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Systematic Review

The effect of dietary zinc and zinc physiological status on the composition of the gut microbiome in vivo

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References

  • Abrantes, M. C., M. d F. Lopes, and J. Kok. 2011. Impact of manganese, copper and zinc ions on the transcriptome of the nosocomial pathogen Enterococcus faecalis V583. PloS One 6 (10):e26519.
  • Almoudi, M. M., A. S. Hussein, M. I. A. Hassan, and N. M. Zain. 2018. A systematic review on antibacterial activity of zinc against Streptococcus mutans. The Saudi Dental Journal 30 (4):283–91.
  • Andreini, C., L. Banci, I. Bertini, and A. Rosato. 2005. Counting the zinc-proteins encoded in the human genome. Journal of Proteome Research 5:196–291.
  • Andreini, C., L. Banci, I. Bertini, and A. Rosato. 2006. Zinc through the three domains of life. Journal of Proteome Research 5 (11):3173–8.
  • Bailey, R. L., D. J. Catellier, S. Jun, J. T. Dwyer, E. F. Jacquier, A. S. Anater, and A. L. Eldridge. 2018. Total usual nutrient intakes of US children (under 48 months): findings from the feeding infants and toddlers study (FITS) 2016. The Journal of Nutrition 148 (9S):1557S–1566S.
  • Baker-Austin, C., M. S. Wright, R. Stepanauskas, and J. V. McArthur. 2006. Co-selection of antibiotic and metal resistance. Trends in Microbiology 14 (4):176–82.
  • Barwinska-Sendra, A., and K. J. Waldron. 2017. Chapter Eight – The Role of Intermetal Competition and Mis-Metalation in Metal Toxicity. Advances in Microbial Physiology, Vol. 70, 315–79. Cambridge, MA: Academic Press.
  • Behnsen, J., H. Zhi, A. T. Aron, V. Subramanian, W. Santus, M. H. Lee, R. R. Gerner, D. Petras, J. Z. Liu, K. D. Green, et al. 2021. Siderophore-mediated zinc acquisition enhances enterobacterial colonization of the inflamed gut. Nature Communications 12 (1):7016.
  • Belkaid, Y., and T. W. Hand. 2014. Role of the microbiota in immunity and inflammation. Cell 157 (1):121–41.
  • Belzer, C. 2022. Nutritional strategies for mucosal health: the interplay between microbes and mucin glycans. Trends in Microbiology 30 (1):13–21. doi: 10.1016/j.tim.2021.06.003.
  • Birchenough, G. M., M. E. Johansson, J. K. Gustafsson, J. H. Bergstrom, and G. C. Hansson. 2015. New developments in goblet cell mucus secretion and function. Mucosal Immunology 8 (4):712–9.
  • Blindauer, C. A., M. D. Harrison, J. A. Parkinson, A. K. Robinson, J. S. Cavet, N. J. Robinson, and P. J. Sadler. 2001. A metallothionein containing a zinc finger within a four-metal cluster protects a bacterium from zinc toxicity. Proceedings of the National Academy of Sciences of the United States of America 98 (17):9593–8.
  • Bombaywala, S., H. J. Purohit, and N. A. Dafale. 2021. Mobility of antibiotic resistance and its co-occurrence with metal resistance in pathogens under oxidative stress. Journal of Environmental Management 297:113315.
  • Burger-van Paassen, N., A. Vincent, P. J. Puiman, M. van der Sluis, J. Bouma, G. Boehm, J. B. Van Goudoever, I. Van Seuningen, and I. B. Renes. 2009. The regulation of intestinal mucin MUC2 expression by short-chain fatty acids: implications for epithelial protection. The Biochemical Journal 420 (2):211–9.
  • Capdevila, D. A., J. Wang, and D. P. Giedroc. 2016. Bacterial strategies to maintain zinc metallostasis at the host-pathogen interface. The Journal of Biological Chemistry 291 (40):20858–68.
  • Castillo, Y., M. Tachibana, Y. Nakatsu, K. Watanabe, T. Shimizu, and M. Watarai. 2015. Combination of zinc and all-trans retinoic acid promotes protection against Listeria monocytogenes infection. PloS One 10 (9):e0137463.
  • Cerasi, M., S. Ammendola, and A. Battistoni. 2013. Competition for zinc binding in the host-pathogen interaction. Frontiers in Cellular and Infection Microbiology 3:108.
  • Cheng, J., H. Bar, and E. Tako. 2021. Zinc status index (ZSI) for quantification of zinc physiological status. Nutrients 13 (10):3399.
  • Chen, P. R., and C. He. 2008. Selective recognition of metal ions by metalloregulatory proteins. Current Opinion in Chemical Biology 12 (2):214–21.
