Distinct Gut Microbiota Signatures in Mice Treated with Commonly Used Food Preservatives
Abstract
:1. Introduction
2. Materials and Methods
2.1. Animals
2.2. Intervention
2.3. Microbiome Measurement
2.4. Gene Expression Analysis
2.5. Statistical Analysis
3. Results
3.1. Different Food Preservatives Distinctly Impact the Gut Microbiome Diversity
3.2. Food Preservatives Generate Distinct Microbiota Composition in the Mouse Gut
3.3. Mice Treated with Different Preservatives Present Unique Gut Microbiota Signatures
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Nagpal, R.; Yadav, H.; Marotta, F. Gut Microbiota: The next-Gen Frontier in Preventive and Therapeutic Medicine? Front. Med. 2014, 1, 15. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nagpal, R.; Kumar, M.; Yadav, A.K.; Hemalatha, R.; Yadav, H.; Marotta, F.; Yamashiro, Y. Gut Microbiota in Health and Disease: An Overview Focused on Metabolic Inflammation. Benef Microbes 2016, 7, 181–194. [Google Scholar] [CrossRef] [PubMed]
- Nagpal, R.; Mainali, R.; Ahmadi, S.; Wang, S.; Singh, R.; Kavanagh, K.; Kitzman, D.W.; Kushugulova, A.; Marotta, F.; Yadav, H. Gut Microbiome and Aging: Physiological and Mechanistic Insights. Nutr. Healthy Aging 2018, 4, 267–285. [Google Scholar] [CrossRef] [Green Version]
- Nagpal, R.; Shively, C.A.; Register, T.C.; Craft, S.; Yadav, H. Gut Microbiome-Mediterranean Diet Interactions in Improving Host Health. F1000Research 2019, 8, 699. [Google Scholar] [CrossRef] [Green Version]
- Kincaid, H.J.; Nagpal, R.; Yadav, H. Diet-Microbiota-Brain Axis in Alzheimer’s Disease. Ann. Nutr. Metab. 2021, 1–7. [Google Scholar] [CrossRef]
- FDA Code of Federal Regulations 21 CFR § 170.3 PART 170—FOOD ADDITIVES. Available online: https://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfcfr/cfrsearch.cfm?fr=170.3 (accessed on 10 September 2021).
- FDA Overview of Food Ingredients, Additives & Colors. Available online: https://www.fda.gov/food/food-ingredients-packaging/overview-food-ingredients-additives-colors (accessed on 10 September 2021).
- Erickson, M.C.; Doyle, M.P. The Challenges of Eliminating or Substituting Antimicrobial Preservatives in Foods. Annu. Rev. Food Sci. Technol. 2017, 8, 371–390. [Google Scholar] [CrossRef]
- Roberts, C.L.; Keita, A.V.; Duncan, S.H.; O’Kennedy, N.; Söderholm, J.D.; Rhodes, J.M.; Campbell, B.J. Translocation of Crohn’s Disease Escherichia Coli across M-Cells: Contrasting Effects of Soluble Plant Fibres and Emulsifiers. Gut 2010, 59, 1331–1339. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Swidsinski, A.; Loening-Baucke, V.; Herber, A. Mucosal Flora in Crohn’s Disease and Ulcerative Colitis—An Overview. J. Physiol. Pharmacol. 2009, 60 (Suppl. 6), 61–71. [Google Scholar]
- Chassaing, B.; Koren, O.; Goodrich, J.K.; Poole, A.C.; Srinivasan, S.; Ley, R.E.; Gewirtz, A.T. Dietary Emulsifiers Impact the Mouse Gut Microbiota Promoting Colitis and Metabolic Syndrome. Nature 2015, 519, 92–96. [Google Scholar] [CrossRef] [Green Version]
