Impact pattern of heavy metals on gut microbiota in the polluted city of Tehran
-
Seyed Mahmoud Barzi
,
Peyman Naderi
,
Fatemeh Haririzadeh Jouriani
,
Mahdi Torkamaneh
,
Seyed Davar Siadat
,
Farnaz Shamkani
,
Seifoddin Javadian
,
Mina Ebrahimi-Rad
,
Reza Saghiri
,
Seyed Ali Nojoumi
Abstract
Background and Objectives: This article focuses on the effects of six heavy metals on gut microbiota, which plays a key role in human health. Gut microbiota plays a key role in metabolism, immunity, and maintaining homeostasis. Heavy metals can affect microbiota composition and function, with health consequences. Consuming large amounts of heavy metals may have harmful impacts, including alteration in microbial composition and bacterial population changes.
Materials and Methods: Six heavy metals—cadmium, chromium (toxic metals), copper, zinc, iron, and selenium (beneficial trace elements)—were detected in peripheral blood, serum, or urine, while feces were used for 16S rRNA sequencing. Serum samples from 100 volunteers from Tehran (polluted area) and Firoozkooh (clean city) were collected. Subjects were analyzed for the presence of Escherichia coli, Bacteroides fragilis, Bifidobacterium longum, Lactobacillus acidophilus, Clostridium clostridioforme, Faecalibacterium prausnitzii and Akkermansia muciniphila to evaluate correlations between metals and microbial composition using biochemical, microbial, and molecular methods.
Results: Escherichia coli and Bifidobacterium longum levels in polluted areas were not significantly different from those in unpolluted areas. Bacteroides fragilis in polluted areas was significantly higher compared to non-polluted locations. Clostridium, Akkermansia, Faecalibacterium, and Lactobacillus acidophilus were significantly lower in polluted areas, amounting to less than half the levels in clean areas. Heavy metal concentrations showed no gender differences in either location.
Conclusion: Some heavy metals change intestinal microbiota composition and metabolic profiles, potentially resulting in metabolic diseases and environmental risks.
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2. Marvasti FE, Moshiri A, Taghavi MS, Riazi S, Taati M, Sadati SF, et al. The first report of differences in gut microbiota composition between obese and normal weight Iranian subjects. Iran Biomed J 2020;24:148-154.
3. Sushila S, Balda A, Balhara N, Aarushi A, Giri A. Literature review and health risks assessment of heavy metal contamination in human milk. Discov Miner 2024;1:2024.
4. Briffa J, Sinagra E, Blundell R. Heavy metal pollution in the environment and their toxicological effects on humans. Heliyon 2020;6(9):e04691.
5. Sweta G, Nukavarapu SP, Jala VR. Effects of heavy metals on gut barrier integrity and gut microbiota. Microbiota Host 2024;2(1):e230015.
6. Kunst C, Schmid S, Michalski M, Tümen D, Buttenschön J, Müller M, et al. The Influence of Gut Microbiota on Oxidative Stress and the Immune System. Biomedicines 2023;11:1388.
7. Oladimeji TE, Oyedemi M, Emetere ME, Agboola O, Adeoye JB, Odunlami OA. Review on the impact of heavy metals from industrial wastewater effluent and removal technologies. Heliyon 2024;10(23):e40370.
8. Rybka P, Klimczak E, Ostrycharz E, Rączka A, Wojciechowska-Koszko I, Dybus A, et al. Small Intestinal Bacterial Overgrowth (SIBO) and Twelve Groups of Related Diseases—Current State of Knowledge. Biomedicines 2024;12:1030.
9. Zinia H, Fatema K, Shoily S, Sajib AA. Disease-associated metabolic pathways affected by heavy metals and metalloid. Toxicol Rep 2023;10:554-570.
10. Mitra S, Chakraborty AJ, Tareq AB, Emran TB, Firzan Nainu F, Khusro A, et al. Impact of heavy metals on the environment and human health: Novel therapeutic insights to counter the toxicity. J King Saud Univ Sci 2022;34:101865.
11. Qinheng Z, Boyan C, Fu Z, Baodan Z, Yujie G, Mengtao P, et al. Toxic and essential metals: metabolic interactions with the gut microbiota and health implications. Front Nutr 2024;11:1448388.
12. Shalenie PD, Jan VB, Yvonne CMS, Janine E, et al. Occupational exposure to hexavalent chromium: Part II Hazard assessment of carcinogenic effects. Regul Toxicol Pharmacol 2021;126:105045.
13. Singh A, Kostova I. Health effects of heavy metal contaminants Vis-à-Vis microbial response in their bioremediation. Inorg Chim Acta 2024;568:122068.
14. Xiwei H, Zhaodong Q, Hui H, Ling Q, Jie G, Xu-Xiang Z. Structural and functional alterations of gut microbiome in mice induced by chronic cadmium exposure. Chemosphere 2020;246:125747.
