Abstract
Potentially toxic elements (Pb and Cd) contamination of soil can adversely affect human health. Moreover, these metal ions interact with the gut microbiota after entering the human digestive system. Based on the physiologically based extraction test and the simulator of human intestinal microbial ecosystem, the bioaccessibility of Pb and Cd in soils contaminated with lead-acid power plants was assessed. The gastric stage exhibited the greatest average bioaccessibility of lead and cadmium (63.39% and 57.22%), followed by the small intestinal stage (6.86% and 36.29%); due to gut microorganisms, the bioaccessibility of lead and cadmium was further reduced in the colon stage (1.86% and 4.22%). Furthermore, to investigate soil contamination’s effects on gut microbes, 16S rRNA high-throughput sequencing was used to identify the gut microbial species after the colon period. Due to Pb and Cd exposure, the relative abundance of Firmicutes and unidentified_Bacteria decreased, while the relative abundance of Proteobacteria, Synergistota, and Bacteroidota increased. The relationship between environmental factors and the number of microbial species in the gut was also examined using Spearman correlation analysis. Pb and Cd exposure has been found to affect the composition and structure of the gut microbiota.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Arun, K. B., Madhavan, A., Sindhu, R., Emmanual, S., Binod, P., Pugazhendhi, A., Sirohi, R., Reshmy, R., Awasthi, M. K., Gnansounou, E., & Pandey, A. (2021). Probiotics and gut microbiome—Prospects and challenges in remediating heavy metal toxicity. Journal of Hazardous Materials, 420, 126676. https://doi.org/10.1016/j.jhazmat.2021.126676
Baurhoo, B., Letellier, A., Zhao, X., & Ruiz-Feria, C. A. (2007). Cecal populations of lactobacilli and bifidobacteria and Escherichia coli populations after in vivo Escherichia coli challenge in birds fed diets with purified lignin or mannanoligosaccharides. Poultry Science, 86, 2509–2516. https://doi.org/10.3382/ps.2007-00136
Bokulich, N. A., Subramanian, S., Faith, J. J., Gevers, D., Gordon, J. I., Knight, R., Mills, D. A., & Caporaso, J. G. (2013). Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nature Methods, 10, 57-U11. https://doi.org/10.1038/nmeth.2276
Bolan, S., Seshadri, B., Grainge, I., Talley, N. J., & Naidu, R. (2021a). Gut microbes modulate bioaccessibility of lead in soil. Chemosphere, 270, 8. https://doi.org/10.1016/j.chemosphere.2020.128657
Bolan, S., Seshadri, B., Keely, S., Kunhikrishnan, A., Bruce, J., Grainge, I., Talley, N. J., & Naidu, R. (2021b). Bioavailability of arsenic, cadmium, lead and mercury as measured by intestinal permeability. Science and Reports, 11, 14675. https://doi.org/10.1038/s41598-021-94174-9
Chang, X., Li, H., Feng, J., Chen, Y., Nie, G., & Zhang, J. (2019). Effects of cadmium exposure on the composition and diversity of the intestinal microbial community of common carp (Cyprinus carpio L.). Ecotoxicology and Environmental Safety, 171, 92–98. https://doi.org/10.1016/j.ecoenv.2018.12.066
Chen, J. S., Gaikwad, V., Holmes, M., Murray, B., Povey, M., Wang, Y., & Zhang, Y. (2011). Development of a simple model device for in vitro gastric digestion investigation. Food & Function, 2, 174–182. https://doi.org/10.1039/c0fo00159g
Chen, L. G., Xu, Z. C., Liu, M., Huang, Y. M., Fan, R. F., Su, Y. H., Hu, G. C., Peng, X. W., & Peng, X. C. (2012). Lead exposure assessment from study near a lead-acid battery factory in China. Science of the Total Environment, 429, 191–198. https://doi.org/10.1016/j.scitotenv.2012.04.015
Curry, K. D., Wang, Q., Nute, M. G., Tyshaieva, A., Reeves, E., Soriano, S., Wu, Q. L., Graeber, E., Finzer, P., Mendling, W., Savidge, T., Villapol, S., Dilthey, A., & Treangen, T. J. (2022). Emu: species-level microbial community profiling of full-length 16S rRNA Oxford Nanopore sequencing data. Nature Methods, 19, 845. https://doi.org/10.1038/s41592-022-01520-4
Dong, Z. M., Yan, K. H., Liu, Y. J., Naidu, R., Duan, L. C., Wijayawardena, A., Semple, K. T., & Rahman, M. M. (2016). A meta-analysis to correlate lead bioavailability and bioaccessibility and predict lead bioavailability. Environment International, 92–93, 139–145. https://doi.org/10.1016/j.envint.2016.04.009
Duruibe, J. O., Ogwuegbu, M. O. C., & Egwurugwu, J. N. (2007). Heavy metal pollution and human biotoxic effects. International Journal of the Physical Sciences, 2, 112–118.
