Gut Microbiome Disruption by Pesticides: Converging Evidence Across Human and Animal Systems
DOI:
https://doi.org/10.53555/jaz.v43i1.5256Abstract
The gut microbiota, a complex ecosystem of bacteria, archaea, fungi, and viruses, plays a vital role in regulating metabolism, immunity, barrier integrity, and neuroendocrine signalling. Emerging evidence indicates that pesticides—chemical agents targeting essential biological pathways in pests—can inadvertently disrupt gut microbial communities across humans, animals, and environmental species. Many microbial taxa share enzymatic pathways with pesticide targets, such as the shikimate pathway inhibited by glyphosate, making them susceptible to compositional and functional disturbances. Experimental studies in rodents and insects have shown that pesticide exposure induces dysbiosis, depleting beneficial taxa, enriching xenobiotic-degrading microbes, and altering the production of key metabolites including short-chain fatty acids, bile acids, and aromatic amino acid derivatives. These microbial changes have been linked to systemic metabolic, immune, and neurobehavioral effects. In pollinators and other insects, microbiota-mediated pesticide degradation contributes to both detoxification and resistance, while dysbiosis reduces immunity and ecological stability. Although human data remain limited and primarily correlational, biomonitoring and dietary studies suggest that chronic exposure to common pesticides such as organophosphates, pyrethroids, and glyphosate-based herbicides may influence microbial diversity and function. Notably, gut microbes are not passive targets; they actively metabolize pesticides via hydrolytic, oxidative, and reductive reactions, producing metabolites with distinct toxicological profiles. This two-way interaction complicates traditional toxicokinetic models and positions the microbiome as both a mediator and modifier of pesticide effects. Integrating microbial endpoints into toxicological and regulatory frameworks is essential for understanding and mitigating the health and ecological impacts of pesticide exposure.
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1. Aktar, M. W., Sengupta, D., & Chowdhury, A. (2009). Impact of pesticides use in agriculture: Their benefits and hazards. Interdisciplinary Toxicology, 2(1), 1–12. https://doi.org/10.2478/v10102-009-0001-7
2. Badr, A. M., El-Demerdash, F. M., & Hassan, M. F. (2019). The role of oxidative stress and inflammatory responses in pesticide-induced toxicity. Toxicology Letters, 307, 42–50. https://doi.org/10.1016/ j.toxlet.2019.03.011
3. Bassil, K. L., Vakil, C., Sanborn, M., Cole, D. C., Kaur, J. S., & Kerr, K. J. (2007). Cancer health effects of pesticides: Systematic review. Canadian Family Physician, 53(10), 1704–1711. https://www.cfp.ca/content/53/10/1704
4. Carding, S., Verbeke, K., Vipond, D. T., Corfe, B. M., & Owen, L. J. (2015). Dysbiosis of the gut microbiota in disease. Microbial Ecology in Health and Disease, 26(1), 26191. https://doi.org/10.3402 /mehd.v26.26191
5. Cheng, D., et al. (2017). Characterization of insecticide metabolism by the gut microbiota of Spodoptera frugiperda. Insect Science, 24(3), 559–571. https://doi.org/10.1111/1744-7917.12343
6. Claus, S. P., Guillou, H., & Ellero-Simatos, S. (2016). The gut microbiota: A major player in the toxicity of environmental pollutants? npj Biofilms and Microbiomes, 2, 16003. https://doi.org/10.1038 /npjbiofilms.2016.3
