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Fluoride-Induced Alteration in the Diversity and Composition of Bacterial Microbiota in Mice Colon

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Abstract

Fluoride, as an environmental toxin, causes damage to intestinal mucosa. It may promote pathogen infection by increasing the intestinal mucosa permeability. In this study, the colonic fecal samples from the control group (C group, 0 mg/L NaF for 60 days) and the fluoride group (F group, 100 mg/L NaF for 60 days) were subjected to high-throughput 16S rRNA sequencing to verify the effects of fluoride on the colonic flora of animals. Results revealed a total of 253 operative taxonomical units (OTUs) in two groups, and 22 unique OTUs occurred in the F group. Fluoride increased the microbiota diversity and species richness of the colon. Concretely, the abundance of the Tenericutes was increased at the level of the phyla in the F group. In addition, in the F group, significant differences at the genus level were observed in Faecalibaculum, Alloprevotella, [Eubacterium]_xylanophilum_group, Prevotellaceae_UCG-001, and Ruminiclostridium_9, compared to the C group. Among them, except for the reduction in Faecalibaculum, the other four bacteria were increased in the F group. In summary, the intestinal microbial composition of mice was reconstituted by the presence of fluoride, and the significantly changing bacteria may partly account for the pathogenesis of fluoride-induced intestinal dysfunction.

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References

  1. Jha SK, Mishra VK, Sharma DK, Damodaran T (2011) Fluoride in the environment and its metabolism in humans. Rev Environ Contam Toxicol 211:121–142

    CAS  PubMed  Google Scholar 

  2. Rashid A, Guan DX, Farooqi A, Khan S, Zahir S, Jehan S, Khattak SA, Khan MS, Khan R (2018) Fluoride prevalence in groundwater around a fluorite mining area in the flood plain of the River Swat, Pakistan. Sci Total Environ 635:203–215

    Article  CAS  Google Scholar 

  3. Jagtap S, Yenkie MK, Labhsetwar N, Rayalu S (2012) Fluoride in drinking water and defluoridation of water. Chem Rev 112(4):2454–2466

    Article  CAS  Google Scholar 

  4. Sharma D, Singh A, Verma K, Paliwal S, Sharma S, Dwivedi J (2017) Fluoride: A review of pre-clinical and clinical studies. Environ Toxicol Pharmacol 56:297–313

    Article  CAS  Google Scholar 

  5. Death CE, Coulson G, Hufschmid J, Morris WK, Gould J, Stevenson M (2019) When less is more: a comparison of models to predict fluoride accumulation in free-ranging kangaroos. Sci Total Environ 660:531–540

    Article  CAS  Google Scholar 

  6. Whitford GM (1996) The metabolism and toxicity of fluoride. Monogr Oral Sci 16 Rev 2:1–153

    Google Scholar 

  7. Wang H, Liu J, Zhao W, Zhang Z, Li S, Li S, Zhu S, Zhou B (2019) Effect of fluoride on small intestine morphology and serum cytokine contents in rats. Biol Trace Elem Res 189(2):511–518

    Article  CAS  Google Scholar 

  8. Luo Q, Cui H, Peng X, Fang J, Zuo Z, Deng J, Liu J, Deng Y (2013) Intestinal IgA+ cell numbers as well as IgA, IgG, and IgM contents correlate with mucosal humoral immunity of broilers during supplementation with high fluorine in the diets. Biol Trace Elem Res 154(1):62–72

    Article  CAS  Google Scholar 

  9. Luo Q, Cui H, Peng X, Fang J, Zuo Z, Deng J, Liu J, Deng Y (2013) Suppressive effects of dietary high fluorine on the intestinal development in broilers. Biol Trace Elem Res 156(1-3):153–165

    Article  CAS  Google Scholar 

  10. Kim YS, Ho SB (2010) Intestinal goblet cells and mucins in health and disease: recent insights and progress. Curr Gastroenterol Rep 12(5):319–330

    Article  Google Scholar 

  11. Kitajima S, Morimoto M, Sagara E, Shimizu C, Ikeda Y (2001) Dextran sodium sulfate-induced colitis in germ-free IQI/Jic mice. Exp Anim 50(5):387–395

    Article  CAS  Google Scholar 

  12. Johansson ME, Gustafsson JK, Sjöberg KE, Petersson J, Holm L, Sjövall H, Hansson GC (2010) Bacteria penetrate the inner mucus layer before inflammation in the dextran sulfate colitis model. Plos One 5(8):e12238

    Article  Google Scholar 

  13. Barko PC, Mcmichael MA, Swanson KS, Williams DA (2018) The gastrointestinal microbiome: A review. J Vet Intern Med 32(1):9–25

    Article  CAS  Google Scholar 

  14. Tilocca B, Burbach K, Heyer CME, Hoelzle LE, Mosenthin R, Stefanski V, Camarinha-Silva A, Seifert J (2017) Dietary changes in nutritional studies shape the structural and functional composition of the pigs’ fecal microbiome-from days to weeks. Microbiome 5(1):144

    Article  Google Scholar 

  15. Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R (2012) Diversity, stability and resilience of the human gut microbiota. Nature 489(7415):220–230

    Article  CAS  Google Scholar 

  16. Liu J, Wang H, Lin L, Miao C, Zhang Y, Zhou B (2019) Intestinal barrier damage involved in intestinal microflora changes in fluoride-induced mice. Chemosphere 234:409–418

    Article  CAS  Google Scholar 

  17. Allaire JM, Crowley SM, Law HT, Chang SY, Ko HJ, Vallance BA (2018) The intestinal epithelium: central coordinator of mucosal immunity. Trends Immunol 39(9):677–696

