Yu, D. (2014). Transformation of heavy metal fractions on soil urease and nitrate reductase activities in copper and selenium co–contaminated soil. Ecotoxicology and Environmental Safety, 110, 41–48.
Ikhajiagbe, B. (2013). Changes in heavy metal contents of a waste engine oil polluted soil exposed to soil pH adjustments. British Biotechnology Journal, 3, 158–168.
Kelly, J. J., & Tate, R. L. (1998). Effects of heavy metal contamination and remediation on soil microbial communities in the vicinity of a zinc smelter. Journal of Environmental Quality, 27, 609–617.
Kenarova, A., Radeva, G., Traykov, I., & Boteva, S. (2014). Community level physiological profiles of bacterial communities inhabiting uranium mining impacted sites. Ecotoxicology and Environmental Safety, 100, 226–232.
Khan, S., Hesham, A. E. L., Qiao, M., Rehman, S., & He, J. Z. (2010). Effects of Cd and Pb on soil microbial community structure and activities. Environmental Science and Pollution Research, 17, 288–296.
Kuscu, I. S. K. (2019). Changing of soil properties and urease–catalase enzyme activity depending on plant type and shading. Environmental Monitoring and Assessment, 191, 178.
La, S. B., Birtles, R. J., Mallet, M. N., & Raoult, D. (1998). Massilia timonae gen. nov., sp. nov., isolated from blood of an immunocompromised patient with cerebellar lesions. Journal of Clinical Microbiology, 36, 2847–2852.
Li, Q., Hu, Q., Zhang, C. L., Müller, W. G., Schröder, H., Li, Z. Y., Zhang, Y., Liu, C., & Jin, Z. J. (2015). The effect of toxicity of heavy metals contained in tailing sands on the organic carbon metabolic activity of soil microorganisms from different land use types in the karst region. Environmental Earth Sciences, 74, 6747–6756.
Li, H. X., Zhou, L. J., Lin, H., Xu, X. Y., Jia, R. Y., & Xia, S. Q. (2018). Dynamic response of biofilm microbial ecology to para–chloronitrobenzene biodegradation in a hydrogen-based, denitrifying and sulfate–reducing membrane biofilm reactor. Science of the Total Environment, 643, 842–849.
Lin, L. (2013). Clonization and modulation of host growth and metal uptake by endophytic bacteria of Sedum alfredii. International Journal of Phytoremediation 15, 51–64.
Liu, R., Xiao, N., Wei, S., Zhao, L., & An, J. (2014). Rhizosphere effects of PAH-contaminated soil phytoremediation using a special plant named Fire Phoenix. Science of the Total Environment, 473, 350–358.
Liu, Z. J., Rong, Q., Zhou, W., & Liang, G. Q. (2017). Effects of inorganic and organic amendment on soil chemical properties, enzyme activities, microbial community and soil quality in yellow clayey soil. PLoS One, 12(3), e0172767.
Lu, R. K. (1999). Analytical methods of agricultural chemistry in soil. Beijing: China Agricultural Scientech Press.
Luo, X. S., Yu, S., Zhu, Y. G., & Li, X. D. (2012). Trace metal contamination in urban soils of China. Science of the Total Environment, 421–422, 17–30.
Manici, L. M., Saccà, M. L., Caputo, F., Zanzotto, A., Gardiman, M., & Fila, G. (2017). Long–term grapevine cultivation and agro–environment affect rhizosphere microbiome rather than plant age. Applied Soil Ecology, 119, 214–225.
Maron, P. A., Sarr, A., Kaisermann, A., Lévêque, J., Mathieu, O., Guigue, J., Karimi, B., Bernard, L., Dequiedt, S., Terrat, S., Chabbi, A., & Ranjard, L. (2018). High microbial diversity promotes soil ecosystem functioning. Applied & Environmental Microbiology, 84, e02738–e02717.
Menegassi, A., Silva, R. D. S. E., Carlini, C. R., Mithöfer, A., & Becker-Ritt, A. B. B. (2017). Analysis of herbivore stress– and phytohormone–mediated urease expression in soybean (Glycine max). Journal of Plant Growth Regulation, 7, 1–7.
