Naturally Acquired Lactic Acid Bacteria from Fermented Cassava Improves Nutrient and Anti-dysbiosis Activity of Soy Tempeh

Rio Kusuma; Jaka Widada; Emy Huriyati; Madarina Julia

doi:10.3889/oamjms.2021.7540

Authors

Rio Kusuma Department of Nutrition and Health, Faculty of Medicine, Public Health and Nursing, Universitas Gadjah Mada, Yogyakarta, Indonesia; Doctorate Program of Medicine and Health, Faculty of Medicine, Public Health and Nursing, Universitas Gadjah Mada, Yogyakarta, Indonesia https://orcid.org/0000-0003-0762-4361
Jaka Widada Department of Agricultural Microbiology, Faculty of Agriculture, Universitas Gadjah Mada, Yogyakarta, Indonesia
Emy Huriyati Department of Nutrition and Health, Faculty of Medicine, Public Health and Nursing, Universitas Gadjah Mada, Yogyakarta, Indonesia; Doctorate Program of Medicine and Health, Faculty of Medicine, Public Health and Nursing, Universitas Gadjah Mada, Yogyakarta, Indonesia
Madarina Julia Doctorate Program of Medicine and Health, Faculty of Medicine, Public Health and Nursing, Universitas Gadjah Mada, Yogyakarta, Indonesia; Department of Child Health, Faculty of Medicine, Public Health and Nursing, Universitas Gadjah Mada, Yogyakarta, Indonesia

DOI:

https://doi.org/10.3889/oamjms.2021.7540

Keywords:

Diabetes mellitus, Lactic acid bacteria, Tempeh, Gut microbiota, Short-chain fatty acids

Abstract

Introduction: Gut microbiota dysbiosis indicated by increased gram-negative bacteria and reduced Firmicutes-producing short chain fatty acids bacteria has been linked with impairment in glucose metabolism. Tempeh is traditional fermented soy food that can stimulate the growth of beneficial bacteria. In Indonesia, some tempeh was produced by adding acidifier that contains lactic acid bacteria. This process may impact the nutrient and anti-dysbiosis activity of tempeh.

Objectives: To evaluate the impact of acidifier on nutrient and gut microbiota profile of diabetic animal model.

Method: Modified tempeh was made by addition of water extract of fermented cassava. Standard and modified tempeh were subjected to proximate analysis and dietary fibre. Diabetic animals were received standard tempeh or modified tempeh diet replacing 15% and 30% of protein in the diet for 4 weeks of intervention. At the end of experiment, caecal content was collected. Short chain fatty acids and microbiota composition were analysed using 16s rDNA next generation sequencing (NGS).

Result: There is significant different (p<0.05) on fat, protein, water and dietary fibre content between regular soy tempeh and modified tempeh. There is significant different (p<0.05) on serum glucose and short chain fatty acid composition among group. Diabetic animal has low ratio of Firmicutes/Bacteroidetes. Supplementation of both tempeh increased bacterial diversity, Firmicutes /Bacteroidetes ratio and short chain fatty acids producing bacteria.

Conclusion: Addition of naturally occurred lactic acid bacteria from fermented cassava during tempeh processing improved both nutrient and microbiota composition in the gut of diabetes mellitus.

Downloads

Download data is not yet available.

Metrics

Metrics Loading ...

Plum Analytics Artifact Widget Block

References

Punthakee Z, Goldenberg R, Katz P. Definition, classification and diagnosis of diabetes, prediabetes and metabolic syndrome. Can J Diabetes. 2018;42 Suppl 1:S10-5. https://doi.org/10.1016/j.jcjd.2017.10.003 PMid:29650080 DOI: https://doi.org/10.1016/j.jcjd.2017.10.003

Cho NH, Shaw JE, Karuranga S, Huang Y, da Rocha Fernandes JD, Ohlrogge AW, et al. IDF diabetes atlas: Global estimates of diabetes prevalence for 2017 and projections for 2045. Diabetes Res Clin Pract. 2018;138:271-81. https://doi.org/10.1016/j.diabres.2018.02.023 PMid:29496507 DOI: https://doi.org/10.1016/j.diabres.2018.02.023

Saeedi P, Petersohn I, Salpea P, Malanda B, Karuranga S, Unwin N, et al. Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: Results from the international diabetes federation diabetes atlas, 9th edition. Diabetes Res Clin Pract. 2019;157:107843. https://doi.org/10.1016/j.diabres.2019.107843 PMid:31518657 DOI: https://doi.org/10.1016/j.diabres.2019.107843

Boles A, Kandimalla R, Reddy PH. Dynamics of diabetes and obesity: Epidemiological perspective. Biochim Biophys Acta Mol Basis Dis. 2017;1863(5):1026-36. https://doi.org/10.1016/j.bbadis.2017.01.016 PMid:28130199 DOI: https://doi.org/10.1016/j.bbadis.2017.01.016

