Search for Author, Title, Keyword
ORIGINAL ARTICLE
Modulation of Caecal Microbiome in Obese Mice Associated with Administration of Amaranth or Soybean Protein Isolates
 
More details
Hide details
1
IPICYT, Instituto Potosino de Investigación Científica y Tecnológica A.C. Camino a la Presa San José 2055, Lomas 4a sección, San Luis Potosí, S.L.P., 78216 Mexico
 
2
Facultad de Ciencias Químicas, Universidad Autónoma de San Luis Potosí. Av. Dr. Salvador Nava 6, Zona Universitaria, San Luis Potosí, S.L.P., 78210 Mexico
 
 
Submission date: 2018-03-27
 
 
Final revision date: 2018-08-20
 
 
Acceptance date: 2018-10-21
 
 
Online publication date: 2018-11-30
 
 
Publication date: 2018-12-17
 
 
Corresponding author
Ana P. Barba de la Rosa   

IPICYT, Instituto Potosino de Investigación Científica y Tecnológica A.C. Camino a la Presa San José 2055, Lomas 4a sección, San Luis Potosí, S.L.P., 78216 Mexico
 
 
Pol. J. Food Nutr. Sci. 2019;69(1):35-44
 
KEYWORDS
ABSTRACT
Obesity is defined as abnormal or excessive body fat accumulation that may have negative effects on health. Healthy diet induces a balance of gut microbiota, helping in turn to combat this metabolic disorder. Amaranth is well known because of its beneficial properties on health, but its effects on microbiota profile are still unknown. The aim of this study was to analyse the changes of gut microbiota in diet-induced obese mice due to amaranth protein consumption and to compare them with the changes due to soybean protein intake. Male C57BL/6 mice were fed for 8 weeks with regular (RD) or high-fat (HF) diet, without or with complementation with amaranth or soybean protein isolates. Morphological changes in caecum ultrathin sections were measured after hematoxylin/eosin staining. Microbiota was isolated from the caecum and 16S rRNA gene was sequenced. Caecal Short Chain Fatty Acids (SCFAs) were quantified by gas chromatography. The consumption of soybean protein induced the ectopic deposition of fat in the whole intestine while amaranth proteins increased caecal crypt depth and calceiform cells number sustaining its beneficial effect on health. The count of Ruminococcacea family bacteria was increased in mice fed with HF diet, but amaranth proteins intake reduced its abundance. In turn, Lachnospiraceae bacteria abundance decreased in mice fed the Control-HF and amaranth HF diets, but increased in mice fed the soybean diets. In mice fed the RD diets, amaranth induced the abundance of Prevotellaceae, an acetate-producing bacteria. Study results indicate that the modulation of caecal microbiota could be one of the mechanisms by which amaranth exerts its beneficial effects on health.
 
REFERENCES (40)
1.
Aguirre, M., Venema, K. (2015). Does the gut microbiota contribute to obesity? Going beyond the gut feeling. Microorganisms, 3(2), 213–235. https://doi.org/10.3390/microo....
 
2.
Barazzoni, R., Cappellari, G.G., Ragni, M., Nisoli, E. (2018). Insulin resistance in obesity: an overview of fundamental alterations. Eating Weight Disorders, 23(2), 149-157. https://doi.org/10.1007/s40519....
 
3.
Battson, M.L., Lee, D.M., Weir, T.L., Gentile Ch.L. (2018). The gut microbiota as a novel regulator of cardiovascular function and disease. The Journal of Nutritional Biochemistry, 56, 1-15. https://doi.org/10.1016/j.jnut....
 
