Skip to main content

Advertisement

Log in

The Variations of Bacterial Community Structures in Tailing Soils Suffering from Heavy Metal Contaminations

  • Published:
Water, Air, & Soil Pollution Aims and scope Submit manuscript

Abstract

Investigations of the impact of heavy metals on microbial community structure are crucial for bioremediation of the contaminated sites. To this end, high-throughput 16S rRNA sequencing was performed to assess the variations of bacterial communities in 6 heavy metal-contaminated soils sampled from Liujiaping (LJP) and Shanping (SP) lead–zinc tailings situated in northwestern China. Compared with those of the farmland soil (NT), the heavy metal levels and chemical properties of the tailing soils were significantly different. Consistently, the bacterial community structures have been changed, displaying as the bacterial richness and diversity in the tailing soils were either increased or decreased, i.e., trending as SP > NT > LJP. The relative abundances of certain bacterial phyla mainly including Actinobacteriota, Acidobacteriota, Cyanobacteria, Gemmatimonadota, and Bacteroidota were significantly increased in certain SP and/or LJP soils. Further, the relative abundances of Actinobacteriota and Bacteroidota were positively correlated with Cd, TP, TK, SOM, TN, and pH. The abundance of Cyanobacteria was significantly upregulated by Cu, Zn, and TP. Acidobacteriota was notably positively correlated with Cr, Pb, and NO3_N. On the contrary, the relative abundance of Chloroflexi was negatively correlated with all the environmental parameters, especially with Cd, NO3_N, TP, SOM, and TN. Together, our results implied that the heavy metals and chemical properties were both driving forces of the variations of the bacterial community structures in the tailing soils. Overall, we have successfully identified certain bacterial species such as s__unclassified_g__Sulfurifustis, s__unclassified_f__Rhodanobacteraceae, s__unclassified_g__Conexibacter, s__unclassified_g__norank_f__norank_o__Gaiellales, and s__unclassified_g__Blastococcus which were probably heavy metal-tolerant in these specific tailing soils, and this will provide a theoretical support for further bioremediations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abia, A. L. K., Alisoltani, A., Keshri, J., & Ubomba-Jaswa, E. (2018). Metagenomic analysis of the bacterial communities and their functional profiles in water and sediments of the Apies River, South Africa, as a function of land use. Science of the Total Environment, 616–617, 326–334.

    Article  CAS  Google Scholar 

  • Agurto-Detzel, H., Bianchi, M., Assumpção, M., Schimmel, M., Collaço, B., Ciardelli, C., Barbosa, J. R., & Calhau, J. (2016). The tailings dam failure of 5 November 2015 in SE Brazil and its preceding seismic sequence. Geophysical Research Letters, 43, 4929–4936.

    Article  Google Scholar 

  • Akcil, A., Erust, C., Ozdemiroglu, S., Fonti, V., & Beolchini, F. (2015). A review of approaches and techniques used in aquatic contaminated sediments: Metal removal and stabilization by chemical and biotechnological processes. Journal of Cleaner Production, 86, 24–36.

    Article  CAS  Google Scholar 

  • An, F., Diao, Z., & Lv, J. (2018). Microbial diversity and community structure in agricultural soils suffering from 4 years of Pb contamination. Canadian Journal of Microbiology, 64, 305–316.

    Article  CAS  Google Scholar 

  • Alvarez, A., Saez, J. M., Costa, J. S. D., Colin, V. L., Fuentes, M. S., Cuozzo, S. A., Benimeli, S. M., Polti, M. A., & Amoroso, J. M. (2017). Actinobacteria: Current research and perspectives for bioremediation of pesticides and heavy metals. Chemosphere, 166, 41–62.

    Article  CAS  Google Scholar 

  • Ash, C., Tejnecký, V., Borůvka, L., & Drábek, O. (2016). Different low-molecular-mass organic acids specifically control leaching of arsenic and lead from contaminated soil. Journal of Contaminant Hydrology, 187, 18–30.