    Article  CAS  Google Scholar 

  18. Qi Y, Sun J, Ren L, Cao X, Dong J, Tao K, Guan X, Cui Y, Su W (2019) Intestinal microbiota is altered in patients with gastric cancer from Shanxi Province, China. Dig Dis Sci 64(5):1193–1203

    Article  CAS  Google Scholar 

  19. Follin-Arbelet B, Moum B (2016) Fluoride: a risk factor for inflammatory bowel disease? Scand J Gastroenterol 51(9):1019–1024

    Article  CAS  Google Scholar 

  20. Lambert GP (2009) Stress-induced gastrointestinal barrier dysfunction and its inflammatory effects. J Anim Sci 87(14 Suppl):E101–E108

    Article  CAS  Google Scholar 

  21. Lloyd-Price J, Abu-Ali G, Huttenhower C (2016) The healthy human microbiome. Genome Med 8(1):51

    Article  Google Scholar 

  22. Augenstein WL, Spoerke DG, Kulig KW, Hall AH, Hall PK, Riggs BS, Saadi M, El RBH (1991) Fluoride ingestion in children: a review of 87 cases. Pediatrics 88(5):907–912

    CAS  PubMed  Google Scholar 

  23. Integrative HMP Research Network Consortium (2019) The integrative human microbiome project. Nature 569(7758):641–648

    Article  Google Scholar 

  24. Kim HB, Isaacson RE (2015) The pig gut microbial diversity: Understanding the pig gut microbial ecology through the next generation high throughput sequencing. Vet Mmicrobiol 177(3-4):242–251

    Article  CAS  Google Scholar 

  25. Wan X, Bi J, Gao X, Tian F, Wang X, Li N, Li J (2015) Partial enteral nutrition preserves elements of gut barrier function, including innate immunity, intestinal alkaline phosphatase (IAP) level, and intestinal microbiota in mice. Nutrients 7(8):6294–6312

    Article  CAS  Google Scholar 

  26. Ma H, Zhang B, Hu Y, Wang J, Liu J, Qin R, Lv S, Wang S (2019) Correlation analysis of intestinal redox state with the gut microbiota reveals the positive intervention of tea polyphenols on hyperlipidemia in high-fat diet fed mice. J Agric Food Chem 67(26):7325–7335

    Article  CAS  Google Scholar 

  27. Chen W, Liu F, Ling Z, Tong X, Xiang C (2012) Human intestinal lumen and mucosa-associated microbiota in patients with colorectal cancer. PLoS One 7(6):e39743

    Article  CAS  Google Scholar 

  28. Ke X, Walker A, Haange SB, Lagkouvardos I, Liu Y, Schmitt-Kopplin P, von Bergen M, Jehmlich N, He X, Clavel T, Cheung PCK (2019) Synbiotic-driven improvement of metabolic disturbances is associated with changes in the gut microbiome in diet-induced obese mice. Mol Metab 22:96–109

    Article  CAS  Google Scholar 

  29. Meehan CJ, Beiko RG (2014) A phylogenomic view of ecological specialization in the Lachnospiraceae, a family of digestive tract-associated bacteria. Genome Biol Evol 6(3):703–713

    Article  CAS  Google Scholar 

  30. Chauhan SS, Mahmood A, Ojha S (2013) Ethanol and age enhances fluoride toxicity through oxidative stress and mitochondrial dysfunctions in rat intestine. Mol Cell Biochem 384(1-2):251–262

    Article  CAS  Google Scholar 

  31. Kang Y, Li Y, Du Y, Guo L, Chen M, Huang X, Yang F, Hong J, Kong X (2019) Konjaku flour reduces obesity in mice by modulating the composition of the gut microbiota. Int J Obes (Lond) 43(8):1631–1643

    Article  CAS  Google Scholar 

  32. Louis S, Tappu RM, Damms-Machado A, Huson DH, Bischoff SC (2016) Characterization of the gut microbial community of obese patients following a weight-loss intervention using whole metagenome shotgun sequencing. PloS One 11(2):e0149564

    Article  Google Scholar 

  33. Yue S, Liu J, Wang W, Wang A, Yang X, Guan H, Wang C, Yan D (2019) Berberine treatment-emergent mild diarrhea associated with gut microbiota dysbiosis. Biomed Pharmacother 116:109002

    Article  CAS  Google Scholar 

  34. Su T, Liu R, Lee A, Long Y, Du L, Lai S, Chen X, Wang L, Si J, Owyang C, Chen S (2018) Altered intestinal microbiota with increased abundance of prevotella is associated with high risk of diarrhea-predominant irritable bowel syndrome. Gastroenterol Res Pract 2018:6961783

    PubMed  PubMed Central  Google Scholar 

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Funding

This work was supported by the Top Young Innovative Talents of Shanxi Agricultural University (Grant No. TYIT201408).

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Correspondence to Zilong Sun.

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Table S1.

Operative taxonomical units (OTU) data in the control group (C group) and the fluoride group (F group). (XLSX 19 kb)

Table S2.

Relative abundance data of bacteria in the control group (C group) and the fluoride group (F group) at the phylum level. (XLSX 9 kb)

Table S3.

Relative abundance data of the top 20 bacteria in the control group (C group) and the fluoride group (F group) at the genus level. (XLSX 9 kb)

Table S4.

The top 50 genera correlation analysis using the SparCC method in the two groups. (XLSX 10 kb)

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Fu, R., Niu, R., Li, R. et al. Fluoride-Induced Alteration in the Diversity and Composition of Bacterial Microbiota in Mice Colon. Biol Trace Elem Res 196, 537–544 (2020). https://doi.org/10.1007/s12011-019-01942-w

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  • DOI: https://doi.org/10.1007/s12011-019-01942-w

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