4.
Beli, E., Yan, Y., Moldovan, L., Vieira, C.P., Gao, R., Duan, Y., Prasad, R., Bhatwadekar, A., White, F.A., Townsend, S., Chan, L., Ryan, C.N., Morton, D., Moldovan, E.G., Chu, F.I., Oudit, G.Y., Gavin Y., Derendorf, H., Adorini, L., Wang, X.X.X., Evans-Molina, C., Mirmira, R.G., Boulton, M.E., Yoder, M.C., Li, Q.H., Levi, M., Busik, J.V., Grant, M.B. (2018). Restructuring of the gut microbiome by intermittent fasting prevents retinopathy and prolongs survival in db/db mice. Diabetes, 67(9), 1867-1979. Doi.org/10.2337/db18-0158. https://doi.org/10.2337/db18-0....
 
5.
Bressani, R., Elias, L.G., González, J.M., Gómez-Brenes, R. (1987). The chemical composition and protein quality of amaranth grain germplasm in Guatemala. Archivos Latinoamericanos de Nutrición, 37(2), 364-377.
 
6.
Cani, P.D., Knauf, C. (2016). How gut microbes talk to organs: The role of endocrine and nervous routes. Molecular Metabolism, 5(9), 743-752. https://doi.org/10.1016/j.molm....
 
7.
Douglass, J.D., Malik, N., Chon, S.H., Wells, K., Zhou, Y.X., Choi, A.S., Joseph, L.B., Storch, J. (2012). Intestinal mucosal triacylglycerol accumulation secondary to decreased lipid secretion in obese and high fat fed mice. Frontiers in Physiology, 3, art. no. 25. https://doi.org/10.3389/fphys.....
 
8.
Escobedo-Moratilla, A., Velarde-Salcedo, A.J., Magana-Hernández, C.V., Barrera-Pacheco, A., Espitia-Rangel, E., Herrera-Estrella, A., Barba de la Rosa, A.P. (2017). Amaranth protein Improves lipid profile and insulin resistance in a diet-induced obese mice model. Journal of Food and Nutrition Research, 5(12), 914-924. https://doi.org/10.12691/jfnr-....
 
9.
Gullan, B., Gullón, P., Tavaria, F., Yánez, R. (2016). Assessment of the prebiotic effect of quinoa and amaranth in the human intestinal ecosystem. Food and Function, 7(9), 3782–3788. https://doi.org/10.1039/C6FO00....
 
10.
Ferrario, C., Statello, R., Carnevali, L., Mancabelli, L., Milani, C., Mangifesta, M., Duranti, S., Lugli, G.A., Jimenez, B., Lodge, S., Viappiani, A., Alessandri, G., Dall'Asta, M., Del Rio, D., Sgoifo, A., van Sinderen, D., Ventura, M., Turroni, F. (2017). How to feed the mammalian gut microbiota: bacterial and metabolic modulation by dietary fibers. Frontiers in Microbiology, 8, art. no. 1749. https://doi.org/10.3389/fmicb.....
 
11.
Gómez-Cardona, E.E., Hernández-Domínguez, E.E., Huerta-Ocampo, J.Á., Jiménez-Islas, H., Díaz-Gois, A., Velarde-Salcedo, J., Barrera-Pacheco, A, Goni-Ochoa, A., Barba de la Rosa, A.P. (2017). Effect of amaranth consumption on diabetes-related biomarkers in patients with diabetes. Diabetes, Obesity & Metabolic Disorders 3, 5–10. [http://www.kenkyugroup.org/art...].
 
12.
Hahnke, S., Maus, I., Wibberg, D., Tomazetto, G., Pühler, A., Klocke, M., Schlüter, A. (2015). Complete genome sequence of the novel Porphyromonadaceae bacterium strain ING2-E5B isolated from a mesophilic lab-scale biogas reactor. Journal of Biotechnology, 193, 34-36. https://doi.org/10.1016/j.jbio....
 
13.
Hedemann, M.S., Theil, P.K., Bach Knudsen, K.E. (2009). The thickness of the intestinal mucous layer in the colon of rats fed various sources of non-digestible carbohydrates is positively correlated with the pool of SCFA but negatively correlated with the proportion of butyric acid in digesta. British Journal of Nutrition, 102(1), 117–125. https://doi.org/10.1017/S00071....
 
