Effects of Microplastics on the Intestinal Barrier, Gut Microbiota and Antibiotic Resistance Genes: A Mini-Review

Faezeh Jahedi; Behnam Ahmadi; Neamatollah Jaafarzadeh Haghighi Fard*; Pouria Abolfazli; Mahmood Maniati

**Faezeh Jahedi, Behnam Ahmadi, Neamatollah Jaafarzadeh Haghighi Fard*, Pouria Abolfazli and Mahmood Maniati**

Volume5-Issue8
Dates: Received: 2024-08-20 | Accepted: 2024-08-30 | Published: 2024-08-31
Pages: 1073-1080

Abstract

Microplastics (MPs) have aroused a global health concern and their coexistence with antibiotics is inevitable. However, how MPs would affect the bioaccumulation and risks of antibiotics in humans remains poorly understood. In this study, we reviewed several articles that examined the abundance and expression changes of ARGs in various environments. These changes were observed upon exposure to antibiotics such as tetracycline, sulfamethoxazole, and macrolides, as well as MPs, or a combination of both. To assess the impact of MPs on ARG abundance, we compiled data from various studies using tables of ARG abundances in tissues or environmental samples. By synthesizing this information, we aimed to identify which ARGs were upregulated or downregulated in response to micronanoplastics and antibiotics. Our findings provide insights into the potential risks posed by environmental pollutants and underscore the importance of understanding the dynamics of ARGs in response to MPs. We identified that shifts in gut microbiota contributed to the changes in ARG profiles. Combined, our results demonstrate that MPs reduced the bioaccumulation of tetracycline, sulfamethoxazole, and macrolides, but they enhanced its effects on gut microbiota and the antibiotic resistome indicating they might have high risks to humans.

FullText HTML FullText PDF DOI: 10.37871/jbres1992

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Jahedi F, Ahmadi B, Haghighi Fard NJ, Abolfazli P, Maniati M. Effects of Microplastics on the Intestinal Barrier, Gut Microbiota and Antibiotic Resistance Genes: A Mini-Review. J Biomed Res Environ Sci. 2024 Aug 31; 5(8): 1073-1080. doi: 10.37871/ jbres1992, Article ID: JBRES1992, Available at: https://www.jelsciences.com/articles/jbres1992.pdf

Subject area(s)

