Altered in vitro metabolomic response of the human microbiota to sweeteners

Genes

Volumn 10, Issue 7, 2019, Pages

  Vamanu, Emanuel ^a   Pelinescu, Diana ^b   Gatea, Florentina ^c   Sârbu, Ionela ^b  

^a UNIVERSITY OF AGRONOMIC SCIENCES AND VETERINARY MEDICINE OF BUCHAREST   (Romania)

^b UNIVERSITY OF BUCHAREST   (Romania)

^c NATIONAL INSTITUTE OF RESEARCH AND DEVELOPMENT FOR BIOLOGICAL SCIENCES   (Romania)

Author keywords

Ammonium; Cyclamate; Dysbiosis; Short chain fatty acids; Steviol

Indexed keywords

AMMONIA; BIOLOGICAL MARKER; CARBOXYLIC ACID; CYCLAMATE SODIUM; SACCHARIN; SHORT CHAIN FATTY ACID; STEVIOL; SWEETENING AGENT; FATTY ACID; KAURANE DERIVATIVE;

ARTICLE; BACTEROIDES; BIFIDOBACTERIUM; CAPILLARY ELECTROPHORESIS; CHEMICAL COMPOSITION; CONTROLLED STUDY; DYSBIOSIS; ENTEROBACTERIACEAE; FEMALE; FERMENTATION TECHNIQUE; HUMAN; LACTOBACILLUS; LACTOCOCCUS; MALE; METABOLOMICS; MICROFLORA; NONHUMAN; PEDIOCOCCUS; PH MEASUREMENT; POLYMERASE CHAIN REACTION; PORPHYROMONAS; PREVOTELLA; QUANTITATIVE ANALYSIS; TEMPERATURE MEASUREMENT; DRUG EFFECT; INTESTINE FLORA; METABOLISM; METABOLOME; METAGENOME; METAGENOMICS; PROCEDURES;

AMMONIA; DITERPENES, KAURANE; DYSBIOSIS; FATTY ACIDS; GASTROINTESTINAL MICROBIOME; HUMANS; METABOLOME; METABOLOMICS; METAGENOME; METAGENOMICS; MICROBIOTA; SWEETENING AGENTS;

EID: 85071368823     PISSN: None     EISSN: 20734425     Source Type: Journal    
DOI: 10.3390/genes10070535     Document Type: Article

References (43)