  • Chen, X., Y. Jiang, Z. Wang, Y. Chen, S. Tang, S. Wang, L. Su, X. Huang, D. Long, L. Wang, et al. 2022. Alteration in gut microbiota associated with zinc deficiency in school-age children. Nutrients 14 (14):2895.
  • Chen, J., J. Li, H. Zhang, W. Shi, and Y. Liu. 2019. Bacterial heavy-metal and antibiotic resistance genes in a copper Tailing Dam Area in Northern China. Frontiers in Microbiology 10:1916.
  • Chen, L., Z. Wang, P. Wang, X. Yu, H. Ding, Z. Wang, and J. Feng. 2021. Effect of long-term and short-term imbalanced Zn manipulation on gut microbiota and screening for microbial markers sensitive to zinc status. Microbiology spectrum 9 (3):e0048321.
  • Chinda, D., S. Nakaji, S. Fukuda, J. Sakamoto, T. Shimoyama, T. Nakamura, T. Fujisawa, A. Terada, and K. Sugawara. 2004. The fermentation of different dietary fibers is associated with fecal Clostridia levels in men. Journal of Nutrition 134:1881–6.
  • Ciesinski, L., S. Guenther, R. Pieper, M. Kalisch, C. Bednorz, and L. H. Wieler. 2018. High dietary zinc feeding promotes persistence of multi-resistant E. coli in the swine gut. PloS One 13 (1):e0191660.
  • Coudray, C., C. Feillet-Coudray, E. Gueux, A. Mazur, and Y. Rayssiguier. 2006. Dietary inulin intake and age can affect intestinal absorption of zinc and copper in rats. The Journal of Nutrition 136 (1):117–22.
  • Council, N. R. 1994. Nutrient Requirements of Poultry. Ninth Revised Edition. Washington, DC, The National Academies Press.
  • Council, N. R. 2012. Nutrient Requirements of Swine. Eleventh Revised Edition. Washington, DC, The National Academies Press.
  • Davis, D. J., P. M. Hecht, E. Jasarevic, D. Q. Beversdorf, M. J. Will, K. Fritsche, and C. H. Gillespie. 2017. Sex-specific effects of docosahexaenoic acid (DHA) on the microbiome and behavior of socially-isolated mice. Brain, Behavior, and Immunity 59:38–48.
  • De Benoist, B., I. Darnton-Hill, L. Davidsson, O. Fontaine, and C. Hotz. 2007. Conclusions of the joint WHO/UNICEF/IAEA/IZiNCG interagency meeting on zinc status indicators. Food and Nutrition Bulletin 28 (3 Suppl):S480–S484.
  • Deplancke, B., and H. R. Gaskins. 2001. Microbial modulation of innate defense: goblet cells and the intestinal mucus layer. The American Journal of Clinical Nutrition 73 (6):1131S–1141S.
  • Derrien, M., C. Belzer, and W. M. de Vos. 2017. Akkermansia muciniphila and its role in regulating host functions. Microbial pathogenesis 106:171–81.
  • Durrani, M., R. Nazli, N. Sher, M. Abubakr, and J. Ali. 2021. Gut Microbiome Profile in Zinc Deficient Infants Using Next Generation Sequencing. Kohat-Khyber Pakhtunkhwa, Pakistan: Khyber Medical University Journal.
  • El-Farghali, O., M. A. El-Wahed, N. E. Hassan, S. Imam, and K. Alian. 2015. Early zinc supplementation and enhanced growth of the low-birth weight neonate. Open access Macedonian Journal of Medical Sciences 3 (1):63–8.
  • Feng, W., H. Ao, and C. Peng. 2018. Gut microbiota, short-chain fatty acids, and herbal medicines. Frontiers in Pharmacology 9:1354.
  • Foligne, B., F. George, A. Standaert, A. Garat, S. Poiret, V. Peucelle, S. Ferreira, H. Sobry, G. Muharram, A. Lucau-Danila, et al. 2020. High-dose dietary supplementation with zinc prevents gut inflammation: Investigation of the role of metallothioneins and beyond by transcriptomic and metagenomic studies. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology 34 (9):12615–33.
  • Foligne, B., S. Nutten, C. Grangette, V. Dennin, D. Goudercourt, S. Poiret, J. Dewulf, D. Brassart, A. Mercenier, and B. Pot. 2007. Correlation between in vitro and in vivo immunomodulatory properties of lactic acid bacteria. World journal of Gastroenterology 13 (2):236–43.
  • Fosmire, G. J. 1990. Zinc toxicity. The American Journal of Clinical Nutrition 51 (2):225–7. doi: 10.1093/ajcn/51.2.225.