    Article  CAS  Google Scholar 

  • Ashok, B.,& Geetha, N. (2018). Chapter 18 - Recent trends in biosorption of heavy metals by Actinobacteria, Editor(s): Bhim Pratap Singh, Vijai Kumar Gupta, Ajit Kumar Passari, New and future developments in microbial biotechnology and bioengineering, Elsevier, 257–275

  • Audu, K. E., Adeniji, S. E., & Obidah, J. S. (2020). Bioremediation of toxic metals in mining site of Zamfara metropolis using resident bacteria (Pantoea agglomerans): A optimization approach. Heliyon, 6(e04704), 1–7. https://doi.org/10.1016/j.heliyon.2020.e04704

    Article  Google Scholar 

  • Becerra-Castro, C., Lopes, A. R., Vaz-Moreira, I., Silva, E. F., Manaia, C. M., & Nunes, O. C. (2015). Wastewater reuse in irrigation: A microbiological perspective on implications in soil fertility and human and environmental health. Environmental International, 75, 117–135.

    Article  CAS  Google Scholar 

  • Bier, R. L., Voss, K. A., & Bernhardt, E. S. (2015). Bacterial community responses to a gradient of alkaline mountaintop mine drainage in Central Appalachian streams. The International Society for Microbial Ecology Journal, 9, 1378–1390.

    CAS  Google Scholar 

  • Caban, J. R., Kuppusamy, S., Kim, J. H., Yoon, Y., Kim, S. Y., & Lee, Y. B. (2018). Green manure amendment enhances microbial activity and diversity in antibiotic-contaminated soil. Applied Soil Ecology, 129, 72–76.

    Article  Google Scholar 

  • Chikere, C. B., Mordi, I. J., Chikere, B. O., Selvarajan, R., Ashafa, T. O., & Obieze, C. C. (2019). Comparative metagenomics and functional profiling of crude oil-polluted soils in Bodo West Community, Ogoni, with other sites of varying pollution history. Annals of Microbiology, 69, 495–513.

    Article  CAS  Google Scholar 

  • Choudhury, S. G., Srivastava, S., Singh, R., Chaudhari, S. K., Sharma, D. K., Singh, S. K., & Sarkar, D. (2014). Tillage and residue management effects on soil aggregation, organic carbon dynamics and yield attribute in rice-wheat cropping system under reclaimed sodic soil. Soil and Tillage Research, 136, 76–83.

    Article  Google Scholar 

  • Cui, J. Q., He, Q. S., Liu, M. H., Chen, H., Sun, M. B., & Wen, J. P. (2020). Comparative study on different remediation strategies applied in petroleum contaminated soils. International Journal of Environmental Research and Public Health, 17, 1–17.

    Article  Google Scholar 

  • Dixit, R., Malaviya, D., Pandiyan, K., Singh, U. B., Sahu, A., Shukla, R., Singh, B. P., Rai, J. P., Sharma, P. K., & Lade, H. (2015). Bioremediation of heavy metals from soil and aquatic environment: An overview of principles and criteria of fundamental processes. Sustainability, 7, 2189–2212.

    Article  Google Scholar 

  • Eichorst, S. A., Breznak, J. A., & Schmidt, T. M. (2007). Isolation and characterization of soil bacteria that define Terriglobus gen. nov., in the phylum Acidobacteria. Applied and Environmental Microbiology, 73, 2708–2717.

    Article  CAS  Google Scholar 

  • Fernández, N., Sierra-Alvarez, R., Field, J. A., Amils, R., & Sanz, J. L. (2008). Microbial community dynamics in a chemolithotrophic denitrification reactor inoculated with methanogenic granular sludge. Chemosphere, 70, 462–474.

    Article  CAS  Google Scholar 

  • Fierer, N., Morse, J. L., Berthrong, S. T., Bernhardt, E. S., & Jackson, R. B. (2007). Environmental controls on the landscape-scale biogeography of stream bacterial communities. Ecology, 88, 2162–2173.

    Article  Google Scholar 

  • Gabarrón, M., Faz, A., & Acosta, J. A. (2018). Use of multivariable and redundancy analysis to assess the behavior of metals and arsenic in urban soil and road dust affected by metallic mining as a base for risk assessment. Journal of Environmental Management, 206, 192–201.