Etcheverry, P., Grusak, M. A., & Fleige, L. E. (2012). Application of in vitro bioaccessibility and bioavailability methods for calcium, carotenoids, folate, iron, magnesium polyphenols, zinc, and vitamins B-6, B-12, D, and E. Frontiers in Physiology. https://doi.org/10.3389/fphys.2012.00317
Gao, B., Chi, L., Mahbub, R., Bian, X., Tu, P., Ru, H., & Lu, K. (2017). Multi-omits reveals that lead exposure disturbs gut microbiome development, key metabolites, and metabolic pathways. Chemical Research in Toxicology, 30, 996–1005. https://doi.org/10.1021/acs.chemrestox.6b00401
Grond, K., Sandercock, B. K., Jumpponen, A., & Zeglin, L. H. (2018). The avian gut microbiota: Community, physiology and function in wild birds. Journal of Avian Biology, 49, 19. https://doi.org/10.1111/jav.01788
Haas, B. J., Gevers, D., Earl, A. M., Feldgarden, M., Ward, D. V., Giannoukos, G., Ciulla, D., Tabbaa, D., Highlander, S. K., Sodergren, E., Methe, B., DeSantis, T. Z., Petrosino, J. F., Knight, R., Birren, B. W., & Human Microbiome, C. (2011). Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Research, 21, 494–504. https://doi.org/10.1101/gr.112730.110
He, X., Qi, Z., Hou, H., Gao, J., & Zhang, X.-X. (2020). Effects of chronic cadmium exposure at food limitation-relevant levels on energy metabolism in mice. Journal of Hazardous Materials. https://doi.org/10.1016/j.jhazmat.2019.121791
Ikegami, M., Yoneda, M., Tsuji, T., Bannai, O., & Morisawa, S. (2014). Effect of particle size on risk assessment of direct soil ingestion and metals adhered to children’s hands at playgrounds. Risk Analysis, 34, 1677–1687. https://doi.org/10.1111/risa.12215
Juhasz, A. L., Weber, J., & Smith, E. (2011). Impact of soil particle size and bioaccessibility on children and adult lead exposure in peri-urban contaminated soils. Journal of Hazardous Materials, 186, 1870–1879. https://doi.org/10.1016/j.jhazmat.2010.12.095
Juhasz, A. L., Weber, J., Smith, E., Naidu, R., Marschner, B., Rees, M., Rofe, A., Kuchel, T., & Sansom, L. (2009). Evaluation of SBRC-gastric and SBRC-intestinal methods for the prediction of in vivo relative lead bioavailability in contaminated soils. Environmental Science and Technology, 43, 4503–4509. https://doi.org/10.1021/es803238u
Karin, L., Selinus, O., Otabbong, E., & Berglund, M. (2006). Metal and arsenic distribution in soil particle sizes relevant to soil ingestion by children. Applied Geochemistry. https://doi.org/10.1016/j.apgeochem.2006.05.005
Khan, M. F., & Wang, H. (2019). Environmental exposures and autoimmune diseases: Contribution of gut microbiome. Frontiers in Immunology, 10, 3094. https://doi.org/10.3389/fimmu.2019.03094
Li, H. B., Cui, X. Y., Li, K., Li, J., Juhasz, A. L., & Ma, L. Q. (2014). Assessment of in vitro lead bioaccessibility in house dust and Its relationship to in vivo lead relative bioavailability. Environmental Science and Technology, 48, 8548–8555. https://doi.org/10.1021/es501899j
Li, H. B., Li, M. Y., Zhao, D., Li, J., Li, S. W., Xiang, P., Juhsaz, A. L., & Ma, L. N. Q. (2020). Arsenic, lead, and cadmium bioaccessibility in contaminated soils: Measurements and validations. Critical Reviews in Environment Science and Technology, 50, 1303–1338. https://doi.org/10.1080/10643389.2019.1656512