  • Francis, J. D., M. A. Guevara, J. Lu, S. A. Madhi, G. Kwatra, D. M. Aronoff, S. D. Manning, and J. A. Gaddy. 2022. The antimicrobial activity of zinc against group B Streptococcus is strain-dependent across diverse sequence types, capsular serotypes, and invasive versus colonizing isolates. BMC Microbiology 22 (1):23.
  • Frederickson, C. J., J. Y. Koh, and A. I. Bush. 2005. The neurobiology of zinc in health and disease. Nature reviews. Neuroscience 6 (6):449–62.
  • Ganesan, K., S. K. Chung, J. Vanamala, and B. Xu. 2018. Causal relationship between diet-induced gut microbiota changes and diabetes: a novel strategy to transplant Faecalibacterium prausnitzii in preventing diabetes. International Journal of Molecular Sciences 19 (12):3720.
  • Garenne, M., H. Becher, Y. Ye, B. Kouyate, and O. Müller. 2007. Sex-specific responses to zinc supplementation in Nouna, Burkina Faso. Journal of Pediatric Gastroenterology and Nutrition 44 (5):619–28.
  • Gaulke, C. A., J. Rolshoven, C. P. Wong, L. G. Hudson, E. Ho, and T. J. Sharpton. 2018. Marginal zinc deficiency and environmentally relevant concentrations of arsenic elicit combined effects on the gut microbiome. mSphere 3 (6):e00521-18.
  • Gefeller, E. M., H. Martens, J. R. Aschenbach, S. Klingspor, S. Twardziok, P. Wrede, R. Pieper, and U. Lodemann. 2015. Effects of age and zinc supplementation on transport properties in the jejunum of piglets. Journal of Animal Physiology and Animal Nutrition ) 99 (3):542–52.
  • Geiser, J., K. J. Venken, R. C. De Lisle, and G. K. Andrews. 2012. A mouse model of acrodermatitis enteropathica: Loss of intestine zinc transporter ZIP4 (Slc39a4) disrupts the stem cell niche and intestine integrity. PLoS Genetics 8 (6):e1002766.
  • Gielda, L. M., and V. J. DiRita. 2012. Zinc competition among the intestinal microbiota. mBio 3 (4):e00171-12.
  • Glover, J. S., T. D. Ticer, and M. A. Engevik. 2022. Characterizing the mucin-degrading capacity of the human gut microbiota. Scientific Reports 12 (1):8456.
  • Gomes, M. J. C., H. S. D. Martino, and E. Tako. 2021. Effects of iron and zinc biofortified foods on gut microbiota in vivo (Gallus gallus): a systematic review. Nutrients 13 (1):189.
  • Gomez, A., D. Luckey, and V. Taneja. 2015. The gut microbiome in autoimmunity: sex matters. Clinical Immunology (Orlando, FL.) 159 (2):154–62.
  • Graham, A. I., S. Hunt, S. L. Stokes, N. Bramall, J. Bunch, A. G. Cox, C. W. McLeod, and R. K. Poole. 2009. Severe zinc depletion of Escherichia coli: roles for high affinity zinc binding by ZinT, zinc transport and zinc-independent proteins. The Journal of Biological Chemistry 284 (27):18377–89.
  • Greetham, H. L., G. R. Gibson, C. Giffard, H. Hippe, B. Merkhoffer, U. Steiner, E. Falsen, and M. D. Collins. 2004. Allobaculum stercoricanis gen. nov., sp. nov., isolated from canine feces. Anaerobe 10 (5):301–7.
  • Grossman, C. 1989. Possible underlying mechanisms of sexual dimorphism in the immune response, fact and hypothesis. Journal of Steroid Biochemistry 34 (1-6):241–51. doi: 10.1016/0022-4731(89)90088-5.
  • Han, X., F. Liu, Q. Zhang, B. Mao, X. Tang, J. Huang, R. Guo, J. Zhao, H. Zhang, S. Cui, et al. 2022. Effects of Zn-enriched Bifidobacterium longum on the growth and reproduction of rats. Nutrients 14 (4):783.
  • Hantke, K. 2005. Bacterial zinc uptake and regulators. Current Opinion in Microbiology 8 (2):196–202. doi: 10.1016/j.mib.2005.02.001.
  • Harris, A. 1969. Inhibition of growth and nucleic acid synthesis in zinc-deficient Mycobacterium smegmatis. Microbiology 56 (1):27–33.
  • Hashimoto, A., M. Nakagawa, N. Tsujimura, S. Miyazaki, K. Kizu, T. Goto, Y. Komatsu, A. Matsunaga, H. Shirakawa, H. Narita, et al. 2016. Properties of Zip4 accumulation during zinc deficiency and its usefulness to evaluate zinc status: a study of the effects of zinc deficiency during lactation. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 310 (5):R459–468.