14.
Houston, M. (2014). The role of nutrition and nutraceutical supplements in the prevention and treatment of hypertension. World Journal of Cardiology, 6(2), 38-66.. https://doi.org/10.4330/wjc.v6....
 
15.
Hsieh, T.C., Ma, K.H., Chao, A. (2016). iNEXT: An R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods in Ecology and Evolution, 7(12), 1451–1456. https://doi.org/10.1111/2041-2....
 
16.
Jakobsson, H.E., Rodríguez-Pineiro, A.M., Schütte, A., Ermund, A., Boysen, P., Bemark, M., Sommer, F., Bäckhed, F., Hansson, G.C., Johansson, M.E. (2015). The composition of the gut microbiota shapes the colon mucus barrier. EMBO Reports, 16(2), 164-177. https://doi.org/10.15252/embr.....
 
17.
Jiao, N., Baker, S.S., Nugent, C.A., Tsompana, M., Cai, L.T., Wang, Y., Buck, M.J., Genco, R.J., Baker, R.D., Zhu, R.Y., Zhu, L. (2018). Gut microbiome may contribute to insulin resistance and systemic inflammation in obese rodents: a meta-analysis. Physiological Genomics, 50(4), 244-254. https://doi.org/10.1152/physio....
 
18.
Kasubuchi, M., Hasegawa, S., Hiramatsu, T., Ichimura, A., Kimura, I. (2015). Dietary gut microbial metabolites, short-chain fatty acids, and host metabolic regulation. Nutrients, 7(4), 2839–2849. https://doi.org/10.3390/nu7042....
 
19.
Kautz, S., Rubin, B.E.R., Russell, J.A., Moreaua, C.S. (2013). Surveying the microbiome of ants: comparing 454 pyrosequencing with traditional methods to uncover bacterial diversity. Applied and Environmental Microbiology, 79(2), 525–534. https://doi.org/10.1128/AEM.03....
 
20.
Laparra, J.M., Sanz, Y. (2010). Interactions of gut microbiota with functional food components and nutraceuticals. Pharmacological Research, 61(3), 219–225. https://doi.org/10.1016/j.phrs....
 
21.
Li, J., Armstrong, C.L.H., Campbell, W.W. (2016). Effects of dietary protein source and quantity during weight loss on appetite, energy expenditure, and cardio-metabolic responses. Nutrients, 8(2), art. no. 63. doi: 10.3390/nu8020063. https://doi.org/10.3390/nu8020....
 
22.
Magnuson, A., Fouts, J., Booth, A., Foster, M. (2015). Obesity-induced chronic low-grade inflammation?: Gastrointestinal and adipose tissue crosstalk. Integrative Obesity and Diabetes, 1(5), 103-108. https://doi.org/10.15761/IOD.1....
 
23.
Marotz, C.A., Zarrinpar, A. (2016). Treating obesity and metabolic syndrome with fecal microbiota transplantation. Yale Journal of Biology Medicine, 89(3), 383–388.
 
24.
Martirosyan, D.M., Miroshnichenko, L.A., Kulakova, S.N., Pogojeva, A.V, Zoloedov, V.I. (2007). Amaranth oil application for coronary heart disease and hypertension. Lipids in Health and Disease,.6, art. no. 1. doi: 10.1186/1476-511X-6-1. https://doi.org/10.1186/1476-5....
 
25.
OECD. (2015). Organization for Economic Co-operation and Development. Key Facts - Mexico, Update 2014. Obesity and the Economics Prevention: Fit not Fat., 1–5. [https://www.oecd.org/mexico/Ob...].
 
26.
Ravussin, Y., Koren, O., Spor, A., LeDuc, C., Gutman, R., Stombaugh, J., Knight, R., Ley, R.E., Leibel, R.L. (2012). Responses of gut microbiota to diet composition and weight loss in lean and obese mice. Obesity (Silver Spring), 20(4). doi: 10.1038/oby.2011.111. https://doi.org/10.1038/oby.20....
 
