Abstract
Metabolic disorders caused by the imbalance of gut microbiota have been associated with the consumption of processed foods. Thus, this study aimed to evaluate the effects of antimicrobial food additives (benzoate, sorbate, nitrite, and bisulfite) and sweeteners (saccharin, stevia, sucralose, aspartame, and cyclamate) on the growth and metabolism of some gut and potentially probiotic bacterial species. The effects on the growth of Bifidobacterium longum, Enterococcus faecium, Lactobacillus acidophilus, and Lactococcus lactis subsp. lactis cultures were investigated using a turbidimetric test and by determining the minimum inhibitory concentration (MIC) and minimum bactericidal concentration (MBC). To evaluate the metabolic activity, the cultures were exposed to compounds with the highest antimicrobial activity, subjected to cultivation with inulin (1.5%), and analyzed by liquid chromatography for the production of short-chain fatty acids (acetate, propionate, and butyrate). The results showed that potassium sorbate (25 mg/mL), sodium bisulfite (0.7 mg/mL), sodium benzoate, and saccharin (5 mg/mL) presented greater antimicrobial activity against the studied species. L. lactis and L. acidophilus bacteria had reduced short-chain fatty acid production after exposure to saccharin and sorbate, and B. longum after exposure to sorbate, in comparison to controls (acetic acid reduction 1387 μg/mL and propionic 23 μg/mL p < 0.05).
This is a preview of subscription content, log in via an institution to check access.
Data availability
The data generated in this study are in the published article and available from the corresponding author upon reasonable request.
References
Abiega-Franyutti P, Freyre-Fonseca V (2021) Chronic consumption of food-additives lead to changes via microbiota gut-brain axis. Toxicology 464:153001. https://doi.org/10.1016/j.tox.2021.153001
Akatsu H, Iwabuchi N, Xiao JZ, Matsuyama Z, Kurihara R, Okuda K, Yamamoto K, Maruyama M (2013) Clinical effects of probiotic Bifidobacterium longum BB 536 on immune function and intestinal microbiota in elderly patients receiving enteral tube feeding. Jpen-Parenter Enter 37:631–640. https://doi.org/10.1177/0148607112467819
Anand SP, Sati N (2013) Artificial preservatives and their harmful effects: looking toward nature for safer alternatives. Int J Pharm Sci Res 4:2496–2501
Beards E, Tuohy K, Gibson G (2010) Bacterial, SCFA and gas profiles of a range of food ingredients following in vitro fermentation by human colonic microbiota. Anaerobe 16:420–425. https://doi.org/10.1016/j.anaerobe.2010.05.006
Bensid A, El Abed N, Houicher RJM, Özogul F (2022) Antioxidant and antimicrobial preservatives: properties, mechanism of action and applications in food – a review. Crit Rev Food Sci Nutr 62:2985–3001. https://doi.org/10.1080/10408398.2020.1862046
Bian X, Tu P, Chi L, Gao B, Ru H, Lu K (2017) Saccharin induced liver inflammation in mice by altering the gut microbiota and its metabolic functions. Food Chem Toxicol 107:530–539. https://doi.org/10.1016/j.fct.2017.04.045
Claesson MJ, Jeffery IB, Conde S, Power SE, O’Connor EM, Cusack S, Harris HMB, Coakley M, Lakshminarayanan B, O’Sullivan O, Fitzgerald GF, Deane J, O’Connor M, Harnedy N, O’Connor K, O’Mahony D, Sinderen D, Wallace M, Brennan L, Stanton C, Marchesi JR, Fitzgerald AP, Shanahan F, Hill C, Ross RP, O’Toole PW (2012) Gut microbiota composition correlates with diet and health in the elderly. Nature 488:178–184. https://doi.org/10.1038/nature11319
CLSI (2012) Methods for antimicrobial susceptibility testing of anaerobic bacteria, CLSI Standard Document M11-A8, 8th ed, Clinical and Laboratory Standards Institute.