  • Hibbing, M. E., C. Fuqua, M. R. Parsek, and S. B. Peterson. 2010. Bacterial competition: surviving and thriving in the microbial jungle. Nature Reviews. Microbiology 8 (1):15–25.
  • Higgins, J. P., D. G. Altman, P. C. Gotzsche, P. Juni, D. Moher, A. D. Oxman, J. Savovic, K. F. Schulz, L. Weeks, J. A. C. Sterne, and Cochrane Bias Methods and G. Cochrane Statistical Methods. 2011. The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ 343:5928.
  • Hooijmans, C. R., M. M. Rovers, R. B. de Vries, M. Leenaars, M. Ritskes-Hoitinga, and M. W. Langendam. 2014. SYRCLE’s risk of bias tool for animal studies. BMC Medical Research Methodology 14:43.
  • Hoskins, L. C., E. T. Boulding, T. A. Gerken, V. R. Harouny, and M. S. Kriaris. 1992. Mucin glycoprotein degradation by mucin oligosaccharide-degrading strains of human faecal bacteria. Characterisation of saccharide cleavage products and their potential role in nutritional support of larger faecal bacterial populations. Microbial Ecology in Health and Disease 5 (4):193–207.
  • Huang, Y., S. Cunnane, D. Horrobin, and J. Davignon. 1982. Most biological effects of zinc deficiency corrected by γ-linolenic acid (18: 3ω6) but not by linoleic acid (18: 2ω6). Atherosclerosis 41 (2-3):193–207.
  • Huang, X., D. Jiang, Y. Zhu, Z. Fang, L. Che, Y. Lin, S. Xu, J. Li, C. Huang, Y. Zou, et al. 2017. Chronic high dose zinc supplementation induces visceral adipose tissue hypertrophy without altering body weight in mice. Nutrients 9 (10):1138.
  • Huang, L., and S. Tepaamorndech. 2013. The SLC30 family of zinc transporters – a review of current understanding of their biological and pathophysiological roles. Molecular Aspects of Medicine 34 (2–3):548–60.
  • Huang, L., Y. Y. Yu, C. P. Kirschke, E. R. Gertz, and K. K. C. Lloyd. 2007. Znt7 (Slc30a7)-deficient mice display reduced body zinc status and body fat accumulation. The Journal of Biological Chemistry 282 (51):37053–63.
  • Huynh, U., and M. L. Zastrow. 2023. Metallobiology of Lactobacillaceae in the gut microbiome. Journal of Inorganic Biochemistry 238:112023.
  • Jeong, J., and D. J. Eide. 2013. The SLC39 family of zinc transporters. Molecular Aspects of Medicine 34 (2–3):612–9. doi: 10.1016/j.mam.2012.05.011.
  • Jiminez, J. A., T. C. Uwiera, D. W. Abbott, R. R. E. Uwiera, and G. D. Inglis. 2017. Butyrate supplementation at high concentrations alters enteric bacterial communities and reduces intestinal inflammation in mice infected with Citrobacter rodentium. mSphere 2 (4):e00243-17.
  • Johansson, M. E. V., and G. C. Hansson. 2016. The mucins. In Encyclopedia of immunobiology, ed. M. J. H. Ratcliffe, 381–8. Oxford: Academic Press.
  • Kable, M. E., N. Riazati, C. P. Kirschke, J. Zhao, S. Tepaamorndech, and L. Huang. 2020. The Znt7-null mutation has sex dependent effects on the gut microbiota and goblet cell population in the mouse colon. PloS One 15 (9):e0239681.
  • Kandler, O. 1983. Carbohydrate metabolism in lactic acid bacteria. Antonie van Leeuwenhoek 49 (3):209–24. doi: 10.1007/BF00399499.
  • Kau, A. L., P. P. Ahern, N. W. Griffin, A. L. Goodman, and J. I. Gordon. 2011. Human nutrition, the gut microbiome and the immune system. Nature 474 (7351):327–36.
  • Kelly, E. J., C. J. Quaife, G. J. Froelick, and R. D. Palmiter. 1996. Metallothionein I and II protect against zinc deficiency and zinc toxicity in mice. The Journal of Nutrition 126 (7):1782–90.
  • Kim, J. J., and W. I. Khan. 2013. Goblet cells and mucins: Role in innate defense in enteric infections. Pathogens (Basel, Switzerland) 2 (1):55–70. doi: 10.3390/pathogens2010055.
  • Kim, S., Y.-C. Shin, T.-Y. Kim, Y. Kim, Y.-S. Lee, S.-H. Lee, M.-N. Kim, E. O, K. S. Kim, and M.-N. Kweon. 2021. Mucin degrader Akkermansia muciniphila accelerates intestinal stem cell-mediated epithelial development. Gut microbes 13 (1):1–20.