7. Cox, L. M., Yamanishi, S., Sohn, J., Alekseyenko, A. V., Leung, J. M., Cho, I., Kim, S. G., Li, H., Gao, Z., Mahana, D., Zárate Rodriguez, J. G., Rogers, A. B., Robine, N., Loke, P., & Blaser, M. J. (2019). Alterations in intestinal microbiota of children exposed to environmental pesticides. Environmental Health Perspectives, 127(4), 47001. https://doi.org/10.1289/EHP4282
8. Damalas, C. A., & Eleftherohorinos, I. G. (2011). Pesticide exposure, safety issues, and risk assessment indicators. International Journal of Environmental Research and Public Health, 8(5), 1402–1419. https://doi.org/10.3390/ijerph8051402
9. De Almeida, L. G., Rosa, C., & De Souza, R. F. (2017). Microbial detoxification of insecticides in insect guts: Current status and future prospects. Journal of Invertebrate Pathology, 149, 82–91. https://doi.org/10.1016/j.jip.2017.07.005
10. Deising, H. B., Reimann, S., & Pascholati, S. F. (2020). Mechanisms and significance of fungicide resistance. Brazilian Journal of Microbiology, 51(3), 713–728. https://doi.org/10.1007/s42770-020-00258-7
11. Fung, T. C., Olson, C. A., & Hsiao, E. Y. (2017). Interactions between the microbiota, immune and nervous systems in health and disease. Nature Neuroscience, 20(2), 145–155. https://doi.org/10.1038/nn.4476
12. Gama, J. A., Henriques, I., & Domingues, I. (2021). Pesticide effects on the gut microbiome: Mechanisms, interactions, and implications for host health. Environmental Research, 200, 111312. https://doi.org/10.1016/j.envres.2021.111312
13. Gao, B., et al. (2017). Gut microbiota dysbiosis associated with hepatotoxicity of chlorpyrifos in mice. Chemosphere, 177, 262–268. https://doi.org/10.1016/j.chemosphere.2017.02.082
14. Huffnagle, G. B., & Noverr, M. C. (2013). The emerging world of the fungal microbiome. Trends in Microbiology, 21(7), 334–341. https://doi.org/10.1016/j.tim.2013.04.002
15. Jin, Y., Zeng, Z., Wu, Y., Zhang, S., & Fu, Z. (2017). Effects of environmental levels of pyrethroid insecticide exposure on the gut microbiota of zebrafish. Chemosphere, 182, 1–8. https://doi.org/10.1016/j.chemosphere.2017.05.018
16. Joly Condette, C., Bach, V., Mayeur, C., Gay-Quéheillard, J., & Khorsi-Cauet, H. (2015). Chlorpyrifos exposure during perinatal life affects intestinal microbiota, barrier function, and inflammatory status in adult rats. Environmental Toxicology and Pharmacology, 42, 17–27. https://doi.org/10.1016/ j.etap.2015.02.004
17. Kakumanu, M. L., Reeves, A. M., Anderson, T. D., Rodrigues, R. R., & Williams, M. A. (2016). Exposure to agricultural pesticides alters the gut microbiota composition and diversity of honey bees. Scientific Reports, 6, 32149. https://doi.org/10.1038/srep32149
18. Kers, J. G., Saccenti, E., Tytgat, H. L. P., Fasse, E., & Smidt, H. (2020). The intestinal microbiome of fish: Impacts of environmental pollutants and dietary factors. Reviews in Aquaculture, 12(3), 2221–2243. https://doi.org/10.1111/raq.12423
19. Kikuchi, Y., Hayatsu, M., Hosokawa, T., Nagayama, A., & Fukatsu, T. (2012). Symbiont-mediated insecticide resistance. Proceedings of the National Academy of Sciences, 109(22), 8618–8622. https://doi.org/10.1073/pnas.1200231109
20. Kim, K. H., Kabir, E., & Jahan, S. A. (2017). Exposure to pesticides and the associated human health effects. Science of the Total Environment, 575, 525–535. https://doi.org/10.1016/j.scitotenv.2016.09.009