15. Chen B, Yu P, Chan WN, Xie F, Zhang Y, Liang L, et al. Cellular zinc metabolism and zinc signaling: from biological functions to diseases and therapeutic targets. Signal Transduct Target Ther 2024;9:6.
16. Mary JD, Scott GD, Linda DB, Nagaraju I, Kyle B, Charlene D, et al. Effects of dietary zinc on the gut microbiome and resistome of the gestating cow and neonatal calf. Anim Microbiome 2024;6:39.
17. De Filippis F, Valentino V, Sequino G, Borriello G, Marita GR, Biancamaria P, et al. Exposure to environmental pollutants selects for xenobiotic-degrading functions in the human gut microbiome. Nat Commun 2024;15:4482.
18. Liu S, Yin J, Wan D, Yin Y. The Role of Iron in Intestinal Mucus: Perspectives from Both the Host and Gut Microbiota. Adv Nutr 2024;15:100307.
19. Knezevic J, Starchl C, Tamura BA, Amrein K. Thyroid-Gut-Axis: How does the microbiota influence thyroid function? Nutrients 2020;12:1769.
20. Yersin S, Vonaesch P. Small intestinal microbiota: from taxonomic composition to metabolism. Trends Microbiol 2024;32:970-983.
21. Hou K, Wu ZX, Chen XY, Wang JQ, Zhang D, Xiao C, et al. Microbiota in health and diseases. Signal Transduct Target Ther 2022;7:135.
22. Garavaglia B, Vallino L, Amoruso A, Pane M, Ferraresi A, Isidoro C. The role of gut microbiota, immune system, and autophagy in the pathogenesis of inflammatory bowel disease: Molecular mechanisms and therapeutic approaches. Aspect Mol Med 2024;4:100056.
23. Ma Z, Zuo T, Frey N, Rangrez AY. A systematic framework for understanding the microbiome in human health and disease: from basic principles to clinical translation. Signal Transduct Target Ther 2024;9:237.
24. Trueba G, Cardenas P, Romo G, Gutierrez B. Reevaluating human-microbiota symbiosis: Strain-level insights and evolutionary perspectives across animal species. BioSystems 2024;244:105283.
25. Naji SC. Cadmium induces migration of colon cancer cells: the roles of reactive oxygen species p38 and Cyclooxygenase-2. [Master's Thesis]. Beirut: American University of Beirut; 2018.
26. Yujie Y, Xia Z, Shufang Z, Shengchen W, Honggui L, Shiwen X. Subacute cadmium exposure promotes M1 macrophage polarization through oxidative stress-evoked inflammatory response and induces porcine adrenal fibrosis. Toxicology 2021;461:152899.
27. Hossein-Khannazer N, Azizi G, Eslami S, Mohammed HA, Fayyaz F, Hosseinzadeh R, et al. The effects of cadmium exposure in the induction of inflammation. Immunopharmacol Immunotoxicol 2020;42:1-8.
28. Mitra S, Chakraborty AJ, Tareq AB, Emran TB, Firzan NF, Khusro A, et al. Impact of heavy metals on the environment and human health: Novel therapeutic insights to counter the toxicity. J King Saud Univ Sci 2022;34:101865.
29. Xue L, Luo X, Jun-Hong X, Wang D, Dong-Xing Z. Isolation and pathogenicity evaluation of Escherichia coli O157:H7 from common carp Cyprinus carpio. Microb Pathog 2023;182:106250.
30. Tseng AS, Roberts MC, Weissman SJ, Rabinowitz PM. Study of heavy metal resistance genes in Escherichia coli isolates from a marine ecosystem with a history of environmental pollution (arsenic, cadmium, copper, and mercury). PLoS One 2023;18(11):e0294565.
31. Peng Z, Liao Y, Yang W, Liu L. Metal(loid)-gut microbiota interactions and microbiota-related protective strategies: A review. Environ Int 2024;192:109017.
32. Runqiu C, Huaijun T, Tingtao C. Potential Application of Living Microorganisms in the Detoxification of Heavy Metals. Foods 2022;11:1905.
33. Li F, Liu J, Maldonado-Gómez MX, Frese SA, Gänzle MG, Walter J. Highly accurate and sensitive absolute quantification of bacterial strains in human fecal samples. Microbiome 2024;12:68.
34. Xiaoyu M. Heavy metals remediation through lactic acid bacteria: Current status and future prospects. Sci Total Environ 2024;946:174455.
35. Chen J, Chen X, Ho CL. Recent Development of Probiotic Bifidobacteria for Treating Human Diseases. Front Bioeng Biotechnol 2021;9:770248.
36. Yinhua N, Zhang Y, Zheng L, Rong N, Yang Y, Gong P, et al. Bifidobacterium and Lactobacillus improve inflammatory bowel disease in zebrafish of different ages by regulating the intestinal mucosal barrier and microbiota. Life Sci 2023;324:121699.