  • Kimura, T., and T. Kambe. 2016. The functions of metallothionein and ZIP and ZnT transporters: an overview and perspective. International Journal of Molecular Sciences 17 (3):336.
  • King, J. C., K. H. Brown, R. S. Gibson, N. F. Krebs, N. M. Lowe, J. H. Siekmann, and D. J. Raiten. 2015. Biomarkers of nutrition for development (BOND)-zinc review. The Journal of Nutrition 146 (4):858S–85S.
  • Klawe, J. J., and M. Tafil-Klawe. 2003. Antibiotic-resistant bacteria. Encyclopedia of Food Sciences and Nutrition (Second Edition), ed. B. Caballero, 247–9. Oxford: Academic Press.
  • Kloubert, V., K. Blaabjerg, T. S. Dalgaard, H. D. Poulsen, L. Rink, and I. Wessels. 2018. Influence of zinc supplementation on immune parameters in weaned pigs. Journal of Trace Elements in Medicine and Biology : Organ of the Society for Minerals and Trace Elements (GMS) 49:231–40.
  • Knez, M., A. Pantovic, E. Tako, andE. Boy. 2022. FADS1 and FADS2 as biomarkers of Zn status- a systematic review and meta-analysis. Critical Reviews in Food Science and Nutrition :1–19. 10.1080/10408398.2022.2103790. PMID: 35880429
  • Kostic, A. D., D. Gevers, H. Siljander, T. Vatanen, T. Hyötyläinen, A.-M. Hämäläinen, A. Peet, V. Tillmann, P. Pöhö, I. Mattila, DIABIMMUNE Study Group, et al. 2015. The dynamics of the human infant gut microbiome in development and in progression toward Type 1 diabetes. Cell Host & Microbes 17 (2):260–73.
  • La Reau, A. J., and G. Suen. 2018. The Ruminococci: key symbionts of the gut ecosystem. Journal of Microbiology (Seoul, Korea) 56 (3):199–208.
  • Laue, H. E., M. R. Karagas, M. O. Coker, D. C. Bellinger, E. R. Baker, S. A. Korrick, and J. C. Madan. 2022. Sex-specific relationships of the infant microbiome and early-childhood behavioral outcomes. Pediatric Research 92 (2):580–91.
  • Liedtke, J., and W. Vahjen. 2012. In vitro antibacterial activity of zinc oxide on a broad range of reference strains of intestinal origin. Veterinary Microbiology 160 (1–2):251–5.
  • Liu, X., B. Mao, J. Gu, J. Wu, S. Cui, G. Wang, J. Zhao, H. Zhang, and W. Chen. 2021. Blautia – a new functional genus with potential probiotic properties? Gut Microbes 13 (1):1–21.
  • Lopez, C. A., and E. P. Skaar. 2018. The Impact of Dietary Transition Metals on Host-Bacterial Interactions. Cell Host & Microbes 23 (6):737–48.
  • Lowe, N. M. 2016. Assessing zinc in humans. Current Opinion in Clinical Nutrition & Metabolic Care 19 (5):321–7.
  • Lowe, N. M., K. Fekete, and T. Decsi. 2009. Methods of assessment of zinc status in humans: A systematic review. The American Journal of Clinical Nutrition 89 (6):2040S–2051S.
  • Maares, M., and H. Haase. 2020. A guide to human zinc absorption: general overview and recent advances of in vitro intestinal models. Nutrients 12 (3):762.
  • Macfarlane, G. T., and S. Macfarlane. 2012. Bacteria, colonic fermentation, and gastrointestinal health. Journal of AOAC International 95 (1):50–60. doi: 10.5740/jaoacint.sge_macfarlane.
  • Maret, W., and H. H. Sandstead. 2006. Zinc requirements and the risks and benefits of zinc supplementation. Journal of Trace Elements in Medicine and Biology: Organ of the Society for Minerals and Trace Elements (GMS) 20 (1):3–18.
  • Mariat, D., O. Firmesse, F. Levenez, V. D. Guimarăes, H. Sokol, J. Doré, G. Corthier, and J. P. Furet. 2009. The Firmicutes/Bacteroidetes ratio of the human microbiota changes with age. BMC Microbiology 9 (1):123.
  • Martin-Gallausiaux, C., L. Marinelli, H. M. Blottière, P. Larraufie, and N. Lapaque. 2021. SCFA: Mechanisms and functional importance in the gut. The Proceedings of the Nutrition Society 80 (1):37–49.
  • Maserejian, N. N., S. A. Hall, and J. B. McKinlay. 2012. Low dietary or supplemental zinc is associated with depression symptoms among women, but not men, in a population-based epidemiological survey. Journal of Affective Disorders 136 (3):781–8.