Grigorescu I, Dumitrascu DL. Implication of gut microbiota in diabetes mellitus and obesity. Acta Endocrinol (Buchar). 2016;12(2):206-14. https://doi.org/10.4183/aeb.2016.206 PMid:31149088 DOI: https://doi.org/10.4183/aeb.2016.206

Harsch I, Konturek P. The role of gut microbiota in obesity and Type 2 and Type 1 diabetes mellitus: New insights into “old” diseases. Med Sci (Basel). 2018;6(2):32. https://doi.org/10.3390/medsci6020032 PMid:29673211 DOI: https://doi.org/10.3390/medsci6020032

Gurung M, Li Z, You H, Rodrigues R, Jump DB, Morgun A, et al. Role of gut microbiota in Type 2 diabetes pathophysiology. EBioMedicine. 2020;51:102590. https://doi.org/10.1016/j.ebiom.2019.11.051 PMid:31901868 DOI: https://doi.org/10.1016/j.ebiom.2019.11.051

Larsen N, Vogensen FK, van den Berg FW, Nielsen DS, Andreasen AS, Pedersen BK, et al. Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One. 2010;5(2):e9085. https://doi.org/10.1371/journal.pone.0009085 PMid:20140211 DOI: https://doi.org/10.1371/journal.pone.0009085

Qin J, Li Y, Cai Z, Li S, Zhu J, Zhang F, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012;490(7418):55-60. https://doi.org/10.1038/nature11450 PMid:23023125 DOI: https://doi.org/10.1038/nature11450

Sun W, Zhang D, Wang Z, Sun J, Xu B, Chen Y, et al. Insulin resistance is associated with total bile acid level in Type 2 diabetic and nondiabetic population: A cross-sectional study. Medicine (Baltimore). 2016;95(10):e2778. https://doi.org/10.1097/MD.0000000000002778 PMid:26962776 DOI: https://doi.org/10.1097/MD.0000000000002778

d’Hennezel E, Abubucker S, Murphy LO, Cullen TW. Total lipopolysaccharide from the human gut microbiome silences toll-like receptor signaling. mSystems. 2017;2(6):e00046-17. https://doi.org/10.1128/mSystems.00046-17 PMid:29152585 DOI: https://doi.org/10.1128/mSystems.00046-17

Houghton D, Hardy T, Stewart C, Errington L, Day CP, Trenell MI, et al. Systematic review assessing the effectiveness of dietary intervention on gut microbiota in adults with Type 2 diabetes. Diabetologia. 2018;61(8):1700-11. https://doi.org/10.1007/s00125-018-4632-0 PMid:29754286 DOI: https://doi.org/10.1007/s00125-018-4632-0

Roubos-van den Hil PJ, Nout MJ, van der Meulen J, Gruppen H. Bioactivity of tempe by inhibiting adhesion of ETEC to intestinal cells, as influenced by fermentation substrates and starter pure cultures. Food Microbiol. 2010;27(5):638-44. https://doi.org/10.1016/j.fm.2010.02.008 PMid:20510782 DOI: https://doi.org/10.1016/j.fm.2010.02.008

Roubos-van den Hil PJ, Dalmas E, Nout MJR, Abee T. Soya bean tempe extracts show antibacterial activity against Bacillus cereus cells and spores. J Appl Microbiol. 2010;109(1):137-45. https://doi.org/10.1111/j.1365-2672.2009.04637.x PMid:20002864 DOI: https://doi.org/10.1111/j.1365-2672.2009.04637.x

Kuligowski M, Jasińska-Kuligowska I, Nowak J. Evaluation of bean and soy tempeh influence on intestinal bacteria and estimation of antibacterial properties of bean tempeh. Pol J Microbiol. 2013;62(2):189-94. PMid:24053022 DOI: https://doi.org/10.33073/pjm-2013-024

Stephanie S, Kartawidjajaputra F, Silo W, Yogiara Y, Suwanto A. Tempeh consumption enhanced beneficial bacteria in the human gut. Food Res. 2018;3(1):57-63. DOI: https://doi.org/10.26656/fr.2017.3(1).230

Huang YC, Wu BH, Chu YL, Chang WC, Wu MC. Effects of Tempeh Fermentation with Lactobacillus plantarum and Rhizopus oligosporus on streptozotocin-induced Type II diabetes mellitus in rats. Nutrients. 2018;10(9):1143. https://doi.org/10.3390/nu10091143 PMid:30135362 DOI: https://doi.org/10.3390/nu10091143

Seumahu CA, Suwanto A, Rusmana I, Solihin DD. Bacterial and fungal communities in tempeh as reveal by amplified ribosomal intergenic sequence analysis. HAYATI J Biosci. 2013;20:65-71. DOI: https://doi.org/10.4308/hjb.20.2.65

Pisol B, Nuraida L, Abdullah N, Suliantari, Khalil KA. Isolation and characterization of lactic acid bacteria from indonesian soybean tempeh. Int Proc Chem Biol Environ Eng. 2013;58:32-6.