21. Kohl, K. D., Cary, T. L., Karasov, W. H., & Dearing, M. D. (2016). Larval exposure to pesticides reduces gut microbial diversity in amphibians. Environmental Toxicology and Chemistry, 35(8), 2221–2229. https://doi.org/10.1002/etc.3371
22. Kumar, A., Thakur, I. S., & Srivastava, S. (2018). Biodegradation of organophosphate pesticides by microbial consortia: A review. Environmental Science and Pollution Research, 25(15), 14182–14204. https://doi.org/10.1007/s11356-018-1651-4
23. Li, H., Ma, L., Wu, J., Zhang, H., & Xu, C. (2018). Role of gut microbiota in pesticide degradation and resistance in insects: A review. Frontiers in Microbiology, 9, 2622. https://doi.org/10.3389 /fmicb.2018.02622
24. Li, Y., Su, J., Qiu, J., & Luo, T. (2019). Sublethal effects of imidacloprid on honeybee gut microbiota and immunity. Environmental Pollution, 254, 112980. https://doi.org/10.1016/j.envpol.2019.07.035
25. Li, Z., Wang, L., & Li, Q. (2019). Impacts of chlorpyrifos exposure on intestinal microbiota composition and metabolism in common carp. Aquatic Toxicology, 217, 105355. https://doi.org/10.1016 /j.aquatox.2019.105355
26. Liang, Y., Zhan, J., Liu, D., Luo, M., Han, J., Liu, X., ... & Zhu, L. (2020). Effects of glyphosate on gut microbiota of mice and its metabolic mechanisms. Environmental Pollution, 261, 114148. https://doi.org/10.1016/j.envpol.2020.114148
27. Lloyd-Price, J., Abu-Ali, G., & Huttenhower, C. (2016). The healthy human microbiome. Genome Medicine, 8, 51. https://doi.org/10.1186/s13073-016-0307-y
28. Lozano, V. L., Fotschki, B., Guérin, V., Olier, M., Chevalier, J., Sergent, T., ... & Gamet-Payrastre, L. (2018). Gut microbiota changes in rats following subchronic exposure to pesticide mixtures. Food and Chemical Toxicology, 112, 196–206. https://doi.org/10.1016/j.fct.2017.12.052
29. Lu, C., Barr, D. B., Pearson, M. A., Waller, L. A., & Bravo, R. (2018). Dietary intake and its contribution to pesticide exposure: A longitudinal study among children. Environmental Health Perspectives, 126(3), 037009. https://doi.org/10.1289/EHP1709
30. Mesnage, R., & Antoniou, M. N. (2020). Computational modelling provides insight into the effects of glyphosate on the shikimate pathway in the human gut microbiome. Current Microbiology, 77(9), 1545–1553. https://doi.org/10.1007/s00284-020-01904-3
31. Mesnage, R., Teixeira, M., Mandrioli, D., Falcioni, L., Ducarmon, Q. R., Zwittink, R. D., ... & Antoniou, M. N. (2021). Multiomics reveal non-alcoholic fatty liver disease in rats following chronic exposure to an ultra-low dose of Roundup herbicide. Environmental Health Perspectives, 129(1), 17005. https://doi.org/10.1289/EHP6990
32. Mesnage, R., Panzacchi, S., Bourne, E., Mein, C. A., Perry, M. J., Hu, J., Chen, J., Mandrioli, D., Belpoggi, F., & Antoniou, M. N. (2021). Glyphosate and its formulations alter bacterial and fungal community composition in the rat caecum microbiome. Frontiers in Microbiology, 12, 702. https://doi.org/10.3389/fmicb.2021.702
33. Mesnage, R., Teixeira, M., & Antoniou, M. N. (2021). Multi-omics investigation of glyphosate-based herbicide exposure in Sprague–Dawley rats reveals gut microbiome perturbations and metabolic pathway alterations. Environmental Health Perspectives, 129(1), 17005. https://doi.org/10.1289/EHP6990
34. Mostafalou, S., & Abdollahi, M. (2017). Pesticides and human chronic diseases: Evidences, mechanisms, and perspectives. Toxicology and Applied Pharmacology, 268(2), 157–177. https://doi.org/10.1016 /j.taap.2013.11.008