Microbiology

Biology

References

Zhao J, Lan R, Wang Z, Su W, Song D, Xue R, Liu Z, Liu X, Dai Y, Yue T, Xing B.Microplastic fragmentation by rotifers in aquatic ecosystems contributes to global nanoplastic pollution. Nature nanotechnology. 2024;19(3):406-414. doi: 10.1038/s41565-023-01534-9
Ben Stride, Abolfathi S, Bending GD, Pearson J. Quantifying microplastic dispersion due to density effects. J Hazard Mater. 2024 Mar 15;466:133440. doi: 10.1016/j.jhazmat.2024.133440. Epub 2024 Jan 6. PMID: 38246058.
Lee Y, Cho J, Sohn J, Kim C. Health Effects of Microplastic Exposures: Current Issues and Perspectives in South Korea. Yonsei Med J. 2023 May;64(5):301-308. doi: 10.3349/ymj.2023.0048. PMID: 37114632; PMCID: PMC10151227.
Sabatino R, Zullo R, Di Cesare A, Piscia R, Musazzi S, Corno G, Volta P, Galafassi S. Traditional and biodegradable plastics host distinct and potentially more hazardous microbes when compared to both natural materials and planktonic community. J Hazard Mater. 2024 Mar 5;465:133166. doi: 10.1016/j.jhazmat.2023.133166. Epub 2023 Dec 5. PMID: 38101010.
Han Z, Osman R, Liu Y, Wei Z, Wang L, Xu M. Analyzing the impacts of cadmium alone and in co-existence with polypropylene microplastics on wheat growth. Front Plant Sci. 2023 Aug 10;14:1240472. doi: 10.3389/fpls.2023.1240472. PMID: 37636097; PMCID: PMC10449543.
Zhang Z, Kang Y, Wang W, Xu L, Liu J, Zhang Z, Wu H. Low-density polyethylene microplastics and biochar interactively affect greenhouse gas emissions and microbial community structure and function in paddy soil. Chemosphere. 2023 Nov;340:139860. doi: 10.1016/j.chemosphere.2023.139860. Epub 2023 Aug 21. PMID: 37611773.
Tian, W, Song P, Zhang H, Duan X, Wei Y, Wang H, Wang S. Microplastic materials in the environment: Problem and strategical solutions. Progress in Materials Science. 2023;132:101035. doi: 10.1016/j.pmatsci.2022.101035.
Bostan N, Ilyas N, Akhtar N, Mehmood S, Saman RU, Sayyed RZ, Shatid AA, Alfaifi MY, Elbehairi SEI, Pandiaraj S. Toxicity assessment of microplastic (MPs); a threat to the ecosystem. Environ Res. 2023 Oct 1;234:116523. doi: 10.1016/j.envres.2023.116523. Epub 2023 Jul 7. PMID: 37422115.
Talukdar A, Kundu P, Bhattacharya S, Dutta N. Microplastic contamination in wastewater: Sources, distribution, detection and remediation through physical and chemical-biological methods. Sci Total Environ. 2024 Mar 15;916:170254. doi: 10.1016/j.scitotenv.2024.170254. Epub 2024 Jan 20. PMID: 38253100.
Jaafarzadeh Haghighi Fard N, Mohammadi MJ, Jahedi F. Effects of nano and microplastics on the reproduction system: In vitro and in vivo studies review. Food Chem Toxicol. 2023 Aug;178:113938. doi: 10.1016/j.fct.2023.113938. Epub 2023 Jul 8. PMID: 37429406.
Xu R, Cao JW, Lv HL, Geng Y, Guo MY. Polyethylene microplastics induced gut microbiota dysbiosis leading to liver injury via the TLR2/NF-κB/NLRP3 pathway in mice. Sci Total Environ. 2024 Mar 20;917:170518. doi: 10.1016/j.scitotenv.2024.170518. Epub 2024 Jan 28. PMID: 38286276.
Fard JH, Jahedi F, Dehdarirad H. The possibility of microplastic removal by earthworms and comparing with conventional chemical removal methods (A Global and Deeply Systematic Review). Journal of Polymers and the Environment. 2023;31(12):5050-5064.
Zhang W, Geng J, Sun M, Jiang C, Lin H, Chen H, Yang Y. Distinct species turnover patterns shaped the richness of antibiotic resistance genes on eight different microplastic polymers. Environmental Research. 2024;259:119562. doi: 10.1016/j.envres.2024.119562.
Perveen S, Pablos C, Reynolds K, Stanley S, Marugán J. Growth and prevalence of antibiotic-resistant bacteria in microplastic biofilm from wastewater treatment plant effluents. Science of the Total Environment. 2023;856:159024. doi: 10.1016/j.scitotenv.2022.159024.
Zheng Z, Huang Y, Liu L, Wang L, Tang J. Interaction between microplastic biofilm formation and antibiotics: Effect of microplastic biofilm and its driving mechanisms on antibiotic resistance gene. J Hazard Mater. 2023 Oct 5;459:132099. doi: 10.1016/j.jhazmat.2023.132099. Epub 2023 Jul 21. PMID: 37517232.
Li N, Zheng N, Pan J, An Q, Li X, Sun S, Chen C, Zhu H, Li Z, Ji Y. Distribution and major driving elements of antibiotic resistance genes in the soil-vegetable system under microplastic stress. Sci Total Environ. 2024 Jan 1;906:167619. doi: 10.1016/j.scitotenv.2023.167619. Epub 2023 Oct 6. PMID: 37806594.