    Article  CAS  Google Scholar 

  • Gao, T., Wan, Z., Liu, X., Fu, J., Chang, G., & H., Sun, H., Li, H., Shen, Y., Liu, Y., & X.W. Fang, X. . (2021). Effects of heavy metals on bacterial community structure in the rhizosphere of Salsola collina and bulk soil in the Jinchuan mining area. Geomicrobiology Journal, 38(7), 620–630.

  • Guo, Y., Liu, X., Tsolmon, B., Chen, J., & Bao, Y. (2019). The influence of transplanted trees on soil microbial diversity in coal mine subsidence areas in the loess plateau of china. Global Ecology and Conservation, 21(e00877), 1–14. https://doi.org/10.1016/j.gecco.2019.e00877

    Article  Google Scholar 

  • Hooda, P. S., & Alloway, B. J. (1998). Cadmium and lead sorption behavior of selected English and Indian soils. Geoderma, 84, 121–134.

    Article  CAS  Google Scholar 

  • Jacobson, R., & Faust, T. (2014). Hydrologic connectivity of floodplains, northern Missouri-Implications for management and restoration of floodplain forest communities in disturbed landscapes. River Research and Applications, 30, 269–286.

    Article  Google Scholar 

  • Jiang, B., Adebayo, A., Jia, J., Xing, Y., Deng, S., Guo, L., Liang, Y., & Zhang, D. (2020). Impacts of heavy metals and soil properties at a Nigerian e-waste site on soil microbial community. Journal of Hazardous Materials, 362, 187–195.

    Article  CAS  Google Scholar 

  • Jiang, B., Zhang, B., Li, L., Zhao, Y., Shi, Y., Jiang, Q., & Jia, L. (2021). Analysis of microbial community structure and diversity in surrounding rock soil of different waste dump sites in Fushun western opencast mine. Chemosphere, 269(128777), 1–11. https://doi.org/10.1016/j.chemosphere.2020.128777

    Article  CAS  Google Scholar 

  • Kan, X., Dong, Y., Feng, L., Zhou, M., & Hou, H. (2021). Contamination and health risk assessment of heavy metals in China’s lead-zinc mine tailings: A meta-analysis. Chemosphere, 267(128909), 1–9. https://doi.org/10.1016/j.chemosphere.2020.128909

    Article  CAS  Google Scholar 

  • Kang, X. H., Leng, Y., & O, M. M., Zeng, X. Y., & Li, S. W. . (2020). The seasonal changes of core bacterial community decide sewage purification in sub-plateau municipal sewage treatment plants. Bioprocess and Biosystems Engineering, 43, 1609–1617.

  • Katiyar, P., Pandey, N., & Sahu, K. K. (2020). Biological approaches of fluoride remediation: Potential for environmental clean-up. Environmental Science and Pollution Research, 27, 13044–13055.

    Article  CAS  Google Scholar 

  • Kuang, J. L., Huang, L. N., Chen, L. X., Hua, Z. S., Li, S. J., Hu, M., Li, J. T., & Shu, W. S. (2013). Contemporary environmental variation determines microbial diversity patterns in acid mine drainage. ISME Journal, 7, 1038–1050.

    Article  CAS  Google Scholar 

  • Li, H., Ye, D., Wang, X., Settles, M., Wang, J., Hao, Z., Zhou, L., Dong, P., Jiang, Y., & Ma, Z. (2014a). Soil bacterial communities of different natural forest types in Northeast China. Plant and Soil, 383, 203–216.

    Article  CAS  Google Scholar 

  • Li Zeng He Chen Han Wang, H. X. C. Z. X. E. G. Y. Y. (2016). Long-term performance of rapid oxidation of arsenite in simulated groundwater using a population of arsenite-oxidizing microorganisms in a bioreactor. Water Research., 101, 393–401.