  • Mayneris-Perxachs, J., D. T. Bolick, J. Leng, G. L. Medlock, G. L. Kolling, J. A. Papin, J. R. Swann, and R. L. Guerrant. 2016. Protein- and zinc-deficient diets modulate the murine microbiome and metabolic phenotype. The American Journal of Clinical Nutrition 104 (5):1253–62.
  • McInnes, R. S., G. E. McCallum, L. E. Lamberte, and W. van Schaik. 2020. Horizontal transfer of antibiotic resistance genes in the human gut microbiome. Current opinion in Microbiology 53:35–43.
  • Mohd Yusof, H., R. Mohamad, U. H. Zaidan, and N. A. A. Rahman. 2020. Sustainable microbial cell nanofactory for zinc oxide nanoparticles production by zinc-tolerant probiotic Lactobacillus plantarum strain TA4. Microbial Cell Factories 19 (1):10.
  • Mrvčić, J., T. Prebeg, L. Barišić, D. Stanzer, V. Bačun-Družina, and V. Stehlik-Tomas. 2009. Zinc binding by lactic acid bacteria. Food Technology & Biotechnology 47 (4):381–388.
  • Mu, Q., V. J. Tavella, and X. M. Luo. 2018. Role of Lactobacillus reuteri in human health and diseases. Frontiers in Microbiology 9:757.
  • National Research Council Subcommittee on Laboratory Animal. 1995. Nutrient Requirements of Laboratory Animals. Fourth Revised Edition. Washington (DC): National Academies Press (US).
  • Neupane, D. P., D. Avalos, S. Fullam, H. Roychowdhury, and E. T. Yukl. 2017. Mechanisms of zinc binding to the solute-binding protein AztC and transfer from the metallochaperone AztD. Journal of Biological Chemistry. 292 (42):17496–505.
  • Nielsen, F. H. 2012. History of Zinc in Agriculture. Advances in Nutrition (Bethesda, MD.) 3 (6):783–9. doi: 10.3945/an.112.002881.
  • Nies, D. H. 2003. Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiology Reviews 27 (2-3):313–39.
  • Nies, D. H., and S. Silver. 1995. Ion efflux systems involved in bacterial metal resistances. Journal of Industrial Microbiology 14 (2):186–99. doi: 10.1007/BF01569902.
  • Oh, H. J., Y. J. Park, J. H. Cho, M. H. Song, B. H. Gu, W. Yun, J. H. Lee, J. S. An, Y. J. Kim, J. S. Lee, et al. 2021. Changes in diarrhea score, nutrient digestibility, zinc utilization, intestinal immune profiles, and fecal microbiome in weaned piglets by different forms of zinc. Animals (Basel) 11 (5):1356.
  • Ohashi, Y., and T. Fujisawa. 2019. Analysis of Clostridium cluster XI bacteria in human feces. Bioscience of Microbiota, Food and Health 38 (2):65–8.
  • Oteiza, P. I. 2012. Zinc and the modulation of redox homeostasis. Free radical Biology & Medicine 53 (9):1748–59. doi: 10.1016/j.freeradbiomed.2012.08.568.
  • Page, M. J., J. E. McKenzie, P. M. Bossuyt, I. Boutron, T. C. Hoffmann, C. D. Mulrow, L. Shamseer, J. M. Tetzlaff, E. A. Akl, S. E. Brennan, et al. 2021. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ (Clinical Research ed.) 372:n71.
  • Pasquet, J., Y. Chevalier, J. Pelletier, E. Couval, D. Bouvier, and M.-A. Bolzinger. 2014. The contribution of zinc ions to the antimicrobial activity of zinc oxide. Colloids and Surfaces A: Physicochemical and Engineering Aspects 457:263–74.
  • Percie Du Sert, N., A. Ahluwalia, S. Alam, M. T. Avey, M. Baker, W. J. Browne, A. Clark, I. C. Cuthill, U. Dirnagl, M. Emerson, et al. 2020. Reporting animal research: explanation and elaboration for the ARRIVE guidelines 2.0. PLoS Biology. 18 (7):e3000411.
  • Pieper, R., T. H. Dadi, L. Pieper, W. Vahjen, A. Franke, K. Reinert, and J. Zentek. 2020. Concentration and chemical form of dietary zinc shape the porcine colon microbiome, its functional capacity and antibiotic resistance gene repertoire. The ISME Journal 14 (11):2783–93.
  • Podany, A., J. Rauchut, T. Wu, Y. I. Kawasawa, J. Wright, R. Lamendella, D. I. Soybel, and S. L. Kelleher. 2019. Excess dietary zinc intake in neonatal mice causes oxidative stress and alters intestinal host-microbe interactions. Molecular Nutrition & Food Research 63 (3):e1800947.