Meng, K., Ren, W. J., Teng, Y., Wang, B. B., Han, Y. J., Christie, P., & Luo, Y. M. (2019). Application of biodegradable seedling trays in paddy fields: impacts on the microbial community. Science of the Total Environment, 656, 750–759.
Morelli, F., Benedetti, Y., Perna, P., & Santolini, R. (2018). Associations among taxonomic diversity, functional diversity and evolutionary distinctiveness vary among environments. Ecological Indicators, 88, 8–16.
Morkunas, I., Woźniak, A., Mai, V. C., Rucińska-Sobkowiak, R., & Jeandet, P. (2018). The role of heavy metals in plant response to biotic stress. Molecules, 23, 2320.
Nacke, H., Gonçalves, A. C., Schwantes, D., Nava, I. A., Strey, L., & Coelho, G. F. (2013). Availability of heavy metals (Cd, Pb, and Cr) in agriculture from commercial fertilizers. Archives of Environmental Contamination and Toxicology, 64, 537–544.
Nogueira, T. A. R., Franco, A., He, Z., Braga, V. S., Firme, L. P., & Abreu-Junior, C. H. (2013). Short-term usage of sewage sludge as organic fertilizer to sugarcane in a tropical soil bears little threat of heavy metal contamination. Journal of Environmental Management, 114, 168–177.
Nottingham, A. T., Turner, B. L., Whitaker, J., Ostle, N., Bardgett, R. D., McNamara, N. P., Salinas, N., & Meir, P. (2016). Temperature sensitivity of soil enzymes along an elevation gradient in the Peruvian Andes. Biogeochemistry, 127, 217–230.
Pacwa-Płociniczak, M., Płociniczak, T., Yu, D., Kurola, J. M., Sinkkonen, A., Piotrowska-Seget, Z., & Romantschuk, M. (2018). Effect of silene vulgaris and heavy metal pollution on soil microbial diversity in long–term contaminated soil. Water Air and Soil Pollution, 229, 13.
Pal, A., Dutta, S., & Paul, A. K. (2005). Reduction of hexavalent chromium by cell-free extract of Bacillus sphaericus AND 303 isolated from serpentine soil. Current Microbiology, 51, 327–330.
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, 327–341.
Sahoo, D. K., Kar, R. N., & Das, R. P. (1992). Bioaccumulation of heavy metal ions by Bacillus circulans. Bioresource Technology, 41, 177–179.
Sánchez-Moreno, S., & Navas, A. (2007). Nematode diversity and food web condition in heavy metal polluted soils in a river basin in southern Spain. European Journal of Soil Biology, 43, 166–179.
Sardar, K., Qing, C., Hesham, A. E. L., Yue, X., & He, J. Z. (2007). Soil enzymatic activities and microbial community structure with different application rates of Cd and Pb. Journal of Environmental Sciences, 19, 834–840.
Shi, L. M., Cai, Y. F., Yang, H. L., Xing, P., Li, P. F., Kong, L. D., & Kong, F. X. (2009). Phylogenetic diversity and specificity of bacteria associated with Microcystis aeruginosa and other cyanobacteria. Journal of Environmental Sciences, 21, 1581–1590.
Stefanowicz, A. M., Niklińska, M., & Laskowski, R. (2009). Pollution–induced tolerance of soil bacterial communities in meadow and forest ecosystems polluted with heavy metals. European Journal of Soil Biology, 45, 363–369.
Sud, D., Mahajan, G., & Kau, M. P. (2008). Agricultural waste material as potential adsorbent for sequestering heavy metal ions from aqueous solutions—a review. Bioresource Technology, 99, 6017–6027.
Sullivan, T. S., Mcbride, M. B., & Thies, J. E. (2013). Rhizosphere microbial community and Zn uptake by willow (Salix purpurea L.) depend on soil sulfur concentrations in metalliferous peat soils. Applied Soil Ecology, 67, 53–60.
Sun, Y. B., Zhou, Q. X., Xie, X. K., & Liu, R. (2010). Spatial, sources and risk assessment of heavy metal contamination of urban soils in typical regions of Shenyang, China. Journal of Hazardous Materials, 174, 455–462.