1. Carocho, M.; Morales, P.; Ferreira, I.C.F.R. Sweeteners as food additives in the XXI century: A review of what is known, and what is to come. Food Chem. Toxicol. 2017, 107, 302–317. [CrossRef] [PubMed]
2. Kreuch, D.; Keating, D.J.; Wu, T.; Horowitz, M.; Rayner, C.K.; Young, R.L. Gut mechanisms linking intestinal sweet sensing to glycemic control. Front. Endocrinol. 2018, 9, 741. [CrossRef] [PubMed]
3. Bian, X.; Chi, L.; Gao, B.; Tu, P.; Ru, H.; Lu, K. The artificial sweetener acesulfame potassium affects the gut microbiome and body weight gain in CD-1 mice. PLoS ONE 2017, 12, e0178426. [CrossRef] [PubMed]
4. Ghaisas, S.; Maher, J.; Kanthasamy, A. Gut microbiome in health and disease: Linking the microbiome-gut-brain axis and environmental factors in the pathogenesis of systemic and neurodegenerative diseases. Pharmacol. Ther. 2016, 158, 52–62. [CrossRef] [PubMed]
5. Pistollato, F.; Sumalla Cano, S.; Elio, I.; Masias Vergara, M.; Giampieri, F.; Battino, M. Role of gut microbiota and nutrients in amyloid formation and pathogenesis of Alzheimer disease. Nutr. Rev. 2016, 74, 624–634. [CrossRef] [PubMed]
6. Ruiz-Ojeda, F.J.; Plaza-Díaz, J.; Sáez-Lara, M.J.; Gil, A. Effects of sweeteners on the gut microbiota: A review of experimental studies and clinical trials. Adv. Nutr. 2019, 10, S31–S48. [CrossRef] [PubMed]
7. Aw, W.; Fukuda, S. Toward the comprehensive understanding of the gut ecosystem via metabolomics-based integrated omics approach. Semin. Immunopathol. 2015, 37, 5–16. [CrossRef] [PubMed]
8. Stanhope, K.L.; Schwarz, J.M.; Keim, N.L.; Griffen, S.C.; Bremer, A.A.; Graham, J.L.; Hatcher, B.; Cox, C.L.; Dyachenko, A.; Zhang, W.; et al. Consuming fructose-sweetened, not glucosesweetened, beverages increases visceral adiposity and lipids and decreases insulin sensitivity in overweight/obese humans. J. Clin. Invest. 2009, 119, 1322–1334. [CrossRef] [PubMed]
9. Vamanu, E.; Pelinescu, D.; Sarbu, I. Comparative fingerprinting of the human microbiota in diabetes and cardiovascular disease. J. Med. Food 2016, 19, 1188–1195. [CrossRef]
10. Cárdenas-Castroa, A.P.; Bianchib, F.; Tallarico-Adornoc, M.A.; Montalvo-Gonzáleza, E.; Sáyago-Ayerdia, S.G.; Sivieri, K. In vitro colonic fermentation of Mexican “taco” from corn-tortilla and black beans in a simulator of human microbial ecosystem (SHIME®) system. Food Res. Int. 2019, 118, 81–88. [CrossRef]
11. Umu, Ö.C.O.; Rudi, K.; Diep, D.B. Modulation of the gut microbiota by prebiotic fibers and bacteriocins. Microb. Ecol. Health Dis. 2017, 28, 1348886. [CrossRef] [PubMed]
12. Kubica, P.; Namieśnik, J.; Wasik, A. 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. 2014, 407, 1505–1512. [CrossRef] [PubMed]
13. Vamanu, E.; Pelinescu, D.; Avram, I. Antioxidative effects of phenolic compounds of mushrooms mycelia in simulated regions of the human colon, in vitro study. Pol. J. Food Nutr. Sci. 2018, 68, 83–90. [CrossRef]
14. Vamanu, E.; Gatea, F.; Sârbu, I. In vitro ecological response of the human gut microbiome to bioactive extracts from edible wild mushrooms. Molecules 2018, 23, 2128. [CrossRef] [PubMed]
15. Ketabi, A.; Dieleman, L.A.; Ganzle, M.G. Influence of isomalto-oligosaccharides on intestinalmicrobiota in rats. J. Appl. Micro. 2011, 110, 1297–1306. [CrossRef] [PubMed]
16. Rinttilä, T.; Kassinen, A.; Malinen, E.; Krogius, L.; Palva, A. Development of an extensive set of 16S rDNA-targeted primers for quantification of pathogenic and indigenous bacteria in faecal samples by real-time PCR. J. Appl. Microbiol. 2004, 97, 1166–1177. [CrossRef] [PubMed]
17. Bacchetti De Gregoris, T.; Aldred, N.; Clare, A.S.; Burgess, J.G. Improvement of phylum-and class-specific primers for real-time PCR quantification of bacterial taxa. J. Microbiol. Methods 2011, 86, 351–356. [CrossRef]
18. Gatea, F.; Teodor, E.D.; Paun, G.; Matei, A.O.; Radu, G.L. Capillary electrophoresis method validation for organic acids assessment in probiotics. Food Anal. Methods 2015, 8, 1335–1340. [CrossRef]
19. Truică, G.I.; Teodor, E.D.; Radu, G.L. Organic acids assessments in medicinal plants by capillary electrophoresis. Rev. Roum. Chim. 2013, 58, 809–814.
20. De la Cuesta-Zuluaga, J.; Mueller, N.T.; Álvarez-Quintero, R.; Velásquez-Mejía, E.P.; Sierra, J.A.; Corrales-Agudelo, V.; Carmona, J.A.; Abad, J.M.; Escobar, J.S. Higher fecal short-chain fatty acid levels are associated with gut microbiome dysbiosis, obesity, hypertension and cardiometabolic disease risk factors. Nutrients 2019, 11, 51. [CrossRef]
21. Ktsoyan, Z.A.; Mkrtchyan, M.S.; Zakharyan, M.K.; Mnatsakanyan, A.A.; Arakelova, K.A.; Gevorgyan, Z.U.; Sedrakyan, A.M.; Hovhannisyan, A.I.; Arakelyan, A.A.; Aminov, R.I. Systemic concentrations of short chain fatty acids are elevated in salmonellosis and exacerbation of familial mediterranean fever. Front. Microbiol. 2016, 7, 776. [CrossRef] [PubMed]