    Article  CAS  Google Scholar 

  • Li, J., Xin, Z., Yan, J., Li, H., Chen, J., & Ding, G. (2018). Physicochemical and microbiological assessment of soil quality on a chronosequence of a mine reclamation site. European Journal of Soil Science, 69, 1056–1067.

    Article  CAS  Google Scholar 

  • Li, Q., You, P., Hu, Q., Leng, B., Wang, J., Chen, J., Wan, S., Wang, B., Yuan, C., Zhou, R., & Ouyang, K. (2020). Effects of co-contamination of heavy metals and total petroleum hydrocarbons on soil bacterial community and function network reconstitution. Ecotoxicology and Environmental Safety, 204(111083), 1–10. https://doi.org/10.1016/j.ecoenv.2020.111083

    Article  CAS  Google Scholar 

  • Li, Z., Ma, Z., Kuijp, T. J. V. D., Yuan, Z., & Huang, L. (2014b). A review of soil heavy metal pollution from mines in China: Pollution and health risk assessment. Science of the Total Environment, 468, 843–853.

    Article  CAS  Google Scholar 

  • Liang, X., Chen, L., Liu, Z., Jin, Y., He, M., Zhao, Z., Liu, C., Niyungeko, C., & Arai, Y. (2018). Composition of microbial community in pig manure biochar-amended soils and the linkage to the heavy metals accumulation in rice at harvest. Land Degradation & Development, 29, 2189–2198.

    Article  Google Scholar 

  • Lin, Y., Ye, Y., Hu, Y., & Shi, H. (2019). The variation in microbial community structure under different heavy metal contamination levels in paddy soils. Ecotoxicology and Environmental Safety, 180, 557–564.

    Article  CAS  Google Scholar 

  • Liu, B., Ai, S., Zhang, W., Huang, D., & Zhang, Y. (2017). Assessment of the bioavailability, bioaccessibility and transfer of heavy metals in the soil–grain–human systems near a mining and smelting area in N.W China. Science of the Total Environment, 609, 822–829.

    Article  CAS  Google Scholar 

  • Liu, J., Sui, Y., Yu, Z., Shi, Y., Chu, H., Jin, J., Liu, X., & Wang, G. (2014). High throughput sequencing analysis of biogeographical distribution of bacterial communities in the black soils of northeast China. Soil Biology and Biochemistry, 70, 113–122.

    Article  CAS  Google Scholar 

  • Lopez, S., Piutti, S., Vallance, J., Morel, J. L., Echevarria, G., & Benizri, E. (2017). Nickel drives the bacterial community diversity in the rhizosphere of the hyperaccumulator Alyssum murale. Soil Biology & Biochemistry, 114, 121–130.

    Article  CAS  Google Scholar 

  • Mani, D., & Kumar, C. (2014). Biotechnological advances in bioremediation of heavy metals contaminated ecosystems, an overview with special reference to phytoremediation. International Journal of Environmental Science and Technology, 11, 843–872.

    Article  CAS  Google Scholar 

  • Margesin, R., Plaza, G. A., & Kasenbacher, S. (2011). Characterization of bacterial communities at heavy-metal-contaminated sites. Chemosphere, 82(11), 1583–1588.

    Article  CAS  Google Scholar 

  • Mehrani, M. J., Sobotka, D., Kowal, P., Ciesielski, S., & Makinia, J. (2020). The occurrence and role of Nitrospira in nitrogen removal systems. Bioresource Technology, 303, 122936. https://doi.org/10.1016/j.biortech.2020.122936

    Article  CAS  Google Scholar 

  • Mudd, G. M., Jowitt, S. M., & Werner, T. T. (2017). The world’s lead–zinc mineral resources, scarcity, data, issues and opportunities. Ore Geology Reviews, 80, 1160–1190.

    Article  Google Scholar 

  • Nottingham, A. T., Fierer, N., Turner, B. L., Whitaker, J., Ostle, N. J., McNamara, N. P., Bardgett, R. D., Leff, J. W., Salinas, N., Silman, M. R., Kruuk, L. E. B., & Meir, P. (2018). Microbes follow Humboldt, temperature drives plant and soil microbial diversity patterns from the Amazon to the Andes. Ecology, 99, 2455–2466.