de Souza Machado AA, Lau CW, Till J, Kloas W, Lehmann A, Becker R, Rillig MC. Impacts of Microplastics on the Soil Biophysical Environment. Environ Sci Technol. 2018 Sep 4;52(17):9656-9665. doi: 10.1021/acs.est.8b02212. Epub 2018 Aug 20. PMID: 30053368; PMCID: PMC6128618.
He D, Luo Y, Lu S, Liu M, Song Y, Lei L. Microplastics in soils: Analytical methods, pollution characteristics and ecological risks. TrAC Trends in Analytical Chemistry, 2018. 109: p. 163-172.
Chen H, Wang Y, Sun X, Peng Y, Xiao L. Mixing effect of polylactic acid microplastic and straw residue on soil property and ecological function. Chemosphere. 2020 Mar;243:125271. doi: 10.1016/j.chemosphere.2019.125271. Epub 2019 Nov 2. PMID: 31760289.
Huang Y, Zhao Y, Wang J, Zhang M, Jia W, Qin X. LDPE microplastic films alter microbial community composition and enzymatic activities in soil. Environ Pollut. 2019 Nov;254(Pt A):112983. doi: 10.1016/j.envpol.2019.112983. Epub 2019 Jul 30. PMID: 31394342.
Sun M, Ye M, Jiao W, Feng Y, Yu P, Liu M, Jiao J, He X, Liu K, Zhao Y, Wu J, Jiang X, Hu F. Changes in tetracycline partitioning and bacteria/phage-comediated ARGs in microplastic-contaminated greenhouse soil facilitated by sophorolipid. Journal of Hazardous Materials, 2018. 345: p. 131-139.
Liu J, Lv M, Sun A, Ding J, Wang Y, Chang X, Chen L. Exposure to microplastics reduces the bioaccumulation of sulfamethoxazole but enhances its effects on gut microbiota and the antibiotic resistome of mice. Chemosphere. 2022 May;294:133810. doi: 10.1016/j.chemosphere.2022.133810. Epub 2022 Jan 29. PMID: 35104539.
Gao B, Shi X, Li S, Xu W, Gao N, Shan J, Shen W. Size-dependent effects of polystyrene microplastics on gut metagenome and antibiotic resistance in C57BL/6 mice. Ecotoxicol Environ Saf. 2023 Apr 1;254:114737. doi: 10.1016/j.ecoenv.2023.114737. Epub 2023 Mar 10. PMID: 36950986.
Xu Z, Wu X, Zhang J, Cheng P, Xu Z, Sun W, Zhong Y, Wang Y, Yu G, Liu H. Microplastics existence intensified bloom of antibiotic resistance in livestock feces transformed by black soldier fly. Environ Pollut. 2023 Jan 15;317:120845. doi: 10.1016/j.envpol.2022.120845. Epub 2022 Dec 7. PMID: 36496063.
Chen X, Wang X, Huang Y, Zhu Z, Li T, Cai Z, Li M, Gong H, Yan M. Combined effects of microplastics and antibiotic-resistant bacteria on Daphnia magna growth and expression of functional genes. Science of the Total Environment. 2023;905:166880. doi: 10.1016/j.scitotenv.2023.166880.
Chan SY, Liu SY, Wu R, Wei W, Fang JK, Chua SL. Simultaneous Dissemination of Nanoplastics and Antibiotic Resistance by Nematode Couriers. Environ Sci Technol. 2023 Jun 13;57(23):8719-8727. doi: 10.1021/acs.est.2c07129. Epub 2023 Jun 2. PMID: 37267481.
Liu B, Yu D, Ge C, Luo X, Du L, Zhang X, Hui C. Combined effects of microplastics and chlortetracycline on the intestinal barrier, gut microbiota, and antibiotic resistome of Muscovy ducks (Cairina moschata). Sci Total Environ. 2023 Aug 20;887:164050. doi: 10.1016/j.scitotenv.2023.164050. Epub 2023 May 11. PMID: 37178843.
Zhang P, Lu G, Sun Y, Yan Z, Dang T, Liu J. Metagenomic analysis explores the interaction of aged microplastics and roxithromycin on gut microbiota and antibiotic resistance genes of Carassius auratus. J Hazard Mater. 2022 Mar 5;425:127773. doi: 10.1016/j.jhazmat.2021.127773. Epub 2021 Nov 15. PMID: 34802820.
Xu G, Yu Y. Polystyrene microplastics impact the occurrence of antibiotic resistance genes in earthworms by size-dependent toxic effects. J Hazard Mater. 2021 Aug 15;416:125847. doi: 10.1016/j.jhazmat.2021.125847. Epub 2021 Apr 20. PMID: 34492800.
Ma J, Sheng GD, Chen QL, O'Connor P. Do combined nanoscale polystyrene and tetracycline impact on the incidence of resistance genes and microbial community disturbance in Enchytraeus crypticus? J Hazard Mater. 2020 Apr 5;387:122012. doi: 10.1016/j.jhazmat.2019.122012. Epub 2020 Jan 3. PMID: 31927355.
McCallum G, Tropini C. The gut microbiota and its biogeography. Nat Rev Microbiol. 2024 Feb;22(2):105-118. doi: 10.1038/s41579-023-00969-0. Epub 2023 Sep 22. PMID: 37740073.