37. Abdel-Megeed RM. A Promising Generation of Heavy Metal Detoxification. Biol Trace Elem Res 2021;199:2406-2413.
38. Shashi S, Sabine P, Morse SA. Special Issue: Gram-Positive Bacterial Toxins. Microorganisms 2023;11:2054.
39. Binish MB, Sruthy S, Mahesh M. Effect of Heavy Metals (Pb, Cd, Cu) on the Growth of Sulphate Reduction associated Bacterium Clostridium bifermentans Isolated from Cochin estuary, Southwest coast of India. Int J Mar Sci 2015;5:1-5.
40. Haghighizadeh A, Rajabi O, Nezarat A, Hajyani Z, Haghmohammadi M, Hedayatikhah S, et al. Comprehensive analysis of heavy metal soil contamination in mining Environments: Impacts, monitoring Techniques, and remediation strategies. Arab J Chem 2024;17:105777.
41. Karamzin AM, Ropot AV, Sergeyev OV, Khalturina EO. Akkermansia muciniphila and host interaction within the intestinal tract. Anaerobe 2021;72:102472.
42. Hasr Moradi Kargar S, Hadizadeh SN. Lactobacillus fermentum and Lactobacillus plantarum bioremediation ability assessment for copper and zinc. Arch Microbiol 2021;202:1957-1963.
43. Nagdeo K, Midya V, Lane JM, Torres-Olascoaga LA, Martínez GG, Horton MK, et al. Akkermansia muciniphila may mediate the association between prenatal metal mixture exposure and childhood depressive symptoms. Research Square 2023. doi: 10.21203/rs.3.rs-3342709/v1.
44. Vishal M, Kiran N, Jamil L, Libni TO, Gabriela M, Megan H, et al. Akkermansia muciniphila modifies the association between metal exposure during pregnancy and depressive symptoms in late childhood. Sci Total Environ 2024;916:170361.
45. Sophie V, Séverine L, Sandrine A, Catherine J, Céline H, Sawiya C, et al. Faecalibacterium duncaniae A2-165 regulates the expression of butyrate synthesis, ferrous iron uptake, and stress-response genes based on acetate consumption. Sci Rep 2024;14:987.
46. Iran's Department of Environment. Air Quality Monitoring System. [cited 2024]. Available from: https://aqms.doe.ir/
47. Adamczyk-Szabela D, Lisowska K, Romanowska-Duda Z, Wolf WM. Combined cadmium-zinc interactions alter manganese, lead, copper uptake by Melissa officinalis. Sci Rep 2020;10:1675.
48. Najafzade M, Mosapour A, Nahrevanian H, Zamani Z, Javadian S, Mirkhani F. Effect of trinitroglycerin therapy on serum zinc and copper levels and liver enzyme activities in BALB/c mice infected with Leishmania major MRHO/IR/75/ER. Iran J Basic Med Sci 2015;18:277-283.
49. Xiaoyun S, Yongkuan C, Kangning X. The effect of heavy metal contamination on humans and animals in the vicinity of a zinc smelting facility. PLoS One 2019;14(10):e0207423.
50. Nadkarni MA, Martin FE, Jacques NA, Hunter N. Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology 2002;148:257-266.
51. Ghosh S, Nukavarapu SP, Venkatakrishna RJ. Effects of heavy metals on gut barrier integrity and gut microbiota. Microbiota Host 2024;2:1.
52. Shao M, Zhu Y. Long-term metal exposure changes gut microbiota of residents surrounding a mining and smelting area. Sci Rep 2020;10:4453.
53. Singh S, Sharma P, Pal N, Kumawat M, Shubham S, Sarma DK, et al. Impact of Environmental Pollutants on Gut Microbiome and Mental Health via the Gut-Brain Axis. Microorganisms 2022;10:1457.
54. Behrouzi A, Nafari AM, Siadat SD. The Significance of Microbiome in Personalized Medicine. Clin Transl Med 2019;8:16.
55. Sheng Z, Shen Y, Wang S, Zhaocun L, Rui S, Fei J, et al. Responses of the gut microbiota to environmental heavy metal pollution in tree sparrow (Passer montanus) Nestlings. Ecotoxicol Environ Saf 2023;264:115480.
56. Anka AU, B-Usman A, Azizi G. Potential mechanisms of some selected heavy metals in the induction of inflammation and autoimmunity. Eur J Inflamm 2022;20:1721727X221122719.
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| Files | ||
| Issue | Vol 18 No 2 (2026) | |
| Section | Original Article(s) | |
| Keywords | ||
| Gastrointestinal microbiome Heavy metals Environmental pollution Bacteria Iran | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Barzi SM, Naderi P, Haririzadeh Jouriani F, Torkamaneh M, Siadat SD, Shamkani F, Javadian S, Ebrahimi-Rad M, Saghiri R, Nojoumi SA. Impact pattern of heavy metals on gut microbiota in the polluted city of Tehran. Iran J Microbiol. 2026;18(2):204-216.