Sun, Y. B., Sun, G. H., Xu, Y. M., Wang, L., Liang, X. F., & Lin, D. S. (2013). Assessment of sepiolite for immobilization of cadmium-contaminated soils. Geoderma, 193, 149–155.
Sun, Y. B., Sun, G. H., Xu, Y. M., Liu, W. T., Liang, X. F., & Wang, L. (2016a). Evaluation of the effectiveness of sepiolite, bentonite, and phosphate amendments on the stabilization remediation of cadmium-contaminated soils. Journal of Environmental Management, 166, 204–210.
Sun, Y. B., Xu, Y., Xu, Y. M., Wang, L., Liang, X. F., & Li, Y. (2016b). Reliability and stability of immobilization remediation of Cd polluted soils using sepiolite under pot and field trials. Environmental Pollution, 208, 739–746.
Torrijos, V., Ruiz, I., & Soto, M. (2018). Microbial activities and process rates in two–step vertical and horizontal subsurface flow gravel and sand filters. Water Air & Soil Pollution, 229, 290.
Vorobeichik, E. L., & Kaigorodova, S. Y. (2017). Long–term dynamics of heavy metals in the upper horizons of soils in the region of a copper smelter impacts during the period of reduced emission. Eurasian Soil Science, 50, 977–990.
Wallenius, K., Rita, H., Simpanen, S., Mikkonen, A., & Niemi, R. (2010). Sample storage for soil enzyme activity and bacterial community profiles. Journal of Microbiological Methods, 81, 48–55.
Wei, X., Chen, A., Wang, S., Cao, G., Cai, P., & Shu, L. I. (2016). A comparative study of soil microbial carbon source utilization in different successive rotation plantations of Chinese fir. Chinese Journal of Applied and Environmental Biology, 3, 518–523.
Wickramatilake, A. R. P., Munehiro, R., Nagaoka, T., Wasaki, J., & Kouno, D. K. (2011). Compost amendment enhances population and composition of phosphate solubilizing bacteria and improves phosphorus availability in granitic regosols. Soil Science & Plant Nutrition, 57, 529–540.
Wittebolle, L., Marzorati, M., Clement, L., Balloi, A., Daffonchio, D., Heylen, K., De Vos, P., & Verstraete, W. N. B. (2009). Initial community evenness favours functionality under selective stress. Nature, 458, 623–626.
Xian, Y., Wang, M., & Chen, W. (2015). Quantitative assessment on soil enzyme activities of heavy metal contaminated soils with various soil properties. Chemosphere, 139, 604–608.
Yang, Z. X., Liu, S. Q., Zheng, D. W., & Feng, S. D. (2006). Effects of cadmium, zinc and lead on soil enzyme activities. Journal of Environmental Sciences, 18, 1135–1141.
Yang, Q., Li, Z., Lu, X., Duan, Q., Huang, L., & Bi, J. (2018). A review of soil heavy metal pollution from industrial and agricultural regions in China: pollution and risk assessment. Science of the Total Environment, 642, 690–700.
Yao, H. Y., Xu, J. M., & Huang, C. Y. (2003). Substrate utilization pattern, biomass and activity of microbial communities in a sequence of heavy metal–polluted paddy soils. Geoderma, 115, 139–148.
Zeb, A., Li, S., Wu, J. N., Liang, J. P., Liu, W. T., & Sun, Y. B. (2020). Insights into the mechanisms underlying the remediation potential of earthworms in contaminated soil: a critical review of research progress and prospects. Science of the Total Environment, 740, 140145.
Zhou, Q. X., & Song, Y. F. (2004). Principles and methods of contaminated soil remediation. Beijing: Science Press.
Funding
This work was supported by the National Key Research and Development Program of China (2017YFD0801402; 2018YFD0800305), the National Natural Science Foundation of China (31971525), and the Central Public-Interest Scientific Institution Basal Research Fund(No. Y2020PT03).
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Yuebing, S., Shunan, Z., Lin, W. et al. Changes of Enzymatic Activities, Substrate Utilization Pattern, and Microbial Community Diversity in Heavy Metal-Contaminated Soils. Water Air Soil Pollut 231, 422 (2020). https://doi.org/10.1007/s11270-020-04798-2
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11270-020-04798-2