    Article  Google Scholar 

  • Oliveira, A., & Pampulha, M. E. (2006). Effects of long-term heavy metal contamination on soil microbial characteristics. Journal of Bioscience and Bioengineering, 102, 157–161.

    Article  CAS  Google Scholar 

  • Onireti, O. O., Lin, C., & Qin, J. (2017). Combined effects of low-molecular-weight organic acids on mobilization of arsenic and lead from multi-contaminated soils. Chemosphere, 170, 161–168.

    Article  CAS  Google Scholar 

  • Osman, J. R., Wang, Y., Jaubert, C., Nguyen, T. N., Fernandes, G. R., & DuBow, M. S. (2021). The bacterial communities of surface soils from desert sites in the eastern Utah (USA) portion of the Colorado Plateau. Microbiological Research, 244, 126664. https://doi.org/10.1016/J.MICRES.2020.126664

    Article  CAS  Google Scholar 

  • Pan, J., & Yu, L. (2011). Effects of Cd or/and Pb on soil enzyme activities and microbial community structure. Ecological Engineering, 37, 1889–1894.

    Article  Google Scholar 

  • Pereira, S. I, Lima, A. I, & Figueira, E. M. (2006). Screening possible mechanisms mediating cadmium resistance in Rhizobium leguminosarum bv. viciae isolated from contaminated Portuguese soils. Microbial Ecology, 52(2), 176-186

  • Reijonen, I., Metzler, M., & Hartikainen, H. (2016). Impact of soil pH and organic matter on the chemical bioavailability of vanadium species, the underlying basis for risk assessment. Environmental Pollution, 210, 371–379.

    Article  CAS  Google Scholar 

  • Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., Lesniewski, R. A., Oakley, B. B., Parks, D. H., Robinson, C. J., Sahl, J. W., Stres, B., Thallinger, G. G., Van Horn, D. J., & Weber, C. F. (2009). Introducing mother, open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75, 7537–7541.

    Article  CAS  Google Scholar 

  • Shi, W., Becker, J., Bischoff, M., Turco, R. F., & Konopka, A. E. (2002). Association of microbial community composition and activity with lead, chromium, and hydrocarbon contamination. Applied and Environmental Microbiology, 68, 3859–3866.

    Article  CAS  Google Scholar 

  • Šípková, A., Száková, J., & Tlustoš, P. (2013). Affinity of selected elements to individual fractions of soil organic matter. Water, Air and Soil Pollution, 225, 1–11.

    Google Scholar 

  • Song, W., Qi, R., Zhao, L., Xue, N., Wang, L., & Yang, Y. (2019). Bacterial community rather than metals shaping metal resistance genes in water, sediment and biofilm in lakes from arid Northwestern China. Environmental Pollution, 254, 113041. https://doi.org/10.1016/j.envpol.2019.113041

    Article  CAS  Google Scholar 

  • Strawn, D. G., & Sparks, D. L. (2000). Effects of soil organic matter on the kinetics and mechanisms of Pb (II) sorption and desorption in soil. Soil Science Society of America Journal, 64, 144–156.

    Article  CAS  Google Scholar 

  • Tilman, D., & Kareiva, P. (2018). Spatial ecology, the role of space in population dynamics and interspecific interactions (MPB–30). Princeton University Press.

    Google Scholar 

  • Tsiknia, M., Tzanakakis, V. A., Oikonomidis, D., Paranychianakis, N. V., & Nikolaidis, N. P. (2014). Effects of olive mill wastewater on soil carbon and nitrogen cycling. Applied Microbiology and Biotechnology, 98, 2739–2749.

    Article  CAS  Google Scholar 

  • Vig, K., Megharaj, M., Sethunathan, N., & Naidu, R. (2003). Bioavailability and toxicity of cadmium to microorganisms and their activities in soil, a review. Advances in Environmental Research, 8, 121–135.