Eslick S, Thompson C, Berthon B, Wood L (2022) Short-chain fatty acids as anti-inflammatory agents in overweight and obesity: a systematic review and meta-analysis. Nutr Rev 80:838–856. https://doi.org/10.1093/nutrit/nuab059
Everis L (2001) Injured bacteria in foods. Nutr Food Sci 31:84–87. https://doi.org/10.1108/00346650110367008
Ferreira FS (2015) Aditivos alimentares e suas reações adversas no consumo infantil. Rev Univ Vale Do Rio Verde 13:397–407. https://doi.org/10.5892/ruvrd.v13i1.1845
Fitch C, Keim KS (2012) Position of the Academy of Nutrition and Dietetics: use of nutritive and nonnutritive sweeteners. J Acad Nutr Diet 112:739–758. https://doi.org/10.1016/j.jand.2012.03.009
Flores SH, Alegre RM (2001) Nisin production from Lactococcus lactis ATCC 7962 using supplemented whey permeate. Biotechnol Appl Bioc 34:103–107. https://doi.org/10.1042/ba20010030
Gardner C, Wylie-Rosett J, Gidding SS, Steffen LM, Jonhson RK, Reader D, Lichtenstein AH (2012) Nonnutritive sweeteners: current use and health perspectives: a scientific statement from the American Heart Association and the American Diabetes Association. Circulation 126:509–519. https://doi.org/10.1161/CIR.0b013e31825c42ee
Gorska A, Przystupski D, Niemczura MJ, Kulbacka J (2019) Probiotic bacteria: a promising tool in cancer prevention and therapy. Curr Microbiol 76:939–949. https://doi.org/10.1007/s00284-019-01679-8
Hafidh RR, Abdulamir AS, Vern LS, Bakar FA, Abas F, Jahanshiri F, Sekawi Z (2011) Inhibition of growth of highly resistant bacterial and fungal pathogens by a natural product. Open Microbiol J 5:96–106. https://doi.org/10.2174/2F1874285801105010096
Hrncirova L, Hudcovic T, Sukova E, Machova V, Trckova E, Krejsek J, Hrncir T (2019) Human gut microbes are susceptible to antimicrobial food additives in vitro. Folia Microbiol 64:497–508. https://doi.org/10.1007/s12223-018-00674-z
Huvaere K, Vandevijvere S, Hasni M, Vinkx C, Van Loco J (2012) Dietary intake of artificial sweeteners by the Belgian population. Food Addit Contam A 29:54–65. https://doi.org/10.1080/19440049.2011.627572
Kasti AN, Nikolaki MD, Synodinou KD, Katsas KN, Petsis K, Lambrinou S, Pyrousis IA, Triantafyllou K (2022) The effects of stevia consumption on gut bacteria: friend or foe? Microorganisms 10:744. https://doi.org/10.3390/microorganisms10040744
Kim JE, Kim SY, Lee KW, Lee HJ (2009) Arginine deiminase originating from Lactococcus lactis ssp. lactis American Type Culture Collection (ATCC) 7962 induces G1-phase cell-cycle arrest and apoptosis in SNU-1 stomach adenocarcinoma cells. Brit J Nutr 102:1469–1476. https://doi.org/10.1017/S0007114509990432
Kornienko VY, Minaev MY (2021) An effect of food additives on microbiome. Theor Pract Meat Process 6:259–268. https://doi.org/10.21323/2414-438X-2021-6-3-259-268
Kubica P, Namieśnik J, Wasik A (2015) Determination of eight artificial sweeteners and common Stevia rebaudiana glycosides in non-alcoholic and alcoholic beverages by reversed-phase liquid chromatography coupled with tandem mass spectrometry. Anal Bioanal Chem 407:1505–1512. https://doi.org/10.1007/s00216-014-8355-x
Li D, Kim JM, Jin Z, Zhou J (2008) Prebiotic effectiveness of inulin extracted from edible burdock. Anaerobe 14:29–34. https://doi.org/10.1016/j.anaerobe.2007.10.002
Marco ML, Hill C, Hutkins R, Slavin J, Tancredi DJ, Merenstein D, Sanders ME (2020) Should there be a recommended daily intake of microbes? J Nutr 150:3061–3067. https://doi.org/10.1093/jn/nxaa323