- Hrncirova, L.; Machova, V.; Trckova, E.; Krejsek, J.; Hrncir, T. Food Preservatives Induce Proteobacteria Dysbiosis in Human-Microbiota Associated Nod2-Deficient Mice. Microorganisms 2019, 7, 383. [Google Scholar] [CrossRef] [Green Version]
- Chassaing, B.; Van de Wiele, T.; De Bodt, J.; Marzorati, M.; Gewirtz, A.T. Dietary Emulsifiers Directly Alter Human Microbiota Composition and Gene Expression Ex Vivo Potentiating Intestinal Inflammation. Gut 2017, 66, 1414–1427. [Google Scholar] [CrossRef] [PubMed]
- Hrncirova, L.; Hudcovic, T.; Sukova, E.; Machova, V.; Trckova, E.; Krejsek, J.; Hrncir, T. Human Gut Microbes Are Susceptible to Antimicrobial Food Additives in Vitro. Folia Microbiol. 2019, 64, 497–508. [Google Scholar] [CrossRef] [PubMed]
- Irwin, S.V.; Fisher, P.; Graham, E.; Malek, A.; Robidoux, A. Sulfites Inhibit the Growth of Four Species of Beneficial Gut Bacteria at Concentrations Regarded as Safe for Food. PLoS ONE 2017, 12, e0186629. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- You, X.; Einson, J.E.; Lopez-Pena, C.L.; Song, M.; Xiao, H.; McClements, D.J.; Sela, D.A. Food-Grade Cationic Antimicrobial ε-Polylysine Transiently Alters the Gut Microbial Community and Predicted Metagenome Function in CD-1 Mice. NPJ Sci. Food 2017, 1, 8. [Google Scholar] [CrossRef] [Green Version]
- Ahmadi, S.; Nagpal, R.; Wang, S.; Gagliano, J.; Kitzman, D.W.; Soleimanian-Zad, S.; Sheikh-Zeinoddin, M.; Read, R.; Yadav, H. Prebiotics from Acorn and Sago Prevent High-Fat-Diet-Induced Insulin Resistance via Microbiome-Gut-Brain Axis Modulation. J. Nutr. Biochem. 2019, 67, 1–13. [Google Scholar] [CrossRef]
- Nagpal, R.; Shively, C.A.; Appt, S.A.; Register, T.C.; Michalson, K.T.; Vitolins, M.Z.; Yadav, H. Gut Microbiome Composition in Non-Human Primates Consuming a Western or Mediterranean Diet. Front. Nutr. 2018, 5, 28. [Google Scholar] [CrossRef]
- Nagpal, R.; Wang, S.; Ahmadi, S.; Hayes, J.; Gagliano, J.; Subashchandrabose, S.; Kitzman, D.W.; Becton, T.; Read, R.; Yadav, H. Human-Origin Probiotic Cocktail Increases Short-Chain Fatty Acid Production via Modulation of Mice and Human Gut Microbiome. Sci. Rep. 2018, 8, 12649. [Google Scholar] [CrossRef] [Green Version]
- Caporaso, J.G.; Lauber, C.L.; Walters, W.A.; Berg-Lyons, D.; Huntley, J.; Fierer, N.; Owens, S.M.; Betley, J.; Fraser, L.; Bauer, M.; et al. Ultra-High-Throughput Microbial Community Analysis on the Illumina HiSeq and MiSeq Platforms. ISME J. 2012, 6, 1621–1624. [Google Scholar] [CrossRef] [Green Version]
- Caporaso, J.G.; Kuczynski, J.; Stombaugh, J.; Bittinger, K.; Bushman, F.D.; Costello, E.K.; Fierer, N.; Peña, A.G.; Goodrich, J.K.; Gordon, J.I.; et al. QIIME Allows Analysis of High-Throughput Community Sequencing Data. Nat. Methods 2010, 7, 335–336. [Google Scholar] [CrossRef] [Green Version]