35. Motta, E. V. S., Raymann, K., & Moran, N. A. (2018). Glyphosate perturbs the gut microbiota of honey bees. Proceedings of the National Academy of Sciences, 115(41), 10305–10310. https://doi.org/10.1073 /pnas.1803880115
36. Motta, E. V. S., Raymann, K., & Moran, N. A. (2018). Glyphosate perturbs the gut microbiota of honey bees. Proceedings of the National Academy of Sciences, 115(41), 10305–10310. https://doi.org/10.1073/ pnas.1803880115
37. Mueller, N. T., Shapiro, A. L. B., Appel, L. J., & Martinez-Medina, M. (2017). Dietary patterns and the gut microbiota in humans. Current Opinion in Clinical Nutrition and Metabolic Care, 20(5), 401–407. https://doi.org/10.1097/MCO.0000000000000401
38. Nicholson, J. K., Holmes, E., Kinross, J., Burcelin, R., Gibson, G., Jia, W., & Pettersson, S. (2012). Host-gut microbiota metabolic interactions. Science, 336(6086), 1262–1267. https://doi.org/10.1126 /science.1223813
39. Oates, L., Cohen, M., Braun, L., Schembri, A., Taskova, R., & Clarke, J. (2014). Reduction in urinary organophosphate pesticide metabolites in adults after a week-long organic diet. Environmental Research, 132, 105–111. https://doi.org/10.1016/j.envres.2014.03.021
40. Raymann, K., & Moran, N. A. (2018). The role of the gut microbiome in health and disease of adult honey bee workers. Current Opinion in Insect Science, 26, 97–104. https://doi.org/10.1016/j.cois.2018.02.012.
41. Richard, M. L., & Sokol, H. (2019). The gut mycobiota: Insights into analysis, environmental interactions and role in gastrointestinal diseases. Nature Reviews Gastroenterology & Hepatology, 16(6), 331–345. https://doi.org/10.1038/s41575-019-0121-2
42. Rizzati, V., Briand, O., Guillou, H., & Gamet-Payrastre, L. (2016). Effects of pesticide mixtures in human and animal models: An update of the toxicological evidence. Toxicology, 357–358, 123–135. https://doi.org/10.1016/j.tox.2016.06.009
43. Rosas-Pérez, I., Banihani, Q., Hernández, E., Hernández, M., Rojas-Hernández, S., & Gutiérrez-Ruiz, M. C. (2017). The role of pesticides in the modulation of gut microbiota. Frontiers in Microbiology, 8, 2466. https://doi.org/10.3389/fmicb.2017.02466
44. Rowland, I., Gibson, G., Heinken, A., Scott, K., Swann, J., Thiele, I., & Tuohy, K. (2018). Gut microbiota functions: Metabolism of nutrients and other food components. European Journal of Nutrition, 57(1), 1–24. https://doi.org/10.1007/s00394-017-1445-8
45. Rueda-Ruzafa, L., Cruz, F., Roman, P., & Cardona, D. (2019). Gut microbiota and neurological effects of glyphosate. NeuroToxicology, 75, 1–8. https://doi.org/10.1016/j.neuro.2019.08.002
46. Sharon, G., Sampson, T. R., Geschwind, D. H., & Mazmanian, S. K. (2016). The central nervous system and the gut microbiome. Cell, 167(4), 915–932. https://doi.org/10.1016/j.cell.2016.10.027
47. Stana, A. M., Chiriac, D. V., & Avram, S. (2021). Effects of triazole fungicides on microbiota and immune system: Insights from experimental studies. Environmental Toxicology and Pharmacology, 85, 103656. https://doi.org/10.1016/j.etap.2021.103656
48. Sun, J., Jin, C., & Zhang, Y. (2019). Atrazine exposure alters microbial community and metabolic potential in aquatic sediments. Environmental Pollution, 248, 912–920. https://doi.org/10.1016/ j.envpol.2019.02.079
49. Thursby, E., & Juge, N. (2017). Introduction to the human gut microbiota. Biochemical Journal, 474(11), 1823–1836. https://doi.org/10.1042/BCJ20160510