Liu, B. L., Ai, S. W., Zhang, W. Y., Huang, D. J., & Zhang, Y. M. (2017). Assessment of the bioavailability, bioaccessibility and transfer of heavy metals in the soil-grain-human systems near a mining and smelting area in NW China. Science of the Total Environment, 609, 822–829. https://doi.org/10.1016/j.scitotenv.2017.07.215
Liu, J., Pang, J. J., Tu, Z. C., Wang, H., Sha, X. M., Shao, Y. H., & Liu, G. X. (2019). The accumulation, histopathology, and intestinal microorganism effects of waterborne cadmium on Carassius auratus gibelio. Fish Physiology and Biochemistry, 45, 231–243. https://doi.org/10.1007/s10695-018-0557-2
Liu, W., Feng, H., Zheng, S., Xu, S., Massey, I. Y., Zhang, C., Wang, X., & Yang, F. (2021). Pb toxicity on gut physiology and microbiota. Frontiers in Physiology. https://doi.org/10.3389/fphys.2021.574913
Liu, X., Zhang, J., Si, J., Li, P., Gao, H., Li, W., & Chen, Y. (2023). What happens to gut microorganisms and potential repair mechanisms when meet heavy metal(loid)s. Environmental Pollution (barking, Essex: 1987), 317, 120780–120780. https://doi.org/10.1016/j.envpol.2022.120780
Madrid, F., Biasioli, M., & Ajmone-Marsan, F. (2008). Availability and bioaccessibility of metals in fine particles of some urban soils. Archives of Environmental Contamination and Toxicology, 55, 21–32. https://doi.org/10.1007/s00244-007-9086-1
Mago, T., & Salzberg, S. L. (2011). FLASH: Fast length adjustment of short reads to improve genome assemblies. Bioinformatics, 27, 2957–2963. https://doi.org/10.1093/bioinformatics/btr507.
Molly, K., Woestyne, M. V., & Verstraete, W. (1993). Development of a S-step multi-chamber reactor as a simulation of the human intestinal microbial ecosystem. Applied Microbiology and Biotechnology, 39, 254–258. https://doi.org/10.1007/BF00228615
Navarro, M. C., Perez-Sirvent, C., Martinez-Sanchez, M. J., Vidal, J., & Marimon, J. (2006). Lead, cadmium and arsenic bloavallability in the abandoned mine site of Cabezo Rajao (Murcia, SE Spain). Chemosphere, 63, 484–489. https://doi.org/10.1016/j.chemosphere.2005.08.017
Ng, J. C., Juhasz, A., Smith, E., & Naidu, R. (2015). Assessing the bioavailability and bioaccessibility of metals and metalloids. Environmental Science and Pollution Research, 22, 8802–8825. https://doi.org/10.1007/s11356-013-1820-9
Pang, X., Dai, J., Chen, L., Liu, H., Yu, C., Han, L., Ren, T., Hu, X., Wang, H., Wang, Z., Zhao, X., Zeng, X., Ren, W., & Wang, C. (2019). Soil geochemical background value of 17 cites in Shandong Province. Shandong Land and Resources, 35, 46–56.
Rognes, T., Flouri, T., Nichols, B., Quince, C., & Mahé, F. (2016). VSEARCH: A versatile open source tool for metagenomics. PeerJ Inc. https://doi.org/10.7717/peerj.2584
Roussel, H., Waterlot, C., Pelfrene, A., Pruvot, C., Mazzuca, M., & Douay, F. (2010). Cd, Pb and Zn oral bioaccessibility of urban soils contaminated in the past by atmospheric emissions from two lead and zinc smelters. Archives of Environmental Contamination and Toxicology, 58, 945–954. https://doi.org/10.1007/s00244-009-9425-5
Rubin, S., Alava, P., Zekker, I., Du Laing, G., & Van de Wiele, T. (2014). Arsenic thiolation and the role of sulfate-reducing bacteria from the human intestinal tract. Environmental Health Perspectives, 122, 817–822. https://doi.org/10.1289/ehp.1307759
Ruby, M. V., Davis, A., Schoof, R., Eberle, S., & Sellstone, C. M. (1996). Estimation of lead and arsenic bioavailability using a physiologically based extraction test. Environmental Science and Technology, 30, 422–430.