Marcobal AM, Barboza JW, Froehlich JW, Block DE, German JB, Lebrilla CB, Mills DA (2010) Consumption of human milk oligosaccharides by gut-related microbes. J Agr Food Chem 58:5334–5340. https://doi.org/10.1021/jf9044205
Markowiak P, Slizewska K (2017) Effects of probiotics, prebiotics, and synbiotics on human health. Nutrients 9:1021–1039. https://doi.org/10.3390/nu9091021
Mesquita PDL, Afonso RJDCF, Aquino SFD, Leite GDS (2013) Validação de método de cromatografia líquida para a determinação de sete ácidos graxos voláteis intermediários da digestão anaeróbia. Eng Sanit Ambient 18:295–302. https://doi.org/10.1590/S1413-41522013000400001
Mirza SK, Asema UK, Kasim SS (2017) To study the harmful effects of food preservatives on human health. J Med Chem Drug Discov 2:610–616
Moro TMA, Celegatti CM, Pereira APA, Lopes AS, Barbin DF, Pastore GM, Clerici MTPS (2018) Use of burdock root flour as a prebiotic ingredient in cookies. LWT Food Sci Technol 90:540–546. https://doi.org/10.1016/j.lwt.2017.12.059
Oliphant K, Allen-Vercoe E (2019) Macronutrient metabolism by the human gut microbiome: major fermentation by-products and their impact on host health. Microbiome 7:1–15. https://doi.org/10.1186/s40168-019-0704-8
Oriach CS, Robertson RC, Stanton C, Cryan JF, Dinan TG (2016) Food for thought: the role of nutrition in the microbiota-gut–brain axis. Clin Nutr Exp 6:25–38. https://doi.org/10.1016/j.yclnex.2016.01.003
Palmnäs MS, Cowan TE, Bomhof MR, Su J, Reimer RA, Vogel HJ, Hittel DS, Shearer J (2014) Low-dose aspartame consumption differentially affects gut microbiota-host metabolic interactions in the diet-induced obese rat. PloS One 9:109841. https://doi.org/10.1371/journal.pone.0109841
Park BH, Kim IS, Park JK, Zhi Z, Lee HM, Kwon OW, Lee BC (2021) Probiotic effect of Lactococcus lactis subsp. cremoris RPG-HL-0136 on intestinal mucosal immunity in mice. Appl Biol Chem 64:93. https://doi.org/10.1186/s13765-021-00667-6
Pekmez CT, Dragsted LO, Brahe LK (2019) Gut microbiota alterations and dietary modulation in childhood malnutrition–the role of short chain fatty acids. Clin Nutr 38:615–630. https://doi.org/10.1016/j.clnu.2018.02.014
Pepino MY (2015) Metabolic effects of non-nutritive sweeteners. Physiol Behav 152:450–455. https://doi.org/10.1016/j.physbeh.2015.06.024
Puertollano E, Kolida S, Yaqoob P (2014) Biological significance of short-chain fatty acid metabolism by the intestinal microbiome. Curr Opin Clin Nutr Metab Care 17:139–144. https://doi.org/10.1097/mco.0000000000000025
Pylkas AM, Juneja LR, Slavin JL (2005) Comparison of different fibers for in vitro production of short-chain fatty acids by intestinal microflora. J Med Food 8:113–116. https://doi.org/10.1089/jmf.2005.8.113
Quigley EM (2010) Prebiotics and probiotics; modifying and mining the microbiota. Pharmacol Res 61:213–218. https://doi.org/10.1016/j.phrs.2010.01.004
Ranjbar R, Vahdati SN, Tavakoli S, Khodaie R, Behboudi H (2021) Immunomodulatory roles of microbiota-derived short-chain fatty acids in bacterial infections. Biomed Pharmacother 141:111817. https://doi.org/10.1016/j.biopha.2021.111817
Rehman A, Heinsen FA, Koenen ME, Venema K, Knecht H, Hellmig S, Stefan S, Ott SJ (2012) Effects of probiotics and antibiotics on the intestinal homeostasis in a computer controlled model of the large intestine. BMC Microbiol 12:1–10. https://doi.org/10.1186/1471-2180-12-47
Ruiz-Ojeda FJ, Plaza-Díaz J, Sáez-Lara MJ, Gil A (2019) Effects of sweeteners on the gut microbiota: a review of experimental studies and clinical trials. Adv Nutr 10:S31–S48. https://doi.org/10.1093/advances/nmy037