    Article  CAS  Google Scholar 

  • Wang, F., Yao, J., Si, Y., Chen, H., Russel, M., Chen, K., Qian, Y., Zaray, G., & Bramanti, E. (2010). Short-time effect of heavy metals upon microbial community activity. Journal of Hazardous Materials., 173(1), 510–516.

    Article  CAS  Google Scholar 

  • Xu, S., Wang, B., Li, Y., Jiang, D., Zhou, Y., Ding, A., Zong, Y., Ling, X., Zhang, S., & Lu, H. (2020). Ubiquity, diversity, and activity of comammox Nitrospira in agricultural soils. Science of the Total Environment, 706, 135684. https://doi.org/10.1016/j.scitotenv.2019.135684

    Article  CAS  Google Scholar 

  • Zhang, C., Nie, S., Liang, J., Zeng, G., Wu, H., Hua, S., Liu, J., Yuan, Y., Xiao, H., Deng, L., & Xiang, H. (2016). Effects of heavy metals and soil physicochemical properties on wetland soil microbial biomass and bacterial community structure. Science of the Total Environment, 557–558, 785–790.

    Article  CAS  Google Scholar 

  • Zhang, R., Chen, L., Niu, Z., Song, S., & Zhao, Y. (2019). Water stress affects the frequency of Firmicutes, Clostridiales and Lysobacter in rhizosphere soils of greenhouse grape. Agricultural Water Management, 226, 105776. https://doi.org/10.1016/j.agwat.2019.105776

    Article  Google Scholar 

  • Zhang, X., Yang, L., Li, Y., Li, H., Wang, W., & Ye, B. (2012). Impacts of lead/zinc mining and smelting on the environment and human health in China. Environmental Monitoring and Assessment, 184, 2261–2273.

    Article  CAS  Google Scholar 

  • Zhao, X., Huang, J., Lu, J., & Sun, Y. (2019). Study on the influence of soil microbial community on the long-term heavy metal pollution of different land use types and depth layers in mine. Ecotoxicology and Environmental Safety, 170, 218–226.

    Article  CAS  Google Scholar 

  • Zhou, X. K., Li, W. C., Dong, W. C., & Zhou, B. (2020). A preliminary study of the characteristics of lead-zinc deposits in Shaanxi Province and their distribution laws. Northwest Geology, 3, 127–139.

    Google Scholar 

Download references

Acknowledgements

The authors are thankful to all the colleagues whose comments that have improved the quality of the manuscript.

Funding

This work was funded by the National Natural Science Foundation of China (grant numbers 31860176, 31700059, 41977204), Key Research and Development Program of Shaanxi (2020ZDLSF06-06), Key Research and Development Program of Gansu (20YF3FA037), Natural Science Basic Research Program of Shaanxi (2021JM-510, 2021JQ-791, 2021JQ-792), Science and Technology Program of Xi’an (20NYYF0013), XAWLKYTD012, YZJJ202102, YZJJ202110, and National Undergraduate Training Program for Innovation and Entrepreneurship (S202011080011).

Availability of Data and Materials.

The datasets used during the current study are available from the corresponding author upon reasonable request.

Code Availability.

Not applicable.

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Tianpeng Gao, Haijuan Li, Yueqing He, Yuanyuan Shen, Guangwen Li, Xiangkai Li, Yueli Chen, Yubing Liu, Changming Li, Jing Ji, Jing Xu, and Guohua Chang. The first draft of the manuscript was written by Tianpeng Gao and Haijuan Li, and all authors commented on previous versions of the manuscript. All authors have read and approved the final manuscript.

Corresponding author

Correspondence to Tianpeng Gao.

Ethics declarations

Ethics Approval

Not applicable.

Consent to Participate

Not applicable.

Consent for Publication

Not applicable.

Competing Interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Tianpeng Gao and Haijuan Li have contributed equally to this work and share first authorship.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 433 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gao, T., Li, H., He, Y. et al. The Variations of Bacterial Community Structures in Tailing Soils Suffering from Heavy Metal Contaminations. Water Air Soil Pollut 232, 392 (2021). https://doi.org/10.1007/s11270-021-05338-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11270-021-05338-2

Keywords

Navigation