27.
Rooks, M.G., Veiga, P., Wardwell-Scott, L.H., Tickle, T., Segata, N., Michaud, M., Gallini, C.A., Beal, C., van Hylckama-Vlieg, J.E.T., Ballal, S.A., Morgan, X.C., Glickman, J.N., Gevers, D., Huttenhower, C., Garrett, W.S. (2014). Gut microbiome composition and function in experimental colitis during active disease and treatment-induced remission. The ISME Journal, 8(7), 1403–1417. https://doi.org/10.1038/ismej.....
 
28.
Salonen, A., Lahti, L., Salojärvi, J., Holtrop, G., Korpela, K., Duncan, S.H., Date, P., Farquharson, F., Johnstone, A.M., Lobley, G.E., Louis, P., Flint, H.J., de Vos, W.M. (2014). Impact of diet and individual variation on intestinal microbiota composition and fermentation products in obese men. The ISME Journal, 8, 2218-2230. https://doi.org/10.1038/ismej.....
 
29.
Schwiertz, A., Taras, D., Schäfer, K., Beijer, S., Bos, N.A., Donus, C., Hardt P.D. (2010). Microbiota and SCFA in lean and overweight healthy subjects. Obesity, 18(1), 190–195. https://doi.org/10.1038/oby.20....
 
30.
Tagliabue, A., Elli, M. (2013). The role of gut microbiota in human obesity: Recent findings and future perspectives. Nutrition, Metabolism and Cardiovascular Diseases, 23(3), 160-168. https://doi.org/10.1016/j.nume....
 
31.
Tomas, J., Mulet, C., Saffarian, A., Cavin, J.B., Ducroc, R., Regnault, B., Tan, C.K., Duszka, K., Burcelin, R., Wahli, W., Sansonetti, P.J., Pédron, T., (2016). High-fat diet modifies the PPAR- pathway leading to disruption of microbial and physiological ecosystem in murine small intestine. Proceedings of the National Academy of Sciences of the United States of America, 113(40), E5934-E5943. https://doi.org/10.1073/pnas.1....
 
32.
Turnbaugh, P.J., Bäckhed, F., Fulton, L., Gordon, J.I. (2008). Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host & Microbe, 3(4), 213–223. https://doi.org/10.1016/j.chom....
 
33.
Tun, H.M., Bridgman, S.L., Chari, R., Field, C.J., Guttman, D.S., Becker, A.B., Mandhane, P.J, Turvey, S.E., Subbarao, P., Sears, M.R., Scott, J.A., Kozyrskyi, A.L. (2018). Roles of birth mode and infant gut microbiota in intergenerational transmission of overweight and obesity from mother to offspring. JAMA Pediatrics, 172(4), 368-377. https://doi.org/10.1001/jamape....
 
34.
Velarde-Salcedo, A.J., Regalado-Rentería, E., Velarde-Salcedo, R., Juárez-Flores, B.I., Barrera-Pacheco, A., de Mejía, E.G., Barba de la Rosa, A.P. (2017). Consumption of amaranth induces the accumulation of the antioxidant protein paraoxonase/arylesterase 1 and modulates dipeptidyl peptidase iv activity in plasma of streptozotocin-induced hyperglycemic rats. Journal of Nutrigenetics and Nutrigenomics, 10, 181–193. https://doi.org/10.1159/000486....
 
35.
Vital, M., Gao, J., Rizzo, M., Harrison, T., Tiedje, J.M. (2015). Diet is a major factor governing the fecal butyrate-producing community structure across Mammalia, Aves and Reptilia. The ISME Journal, 9(4), 834-843. https://doi.org/10.1038/ismej.....
 
36.
WHO, World Health Organization. Obesity and overweight, fact sheet No311, 2016 [http://www.who.int/mediacentre...] (accessed Jul 20, 2017).
 