Shariati M, Matin S, Ghanei M, Kalani N (2016) Nitrate, sorbate and benzoate a justification for the conflicting results of epidemiological studies of cancer in nutrition. J Fund Appl Sci 8:2473–2485. https://doi.org/10.4314//jfas.v8i3s.357
Shastry RP, Rekha PD (2021) Bacterial cross talk with gut microbiome and its implications: a short review. Folia Microbiol 66:15–24. https://doi.org/10.1007/s12223-020-00821-5
Soldavini J, Kaunitz JD (2013) Pathobiology and potential therapeutic value of intestinal short-chain fatty acids in gut inflammation and obesity. Digest Dis Sci 58:2756–2766. https://doi.org/10.1007/s10620-013-2744-4
Suez J, Korem T, Zeevi D, Zilberman-Schapira G, Thaiss CA, Maza O, Israeli D, Zmora N, Gilad S, Weinberger A, Kuperman Y, Harmelin A, Kolodkin-Gal I, Shapiro H, Halpern Z, Segal E, Elinav E (2014) Artificial sweeteners induce glucose intolerance by altering the gut microbiota. Nature 514:181–186. https://doi.org/10.1038/nature13793
Thursby E, Juge N (2017) Introduction to the human gut microbiota. Biochem J 474:1823–1836. https://doi.org/10.1042/BCJ20160510
Wong CB, Odamaki T, Xiao JZ (2019) Beneficial effects of Bifidobacterium longum subsp. longum BB536 on human health: modulation of gut microbiome as the principal action. J Funct Foods 54:506–519. https://doi.org/10.1016/j.jff.2019.02.002
Wu W, Fu G, Xuan R, Zhai L, Lu Y, Tang M, Liu J, Zhang C, Chen H, Wang F (2022) Food additive sodium bisulfite induces intracellular imbalance of biothiols levels in NCM460 colonic cells to trigger intestinal inflammation in mice. Toxicol Lett 359:73–83.https://doi.org/10.1016/j.toxlet.2022.01.019
Xiong RG, Zhou DD, Wu SX, Huang SY, Saimaiti A, Yang ZJ, Shang A, Zhao CN, Ry G, Li HB (2022) Health benefits and side effects of short-chain fatty acids. Foods 11:2863. https://doi.org/10.3390/foods11182863
Yardimci BK, Sahin SC, Sever NI, Ozek NS (2022) Biochemical effects of sodium benzoate, potassium sorbate and sodium nitrite on food spoilage yeast Saccharomyces cerevisiae. Biologia 77:547–557. https://doi.org/10.1007/s11756-021-00964-x
Yu Z, Henderson IR, Guo J (2023) Non-caloric artificial sweeteners modulate conjugative transfer of multi-drug resistance plasmid in the gut microbiota. Gut Microbes 15:2157698. https://doi.org/10.1080/19490976.2022.2157698
Yu Z, Guo J (2022) Non-caloric artificial sweeteners exhibit antimicrobial activity against bacteria and promote bacterial evolution of antibiotic tolerance. J Hazard Mater 433:128840. https://doi.org/10.1016/j.jhazmat.2022.128840
Acknowledgements
The authors are thankful for the financial support provided by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, DF, Brazil—financial code 001) and the Coleção de Culturas Tropical for the donation of the bacteria B. longum.
Author information
Authors and Affiliations
Contributions
A.S.L. designed study, performed research, analyzed data, contributed new methods, and wrote the paper. A.E.C.A. contributed new methods, designed study, and wrote the paper. K.I.A.M. analyzed data. A.S. analyzed data and contributed new methods. M.C.T.D. performed research and designed study.
Corresponding author
Ethics declarations
Ethics approval
No ethical approval was required for this study.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
de Souza Lopes, A., Elisabete Costa Antunes, A., Idelça Aires Machado, K. et al. The impact of antimicrobial food additives and sweeteners on the growth and metabolite production of gut bacteria. Folia Microbiol 68, 813–821 (2023). https://doi.org/10.1007/s12223-023-01076-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12223-023-01076-6