22. Beloborodova, N.; Bairamov, I.; Olenin, A.; Shubina, V.; Teplova, V.; Fedotcheva, N. Effect of phenolic acids of microbial origin on production of reactive oxygen species in mitochondria and neutrophils. J. Biomed. Sci. 2012, 19, 89. [CrossRef] [PubMed]
23. Beloborodova, N.V.; Bairamov, I.T.; Olenin, A.Y.; Khabib, O.N.; Fedotcheva, N.I. Anaerobic microorganisms from human microbiota produce species-specific exometabolites important in heath and disease. Glob. J. Pathol. Microbiol. 2013, 1, 43–53. [CrossRef]
24. Chaudhari, S.S.; Gokhale, D.V. Phenyllactic acid: A potential antimicrobial compound in lactic acid bacteria. J. Bacteriol. Mycol. 2016, 2, 121–125. [CrossRef]
25. Yusuf, F.; Adewiah, S.; Syam, A.F.; Fatchiyah, F. Altered profile of gut microbiota and the level short chain fatty acids in colorectal cancer patients. J. Phys. Conf. Ser. 2019, 1146, 012037. [CrossRef]
26. Kindt, A.; Liebisch, G.; Clavel, T.; Haller, D.; Hörmannsperger, G.; Yoon, H.; Kolmeder, D.; Sigruener, A.; Krautbauer, S.; Seeliger, C.; et al. The gut microbiota promotes hepatic fatty acid desaturation and elongation in mice. Nat. Commun. 2018, 14, 3760. [CrossRef] [PubMed]
27. Bian, X.; Chi, L.; Gao, B.; Tu, P.; Ru, H.; Lu, K. Gut microbiome response to sucralose and its potential role in inducing liver inflammation in mice. Front. Physiol. 2017, 8, 487. [CrossRef]
28. Sharma, A.; Amarnath, S.; Thulasimani, M.; Ramaswamy, S. Artificial sweeteners as a sugar substitute: Are they really safe? Indian J. Pharmacol. 2016, 48, 237–240. [CrossRef]
29. Suez, J.; Korem, T.; Zeevi, D.; Zilberman-Schapira, G.; Thaiss, C.A.; Maza, O.; Israeli, D.; Zmora, N.; Gilad, S.; Weinberger, A.; et al. Artificial sweeteners induce glucose intolerance by altering the gut microbiota. Nature 2014, 514, 181–186. [CrossRef]
30. Kunová, G.; Rada, V.; Vidaillac, A.; Lisova, I. Utilisation of steviol glycosides from Stevia rebaudiana (Bertoni) by lactobacilli and bifidobacteria in in vitro conditions. Folia Microbiol. 2014, 59, 251–255. [CrossRef]
31. Farup, P.G.; Rudi, K.; Hestad, K. Faecal short-chain fatty acids—A diagnostic biomarker for irritable bowel syndrome? BMC Gastroenterol. 2016, 16, 51. [CrossRef] [PubMed]
32. Magnuson, B.A.; Carakostas, M.C.; Moore, N.H.; Poulos, S.P. Renwick AG biological fate of low-calorie sweeteners. Nutr. Rev. 2016, 74, 670–689. [CrossRef] [PubMed]
33. Uebanso, T.; Ohnishi, A.; Kitayama, R.; Yoshimoto, A.; Nakahashi, M.; Shimohata, T.; Mawatari, K.; Takahashi, A. Effects of low-dose non-caloric sweetener consumption on gut microbiota in mice. Nutrients 2017, 9, 560. [CrossRef] [PubMed]
34. Denina, I.; Semjonovs, P.; Fomina, A.; Treimane, R.; Linde, R. The influence of stevia glycosides on the growth of Lactobacillus reuteri strains. Lett. Appl. Microbiol. 2014, 58, 278–284. [CrossRef] [PubMed]
35. Mansoorian, B.; Combet, E.; Alkhaldy, A.; Garcia, A.L.; Edwards, C.A. Impact of fermentable fibers on the colonic microbiota metabolism of dietary polyphenols rutin and quercetin. Int. J. Environ. Res. Pub. Health 2019, 16, 292. [CrossRef] [PubMed]
36. Rizzo, B.; Zambonin, L.; Angeloni, C.; Leoncini, E.; Dalla Sega, F.V.; Prata, C.; Fiorentini, D.; Hrelia, S. Steviol glycosides modulate glucose transport in different cell types. Oxid. Med. Cell. Longev. 2013, 2013, 348169. [CrossRef] [PubMed]
37. Kasubuchi, M.; Hasegawa, S.; Hiramatsu, T.; Ichimura, A.; Kimura, I. Dietary gut microbial metabolites, short-chain fatty acids, and host metabolic regulation. Nutrients 2015, 7, 2839–2849. [CrossRef] [PubMed]
38. Roduit, C.; Frei, R.; Ferstl, R.; Loeliger, S.; Westermann, P.; Rhyner, C.; Schiavi, E.; Barcik, W.; Rodriguez-Perez, N.; Wawrzyniak, M.; et al. High levels of butyrate and propionate in early life are associated with protection against atopy. Allergy 2018, 74, 799–809. [CrossRef]
39. Ceunen, S.; Geuns, J.M.C. Steviol glycosides: Chemical diversity, metabolism, and function. J. Nat. Prod. 2013, 766, 1201–1228. [CrossRef]
40. Murakami, S.; Goto, Y.; Ito, K.; Hayasaka, S.; Kurihara, S.; Soga, T.; Tomita, M.; Fukuda, S. The consumption of bicarbonate-rich mineral water improves glycemic control. Evid. Based Complement. Alt. Med. 2015, 2015, 10. [CrossRef]
41. DuBois, G.E.; Prakash, I. Non-caloric sweeteners, sweetness modulators, and sweetener enhancers. Annu. Rev. Food Sci. Technol. 2012, 3, 353–380. [CrossRef] [PubMed]
42. Harpaz, D.; Yeo, L.P.; Cecchini, F.; Koon, T.H.P.; Kushmaro, A.; Tok, A.I.Y.; Marks, R.S.; Eltzov, E. Measuring artificial sweeteners toxicity using a bioluminescent bacterial panel. Molecules 2018, 23, 2454. [CrossRef] [PubMed]
43. Wang, Q.P.; Browman, D.; Herzog, H.; Neely, G.G. Non-nutritive sweeteners possess a bacteriostatic effect and alter gut microbiota in mice. PLoS ONE 2018, 13, e0199080. [CrossRef]