Xue YX, Huang LJ, Wang HY, Peng JJ, Jin MK, Hu SL, Li HB, Xue XM, Zhu YG. Interaction of tetracycline and copper co-intake in inducing antibiotic resistance genes and potential pathogens in mouse gut. Environ Int. 2024 Apr;186:108594. doi: 10.1016/j.envint.2024.108594. Epub 2024 Mar 21. PMID: 38527398.
Fu Y, Jia F, Su J, Xu X, Zhang Y, Li X, Jiang X, Schäffer A, Virta M, Tiedje JM, Wang F. Co-occurrence patterns of gut microbiome, antibiotic resistome and the perturbation of dietary uptake in captive giant pandas. J Hazard Mater. 2024 Jun 5;471:134252. doi: 10.1016/j.jhazmat.2024.134252. Epub 2024 Apr 12. PMID: 38657507.
Jensen O, Trujillo E, Hanson L, Ost KS. Controlling Candida: immune regulation of commensal fungi in the gut. Infect Immun. 2024 Apr 22:e0051623. doi: 10.1128/iai.00516-23. Epub ahead of print. PMID: 38647290.
Zhang J, Ma W, Li Y, Zhong D, Zhou Z, Ma J. The resistance change and stress response mechanisms of chlorine-resistant bacteria under microplastic stress in drinking water distribution system. Environ Pollut. 2024 Sep 1;356:124331. doi: 10.1016/j.envpol.2024.124331. Epub 2024 Jun 5. PMID: 38848962.
Li H, Lian Y, Li S, Yang M, Xie Q, Qiu L, Liu H, Long Y, Hu L, Fang C. The stress response of tetracycline resistance genes and bacterial communities under the existence of microplastics in typical leachate biological treatment system. J Environ Manage. 2024 Aug;366:121865. doi: 10.1016/j.jenvman.2024.121865. Epub 2024 Jul 16. PMID: 39018858.
Khare T, Mathur V, Kumar V. Agro-ecological Microplastics enriching the antibiotic resistance in aquatic environment. Current Opinion in Environmental Science & Health, 2024: p. 100534. doi: 10.1016/j.coesh.2024.100534.
Okaiyeto SA, Sutar PP, Chen C, Ni JB, Wang J, Mujumdar AS, Zhang JS, Xu MQ, Fang XM, Zhang C, Xiao HW. Antibiotic resistant bacteria in food systems: Current status, resistance mechanisms, and mitigation strategies. Agriculture Communications. 2024;100027. doi: 10.1016/j.agrcom.2024.100027.
Wei L, Su Z, Yue Q, Huang X, Wei M, Wang J. Microplastics, heavy metals, antibiotics, and antibiotic resistance genes in recirculating aquaculture systems. TrAC Trends in Analytical Chemistry. 2024;117564. doi: 10.1016/j.trac.2024.117564.
Gao B, Shi X, Li S, Xu W, Gao N, Shan J, Shen W. Size-dependent effects of polystyrene microplastics on gut metagenome and antibiotic resistance in C57BL/6 mice. Ecotoxicol Environ Saf. 2023 Apr 1;254:114737. doi: 10.1016/j.ecoenv.2023.114737. Epub 2023 Mar 10. PMID: 36950986.
Zhang Z, Chen W, Chan H, Peng J, Zhu P, Li J, Jiang X, Zhang Z, Wang Y, Tan Z, Peng Y, Zhang S, Lin K, Yung KK. Polystyrene microplastics induce size-dependent multi-organ damage in mice: Insights into gut microbiota and fecal metabolites. J Hazard Mater. 2024 Jan 5;461:132503. doi: 10.1016/j.jhazmat.2023.132503. Epub 2023 Sep 6. PMID: 37717443.
Xiao S, Zhang Y, Wu Y, Li J, Dai W, Pang K, Liu Y, Wu R. Bacterial community succession and the enrichment of antibiotic resistance genes on microplastics in an oyster farm. Mar Pollut Bull. 2023 Sep;194(Pt A):115402. doi: 10.1016/j.marpolbul.2023.115402. Epub 2023 Aug 21. PMID: 37611336.
Csongradi C, du Plessis J, Aucamp ME, Gerber M. Topical delivery of roxithromycin solid-state forms entrapped in vesicles. Eur J Pharm Biopharm. 2017 May;114:96-107. doi: 10.1016/j.ejpb.2017.01.006. Epub 2017 Jan 22. PMID: 28119103.
Zhang C, Li X, Liu L, Gao L, Ou S, Luo J, Peng X. Roxithromycin regulates intestinal microbiota and alters colonic epithelial gene expression. Appl Microbiol Biotechnol. 2018 Nov;102(21):9303-9316. doi: 10.1007/s00253-018-9257-1. Epub 2018 Aug 2. PMID: 30073395.
Jiang X, Wang X, Kah M, Li M. Environmentally relevant concentrations of microplastics from agricultural mulch and cadmium negatively impact earthworms by triggering neurotoxicity and disrupting homeostasis. J Hazard Mater. 2024 Sep 5;476:135158. doi: 10.1016/j.jhazmat.2024.135158. Epub 2024 Jul 10. PMID: 39002475.
Liu B, Yu D, Ge C, Luo X, Du L, Zhang X, Hui C. Combined effects of microplastics and chlortetracycline on the intestinal barrier, gut microbiota, and antibiotic resistome of Muscovy ducks (Cairina moschata). Sci Total Environ. 2023 Aug 20;887:164050. doi: 10.1016/j.scitotenv.2023.164050. Epub 2023 May 11. PMID: 37178843.