Ruby, M. V., & Lowney, Y. W. (2012). Selective soil particle adherence to hands: Implications for understanding oral exposure to soil contaminants. Environmental Science and Technology, 46, 12759–12771. https://doi.org/10.1021/es302473q
Ruby, M. V., Schoof, R., Brattin, W., Goldade, M., Post, G., Harnois, M., Mosby, D. E., Casteel, S. W., Berti, W., & Carpenter, M. (1999). Advances in evaluating the oral bioavailability of inorganics in soil for use in human health risk assessment. Environmental Science and Technology, 33, 3697–3705.
Satya, P., Laetitia, R., Michael, C. C., Catherine, T. D., Catherine, T. D., & Coussa-Charley & Rodes. (2011). Gut microbiota: next frontier in understanding human health and development of biotherapeutics. Biologics: Targets Therapy, 5, 71.
Tremaroli, V., & Backhed, F. (2012). Functional interactions between the gut microbiota and host metabolism. Nature, 489, 242–249. https://doi.org/10.1038/nature11552
Van den Abbeele, P., Grootaert, C., Marzorati, M., Possemiers, S., Verstraete, W., Gerard, P., Rabot, S., Bruneau, A., El Aidy, S., Derrien, M., Zoetendal, E., Kleerebezem, M., Smidt, H., & Van de Wiele, T. (2010). Microbial community development in a dynamic gut model is reproducible, colon region specific, and selective for Bacteroidetes and Clostridium cluster IX. Applied and Environment Microbiology, 76, 5237–5246. https://doi.org/10.1128/AEM.00759-10
Wang, L., Yin, X., Gao, S., Jiang, T., & Ma, C. (2020a). In vitro oral bioaccessibility investigation and human health risk assessment of heavy metals in wheat grains grown near the mines in North China. Chemosphere, 252, 126522. https://doi.org/10.1016/j.chemosphere.2020.126522
Wang, L. H., Yin, X. X., Gao, S. L., Jiang, T. L., & Ma, C. X. (2020b). In vitro oral bioaccessibility investigation and human health risk assessment of heavy metals in wheat grains grown near the mines in North China. Chemosphere, 252, 6. https://doi.org/10.1016/j.chemosphere.2020.126522
Wang, P., Yin, N., Cai, X., Du, H., Fu, Y., Geng, Z., Sultana, S., Sun, G., & Cui, Y. (2021). Assessment of arsenic distribution, bioaccessibility and speciation in rice utilizing continuous extraction and in vitro digestion. Food Chemistry, 346, 128969. https://doi.org/10.1016/j.foodchem.2020.128969
Wiele, T. V. D., Boon, N., Possemiers, S., Jacobs, H., & Verstraete, W. (2004). Prebiotic effects of chicory inulin in the simulator of the human intestinal microbial ecosystem. FEMS Microbiology Ecology, 51(1), 143–153.