- Nagpal, R.; Neth, B.J.; Wang, S.; Craft, S.; Yadav, H. Modified Mediterranean-Ketogenic Diet Modulates Gut Microbiome and Short-Chain Fatty Acids in Association with Alzheimer’s Disease Markers in Subjects with Mild Cognitive Impairment. EBioMedicine 2019, 47, 529–542. [Google Scholar] [CrossRef] [Green Version]
- Ohtsuki, S.; Yamaguchi, H.; Katsukura, Y.; Asashima, T.; Terasaki, T. MRNA Expression Levels of Tight Junction Protein Genes in Mouse Brain Capillary Endothelial Cells Highly Purified by Magnetic Cell Sorting. J. Neurochem. 2008, 104, 147–154. [Google Scholar] [CrossRef]
- Pinget, G.; Tan, J.; Janac, B.; Kaakoush, N.O.; Angelatos, A.S.; O’Sullivan, J.; Koay, Y.C.; Sierro, F.; Davis, J.; Divakarla, S.K.; et al. Impact of the Food Additive Titanium Dioxide (E171) on Gut Microbiota-Host Interaction. Front. Nutr. 2019, 6, 57. [Google Scholar] [CrossRef] [Green Version]
- Ukena, S.N.; Singh, A.; Dringenberg, U.; Engelhardt, R.; Seidler, U.; Hansen, W.; Bleich, A.; Bruder, D.; Franzke, A.; Rogler, G.; et al. Probiotic Escherichia Coli Nissle 1917 Inhibits Leaky Gut by Enhancing Mucosal Integrity. PLoS ONE 2007, 2, e1308. [Google Scholar] [CrossRef] [PubMed]
- Wang, C.; Yu, X.; Cao, Q.; Wang, Y.; Zheng, G.; Tan, T.K.; Zhao, H.; Zhao, Y.; Wang, Y.; Harris, D.C. Characterization of Murine Macrophages from Bone Marrow, Spleen and Peritoneum. BMC Immunol. 2013, 14, 6. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Segata, N.; Izard, J.; Waldron, L.; Gevers, D.; Miropolsky, L.; Garrett, W.S.; Huttenhower, C. Metagenomic Biomarker Discovery and Explanation. Genome Biol. 2011, 12, 1–18. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Brul, S. Preservative Agents in Foods Mode of Action and Microbial Resistance Mechanisms. Int. J. Food Microbiol. 1999, 50, 1–17. [Google Scholar] [CrossRef]
- Boerema, J.A.; Broda, D.M. MICROBIOLOGICAL SAFETY OF MEAT | Clostridium botulinum. In Encyclopedia of Meat Sciences; Jensen, W.K., Ed.; Elsevier: Oxford, UK, 2004; pp. 786–793. ISBN 9780124649705. [Google Scholar]
- Majou, D.; Christieans, S. Mechanisms of the Bactericidal Effects of Nitrate and Nitrite in Cured Meats. Meat Sci. 2018, 145, 273–284. [Google Scholar] [CrossRef]
- FDA, C. for F.S. and A. Food Additive Status List. Available online: https://www.fda.gov/food/food-additives-petitions/food-additive-status-list (accessed on 10 September 2021).
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Nagpal, R.; Indugu, N.; Singh, P. Distinct Gut Microbiota Signatures in Mice Treated with Commonly Used Food Preservatives. Microorganisms 2021, 9, 2311. https://doi.org/10.3390/microorganisms9112311
Nagpal R, Indugu N, Singh P. Distinct Gut Microbiota Signatures in Mice Treated with Commonly Used Food Preservatives. Microorganisms. 2021; 9(11):2311. https://doi.org/10.3390/microorganisms9112311
Chicago/Turabian StyleNagpal, Ravinder, Nagaraju Indugu, and Prashant Singh. 2021. "Distinct Gut Microbiota Signatures in Mice Treated with Commonly Used Food Preservatives" Microorganisms 9, no. 11: 2311. https://doi.org/10.3390/microorganisms9112311