50. Tu, P., Gao, B., Chi, L., Lai, Y., Bian, X., Ru, H., & Lu, K. (2019). Subchronic low-dose diazinon exposure triggers oxidative stress and alters the gut microbiome in mice. Toxicological Sciences, 171(2), 380–393. https://doi.org/10.1093/toxsci/kfz166
51. Tu, Y., Chen, Y., & Guo, Y. (2019). Occupational-dose exposure of mice to 2,4-D changed the Firmicutes-to-Bacteroidetes ratio to a dysbiotic one and affected the metabolism of urea, amino acids, and carbohydrates. Environmental Toxicology and Pharmacology, 67, 103417. https://doi.org/10.1016/ j.etap.2019.103417
52. Valdes, A. M., Walter, J., Segal, E., & Spector, T. D. (2018). Role of the gut microbiota in nutrition and health. BMJ, 361, k2179. https://doi.org/10.1136/bmj.k2179
53. Velmurugan, G., Ramprasath, T., Gilles, M., Swaminathan, K., & Ramasamy, S. (2017). Environmental pollutants and the gut microbiome: An emerging link in human health. Toxicology Letters, 279, 23–31. https://doi.org/10.1016/j.toxlet.2017.07.021
54. Wang, G., Li, C., & Zeng, Z. (2021). Pesticide exposure and gut microbiota: A new target for toxicology research. Environmental Pollution, 273, 116460. https://doi.org/10.1016/j.envpol.2021.116460
55. Xia, X., et al. (2018). Gut microbiota mediate insecticide resistance in the diamondback moth, Plutella xylostella. Frontiers in Microbiology, 9, 25. https://doi.org/10.3389/fmicb.2018.00025
56. Ye, M., Beach, J., Martin, J. W., & Senthilselvan, A. (2020). Urinary pesticide concentrations and dietary predictors in the general population: Results from the Canadian Health Measures Survey. Environmental Research, 186, 109478. https://doi.org/10.1016/j.envres.2020.109478
57. Zhang, J., Sun, W., Zhang, S., & Lu, C. (2018). Azole fungicide exposure disturbs intestinal microbial composition and lipid metabolism in zebrafish. Environmental Science and Pollution Research, 25(28), 28451–28460. https://doi.org/10.1007/s11356-018-2850-2
58. Zhang, J., Zhu, S., Zhang, X., Zhang, L., & Lu, C. (2020). Deltamethrin exposure alters gut microbiota and induces inflammatory responses in mice. Environmental Pollution, 265, 114519. https://doi.org/10.1016/j.envpol.2020.114519
59. Zhang, L., Nichols, R. G., Correll, J., Murray, I. A., Tanaka, N., Smith, P. B., ... & Patterson, A. D. (2019). Chronic exposure to chlorpyrifos induces obesity and insulin resistance via gut microbiota alteration in mice. Environmental Pollution, 248, 402–410. https://doi.org/10.1016/j.envpol.2019.02.066
60. Zhang, X., Zhao, Y., & Wang, Y. (2020). Urinary pyrethroid metabolites are associated with altered fecal short-chain fatty acids and gut microbiota composition in adolescents. Environmental International, 137, 105579. https://doi.org/10.1016/j.envint.2020.105579
61. Zhang, Y., Zhang, X., & Wang, H. (2017). Cypermethrin exposure affects gut microbial diversity and metabolic profiles in zebrafish. Environmental Pollution, 229, 418–428. https://doi.org/10.1016/ j.envpol.2017.06.102
62. Zhao, Y., Wang, W., Tang, N., Feng, S., & Wang, Y. (2021). Pesticide biodegradation mediated by gut microbiota in insects: Mechanisms and ecological implications. Journal of Hazardous Materials, 406, 124689. https://doi.org/10.1016/j.jhazmat.2020.124689
63. Zhu, Y. C., Parker, R., Luttrell, R., & Snodgrass, G. (2016). The influence of pesticides on soil microbial communities and pesticide degradation. Critical Reviews in Environmental Science and Technology, 46(13), 1179–1212. https://doi.org/10.1080/10643389.2016.1207981
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