  • Raimondi, S., E. Musmeci, F. Candeliere, A. Amaretti, and M. Rossi. 2021. Identification of mucin degraders of the human gut microbiota. Scientific Reports 11 (1):11094.
  • Reed, S., H. Neuman, S. Moscovich, R. P. Glahn, O. Koren, and E. Tako. 2015. Chronic zinc deficiency alters chick gut microbiota composition and function. Nutrients 7 (12):9768–84.
  • Reed, S., X. Qin, R. Ran-Ressler, J. T. Brenna, R. P. Glahn, and E. Tako. 2014. Dietary zinc deficiency affects blood linoleic acid: dihomo-gamma-linolenic acid (LA:DGLA) ratio; a sensitive physiological marker of zinc status in vivo (Gallus gallus). Nutrients 6 (3):1164–80. doi: 10.3390/nu6031164.
  • Rowland, I., G. Gibson, A. Heinken, K. Scott, J. Swann, I. Thiele, and K. Tuohy. 2018. Gut microbiota functions: metabolism of nutrients and other food components. European Journal of Nutrition 57 (1):1–24.
  • Ruas-Madiedo, P., J. Hugenholtz, and P. Zoon. 2002. An overview of the functionality of exopolysaccharides produced by lactic acid bacteria. International Dairy Journal 12 (2):163–71.
  • Saper, R. B., and R. Rash. 2009. Zinc: an essential micronutrient. American Family Physician 79 (9):768–72.
  • Sauer, A. K., and A. M. Grabrucker. 2019. Zinc deficiency during pregnancy leads to altered microbiome and elevated inflammatory markers in mice. Frontiers in Neuroscience 13:1295.
  • Shin, J., J.-R. Noh, D.-H. Chang, Y.-H. Kim, M. H. Kim, E. S. Lee, S. Cho, B. J. Ku, M.-S. Rhee, B.-C. Kim, et al. 2019. Elucidation of Akkermansia muciniphila probiotic traits driven by mucin depletion. Frontiers in Microbiology 10:1137.
  • Shin, N.-R., T. W. Whon, and J.-W. Bae. 2015. Proteobacteria: microbial signature of dysbiosis in gut microbiota. Trends in Biotechnology 33 (9):496–503.
  • Slifierz, M. J., R. Friendship, and J. S. Weese. 2015. Zinc oxide therapy increases prevalence and persistence of methicillin-resistant Staphylococcus aureus in pigs: a randomized controlled trial. Zoonoses and Public Health 62 (4):301–8.
  • Smillie, C. S., M. B. Smith, J. Friedman, O. X. Cordero, L. A. David, and E. J. Alm. 2011. Ecology drives a global network of gene exchange connecting the human microbiome. Nature 480 (7376):241–4.
  • Smith, J. C., Jr, E. McDaniel, L. McBean, F. S. Doft, and J. A. Halsted. 1972. Effect of microorganisms upon zinc metabolism using germfree and conventional rats. The Journal of Nutrition 102 (6):711–9.
  • Starke, I. C., R. Pieper, K. Neumann, J. Zentek, and W. Vahjen. 2014. The impact of high dietary zinc oxide on the development of the intestinal microbiota in weaned piglets. FEMS Microbiology Ecology 87 (2):416–27.
  • Stevens, G. A., T. Beal, M. N. N. Mbuya, H. Luo, L. M. Neufeld, O. Y. Addo, S. Adu-Afarwuah, S. Alayón, Z. Bhutta, K. H. Brown, Global Micronutrient Deficiencies Research Group, et al. 2022. Micronutrient deficiencies among preschool-aged children and women of reproductive age worldwide: a pooled analysis of individual-level data from population-representative surveys. The Lancet. Global Health 10 (11):e1590–e1599.
  • Takagishi, T., T. Hara, and T. Fukada. 2017. Recent advances in the role of SLC39A/ZIP zinc transporters in vivo. International Journal of Molecular Sciences. 18 (12):2708.
  • Turroni, F., S. Duranti, F. Bottacini, S. Guglielmetti, D. Van Sinderen, and M. Ventura. 2014. Bifidobacterium bifidum as an example of a specialized human gut commensal. Frontiers in Microbiology 5:437.
  • Vacca, M., G. Celano, F. M. Calabrese, P. Portincasa, M. Gobbetti, and M. De Angelis. 2020. The controversial role of human gut Lachnospiraceae. Microorganisms 8 (4):573.
  • Vahjen, W., R. Pieper, and J. Zentek. 2011. Increased dietary zinc oxide changes the bacterial core and enterobacterial composition in the ileum of piglets. Journal of Animal Science 89 (8):2430–9.
  • Vahjen, W., D. Pietruszynska, I. C. Starke, and J. Zentek. 2015. High dietary zinc supplementation increases the occurrence of tetracycline and sulfonamide resistance genes in the intestine of weaned pigs. Gut Pathogens 7:5.