37.
Wrzosek, L., Miquel, S., Noordine, M.L., Bouet, S., Chevalier-Curt, M.J., Robert, V., Philippe, C., Bridonneau, C., Cherbuy, C., Robbe-Masselot, C., Langella, P., Thomas, M. (2013). Bacteroides thetaiotaomicron and Faecalibacterium prausnitzii influence the production of mucus glycans and the development of goblet cells in the colonic epithelium of a gnotobiotic model rodent. BMC Biology, 11, art. no. 61. https://doi.org/10.1186/1741-7....
 
38.
Zarrinpar, A., Chaix, A., Yooseph, S., Panda, S. (2014). Diet and feeding pattern affect the diurnal dynamics of the gut microbiome. Cell Metabolism, 20(6), 1006-1017. https://doi.org/10.1016/j.cmet....
 
39.
Zeng, H., Ishaq, S.L., Zhao, F.Q., Wright, A.D.G. (2016). Colonic inflammation accompanies an increase of ß-catenin signaling and Lachnospiraceae/Streptococcaceae bacteria in the hind gut of high-fat diet-fed mice. The Journal of Nutritional Biochemistry, 35, 30-36. https://doi.org/10.1016/j.jnut....
 
40.
Zhang, C., Zhang, M.H., Wang, S.Y., Han, R.J., Cao, Y.F., Hua, W.Y., Mao, Y.J., Zhang, X.J., Pang, X.Y., Wei, C.C., Zhao, G.P., Chen, Y., Zhao, L.P. (2010). Interactions between gut microbiota, host genetics and diet relevant to development of metabolic syndromes in mice. The ISME Journal, 4, 232–241. https://doi.org/10.1038/ismej.....
 
 
CITATIONS (10):
1.
The effect of fish and mealworm larvae meals as alternative dietary protein sources on nutrient digestibility and gastrointestinal function in Chinchilla lanigera
Andrzej Gugołek, Janusz Strychalski, Jerzy Juśkiewicz, Ewa Żary-Sikorska
Experimental Animals
 
2.
Effects of manganese and Bacillus subtilis on the reproductive performance, egg quality, antioxidant capacity and gut microbiota of breeding geese during laying period
Yang Wang, Hefei Wang, Baowei Wang, Beibei Zhang, Wenli Li
Poultry Science
 
3.
Pseudocereal grains: Nutritional value, health benefits and current applications for the development of gluten-free foods
Cristina Martínez-Villaluenga, Elena Peñas, Blanca Hernández-Ledesma
Food and Chemical Toxicology
 
4.
Can pseudocereals modulate microbiota by functioning as probiotics or prebiotics?
Aysegul Ugural, Aslı Akyol
Critical Reviews in Food Science and Nutrition
 
5.
Investigations of the maintenance system of the Konik Polski horse and its effects on fecal microbiota activity during the winter and summer seasons
Jerzy Juśkiewicz, Bartosz Fotschki, Joanna Jaworska, Marta Siemieniuch
Animal Science Journal
 
6.
Pseudocereals [Working Title]
Noorazwani Zainol, Harisun Yaakob, Aqila Elia, Abdul Hasmaliana, Karim Abdul, Abang Norulfairuz
 
7.
Utilisation and limitations of pseudocereals (quinoa, amaranth, and buckwheat) in food production: A review
Sara Graziano, Caterina Agrimonti, Nelson Marmiroli, Mariolina Gullì
Trends in Food Science & Technology
 
8.
Amaranth proteins and peptides: Biological properties and food uses
Fan Zhu
Food Research International
 
9.
Protein characteristics, amino acid profile, health benefits and methods of extraction and isolation of proteins from some pseudocereals—a review
Vasundhara Rao, Amrita Poonia
Food Production, Processing and Nutrition
 
10.
Ancient Indian Diet – A Balanced Diet for the Healthy Diversity of Gut Microbiota and Management of Asthma
Monalisa Das, Nooruddin Thajuddin, Sanjib Patra, Megha Pundir
Current Research in Nutrition and Food Science Journal
 
eISSN:2083-6007
ISSN:1230-0322
Journals System - logo
Scroll to top