Wragg, J., Cave, M., Basta, N., Brandon, E., Casteel, S., Denys, S., Gron, C., Oomen, A., Reimer, K., Tack, K., & Van de Wiele, T. (2011). An inter-laboratory trial of the unified BARGE bioaccessibility method for arsenic, cadmium and lead in soil. Science of the Total Environment, 409, 4016–4030. https://doi.org/10.1016/j.scitotenv.2011.05.019
Xia, J. Z., Lu, L., Jin, C. Y., Wang, S. Y., Zhou, J. C., Ni, Y. C., Fu, Z. W., & Jin, Y. X. (2018). Effects of short term lead exposure on gut microbiota and hepatic metabolism in adult zebrafish. Comparative Biochemistry and Physiology Part c: Toxicology & Pharmacology, 209, 1–8. https://doi.org/10.1016/j.cbpc.2018.03.007
Xie, K., Xie, N., Liao, Z., Luo, X., Peng, W., & Yuan, Y. (2022). Bioaccessibility of arsenic, lead, and cadmium in contaminated mining/smelting soils: Assessment, modeling, and application for soil environment criteria derivation. Journal of Hazardous Materials, 443, 130321. https://doi.org/10.1016/j.jhazmat.2022.130321
Ya, J., Ju, Z., Wang, H., & Zhao, H. (2019a). Exposure to cadmium induced gut histopathological damages and microbiota alterations of Chinese toad (Bufo gargarizans) larvae. Ecotoxicology and Environmental Safety, 180, 449–456. https://doi.org/10.1016/j.ecoenv.2019.05.038
Yadav, M., Pandey, R., & Chauhan, N. S. (2020). Catabolic machinery of the human gut microbes bestow resilience against vanillin antimicrobial nature. Frontiers in Microbiology, 11, 588545. https://doi.org/10.3389/fmicb.2020.588545
Yan, K., Dong, Z., Wijayawardena, M. A. A., Liu, Y., Li, Y., & Naidu, R. (2019). The source of lead determines the relationship between soil properties and lead bioaccessibility. Environmental Pollution, 246, 53–59. https://doi.org/10.1016/j.envpol.2018.11.104
Yang, K., & Cattle, S. R. (2015). Bioaccessibility of lead in urban soil of Broken Hill, Australia: A study based on in vitro digestion and the IEUBK model. Science of the Total Environment, 538, 922–933. https://doi.org/10.1016/j.scitotenv.2015.08.084
Yin, N. Y., Du, H. L., Wang, P. F., Cai, X. L., Chen, P., Sun, G. X., & Cui, Y. S. (2017). Interindividual variability of soil arsenic metabolism by human gut microbiota using SHIME model. Chemosphere, 184, 460–466. https://doi.org/10.1016/j.chemosphere.2017.06.018
Yin, N., Du, H., Zhang, Z., Cai, X., Li, Z., Sun, G., & Cui, Y. (2016). Variability of arsenic bioaccessibility and metabolism in soils by human gut microbiota using different in vitro methods combined with SHIME. Science of the Total Environment, 566–567, 1670–1677. https://doi.org/10.1016/j.scitotenv.2016.06.071
Yin, N. Y., Zhang, Z. N., Cai, X. L., Du, H. L., Sun, G. X., & Cui, Y. S. (2015). In vitro method to assess soil arsenic metabolism by human gut microbiota: arsenic speciation and distribution. Environmental Science and Technology, 49, 10675–10681. https://doi.org/10.1021/acs.est.5b03046
Yin, N. Y., Zhao, Y. L., Wang, P. F., Du, H. L., Yang, M., Han, Z. L., Chen, X. C., Sun, G. X., & Cui, Y. S. (2021). Effect of gut microbiota on in vitro bioaccessibility of heavy metals and human health risk assessment from ingestion of contaminated soils*. Environmental Pollution, 279, 9. https://doi.org/10.1016/j.envpol.2021.116943
Zong, Y. T., Xiao, Q., & Lu, S. G. (2016). Distribution, bioavailability, and leachability of heavy metals in soil particle size fractions of urban soils (northeastern China). Environmental Science and Pollution Research, 23, 14600–14607. https://doi.org/10.1007/s11356-016-6652-y
Funding
This study was financially supported by the National Natural Science Foundation of China (41671485), Research Leader Studio Project for Jinan University (2021GXRC093) and Open Fund of Shandong Engineering Research Center for Environmental Protection and Remediation on Groundwater (801KF-2021-5, 801KF-2022-13).
Author information
Authors and Affiliations
Contributions
SXZ and ZWD involved in methodology, investigation, formal analysis, and writing—original draft; HKF, GMS, YYL, XYJ, and XW involved in investigation and data curation; XYY and LHW involved in conceptualization, funding acquisition, resources, supervision, and writing—review and editing.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zhang, S., Deng, Z., Yin, X. et al. Bioaccessibility of lead and cadmium in soils around typical lead-acid power plants and their effect on gut microorganisms. Environ Geochem Health 46, 107 (2024). https://doi.org/10.1007/s10653-023-01840-0
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10653-023-01840-0