  • Van Herreweghen, F., K. De Paepe, H. Roume, F.-M. Kerckhof, and T. Van de Wiele. 2018. Mucin degradation niche as a driver of microbiome composition and Akkermansia muciniphila abundance in a dynamic gut model is donor independent. FEMS Microbiology Ecology 94 (12). doi: 10.1093/femsec/fiy186.
  • Wagner, C. E., K. M. Wheeler, and K. Ribbeck. 2018. Mucins and their role in shaping the functions of mucus barriers. Annual review of Cell and Developmental Biology 34 (1):189–215.
  • Wessels, I., M. Maywald, and L. Rink. 2017. Zinc as a gatekeeper of immune function. Nutrients 9 (12):1286.
  • WHO/FAO. 2004. Vitamin and mineral requirements in human nutrition.
  • Wiegand, S., S. S. Zakrzewski, M. Eichner, E. Schulz, D. Günzel, R. Pieper, R. Rosenthal, C. Barmeyer, A. Bleich, U. Dobrindt, et al. 2017. Zinc treatment is efficient against Escherichia coli α-haemolysin-induced intestinal leakage in mice. Scientific Reports 7:45649.
  • Winder, F., and C. O’Hara. 1964. Effects of iron deficiency and of zinc deficiency on the activities of some enzymes in Mycobacterium smegmatis. The Biochemical Journal 90 (1):122–6.
  • Yan, Z., W. Wang, Y. Wu, W. Wang, B. Li, N. Liang, and W. Wu. 2017. Zinc oxide nanoparticle-induced atherosclerotic alterations in vitro and in vivo. International Journal of Nanomedicine 12:4433–42.
  • Yatsunyk, L. A., J. A. Easton, L. R. Kim, S. A. Sugarbaker, B. Bennett, R. M. Breece, I. I. Vorontsov, D. L. Tierney, M. W. Crowder, and A. C. Rosenzweig. 2008. Structure and metal binding properties of ZnuA, a periplasmic zinc transporter from Escherichia coli. Journal of Biological Inorganic Chemistry: JBIC: A Publication of the Society of Biological Inorganic Chemistry 13 (2):271–88.
  • Yazdankhah, S., K. Rudi, and A. Bernhoft. 2014. Zinc and copper in animal feed – development of resistance and co-resistance to antimicrobial agents in bacteria of animal origin. Microbial Ecology in Health and Disease 25:1.
  • Yonekura, L., and H. Suzuki. 2005. Effects of dietary zinc levels, phytic acid and resistant starch on zinc bioavailability in rats. European journal of Nutrition 44 (6):384–91.
  • Yoshida, K., M. Gi, M. Fujioka, I. Teramoto, and H. Wanibuchi. 2019. Long-term administration of excess zinc impairs learning and memory in aged mice. The Journal of Toxicological Sciences 44 (10):681–91.
  • Yu, T., C. Zhu, S. Chen, L. Gao, H. Lv, R. Feng, Q. Zhu, J. Xu, Z. Chen, and Z. Jiang. 2017. Dietary high zinc oxide modulates the microbiome of ileum and colon in weaned piglets. Frontiers in Microbiology 8:825.
  • Yuan, L., L. Wang, Z.-H. Li, M.-Q. Zhang, W. Shao, and G.-P. Sheng. 2019. Antibiotic resistance and microbiota in the gut of Chinese four major freshwater carp from retail markets. Environmental Pollution 255:113327.
  • Zackular, J. P., J. L. Moore, A. T. Jordan, L. J. Juttukonda, M. J. Noto, M. R. Nicholson, J. D. Crews, M. W. Semler, Y. Zhang, L. B. Ware, et al. 2016. Dietary zinc alters the microbiota and decreases resistance to Clostridium difficile infection. Nature Medicine 22 (11):1330–4. doi: 10.1038/nm.4174.
  • Zeng, H., S. Umar, B. Rust, D. Lazarova, and M. Bordonaro. 2019. Secondary bile acids and short chain fatty acids in the colon: a focus on colonic microbiome, cell proliferation, inflammation, and cancer. International Journal of Molecular Sciences 20 (5):1214.
  • Zhang, Y.-J., S. Li, R.-Y. Gan, T. Zhou, D.-P. Xu, and H.-B. Li. 2015. Impacts of gut bacteria on human health and diseases. International Journal of Molecular Sciences 16 (4):7493–519.
  • Zhou, Y., H. Xu, J. Xu, X. Guo, H. Zhao, Y. Chen, Y. Zhou, and Y. Nie. 2021. F. prausnitzii and its supernatant increase SCFAs-producing bacteria to restore gut dysbiosis in TNBS-induced colitis. AMB Express 11 (1):33.

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