Radita R, Suwanto A, Kurosawa N, Wahyudi A, Rusmana I. Metagenome analysis of tempeh production: Where did the bacterial community in tempeh come from? Malaysian J Microbiol. 2017;13(4):280-82. Available from: https://www.semanticscholar.org/paper/metagenome-analysis-of-tempeh-production%3a-where-did-radita-suwanto/7bbf4d74c4b1eaa9374bf29364671bee8f8af6ad [Last accessed on 2021 Jun 23].

Nuraida L. A review: Health promoting lactic acid bacteria in traditional Indonesian fermented foods. Food Sci Hum Wellness. 2015;4:47-55. DOI: https://doi.org/10.1016/j.fshw.2015.06.001

Astriani A, Diniyah N, Jayus J, Nurhayati N. Phenotypic identification of indigenous fungi and lactic acid bacteria isolated from ‘gatot’ an Indonesian fermented food. Biodiversitas J Biol Divers. 2018;19:947-54. DOI: https://doi.org/10.13057/biodiv/d190325

Jati Kusuma R, Ermamilia A. Fortification of tempeh with encapsulated iron improves iron status and gut microbiota composition in iron deficiency anemia condition. Nutr Food Sci. 2018;48:962-72. DOI: https://doi.org/10.1108/NFS-01-2018-0027

Cempaka L, Eliza N, Ardiansyah A, Handoko DD, Astuti RM. Proximate composition, total phenolic content, and sensory analysis of rice bran tempeh. Makara J Sci. 2018;22:89-94. DOI: https://doi.org/10.7454/mss.v22i2.9616

McCleary BV, DeVries JW, Rader JI, Cohen G, Prosky L, Mugford DC, et al. Determination of insoluble, soluble, and total dietary fiber (CODEX Definition) by enzymatic-gravimetric method and liquid chromatography: Collaborative study. J AOAC Int. 2012;95(3):824-44. https://doi.org/10.5740/jaoacint.cs2011_25 PMid:22816275 DOI: https://doi.org/10.5740/jaoacint.CS2011_25

Arifin WN, Zahiruddin WM. Sample size calculation in animal studies using resource equation approach. Malays J Med Sci. 2017;24(5):101-5. https://doi.org/10.21315/mjms2017.24.5.11 PMid:29386977 DOI: https://doi.org/10.21315/mjms2017.24.5.11

Ghasemi A, Khalifi S, Jedi S. Streptozotocin-nicotinamide-induced rat model of type 2 diabetes (review). Acta Physiol Hung. 2014;101(4):408-20. https://doi.org/10.1556/APhysiol.101.2014.4.2 PMid:25532953 DOI: https://doi.org/10.1556/APhysiol.101.2014.4.2

Sivixay S, Bai G, Tsuruta T, Nishino N, Sivixay S, Bai G, et al. Cecum microbiota in rats fed soy, milk, meat, fish, and egg proteins with prebiotic oligosaccharides. AIMS Microbiol. 2021;7(1):1-12. https://doi.org/10.3934/microbiol.2021001 PMid:33659765 DOI: https://doi.org/10.3934/microbiol.2021001

Ahnan‐Winarno AD, Cordeiro L, Winarno FG, Gibbons J, Xiao H. Tempeh: A semicentennial review on its health benefits, fermentation, safety, processing, sustainability, and affordability. Compr Rev Food Sci Food Saf. 2021;20(2):1717-67. https://doi.org/10.1111/1541-4337.12710 PMid:33569911 DOI: https://doi.org/10.1111/1541-4337.12710

Efriwati, Suwanto A, Rahayu G, Nuraida L. Population dynamics of yeasts and lactic acid bacteria (LAB) during tempeh production. HAYATI J Biosci. 2013;20:57-64. DOI: https://doi.org/10.4308/hjb.20.2.57

Yan Y, Wolkers-Rooijackers J, Nout MJ, Han B. Microbial diversity and dynamics of microbial communities during back-slop soaking of soybeans as determined by PCR-DGGE and molecular cloning. World J Microbiol Biotechnol. 2013;29(10):1969-74. https://doi.org/10.1007/s11274-013-1349-6 PMid:23576016 DOI: https://doi.org/10.1007/s11274-013-1349-6

Vig AP, Walia A. Beneficial effects of Rhizopus oligosporus fermentation on reduction of glucosinolates, fibre and phytic acid in rapeseed (Brassica napus) meal. Bioresour Technol. 2001;78(3):309-12. https://doi.org/10.1016/s0960-8524(01)00030-x PMid:11341693 DOI: https://doi.org/10.1016/S0960-8524(01)00030-X

Nurdini AL, Nuraida L, Suwanto A, Suliantari. Microbial growth dynamics during tempe fermentation in two different home industries. Int Food Res J. 2015;22(4):1668-74.

Starzyńska-Janiszewska A, Duliński R, Stodolak B. Fermentation with edible rhizopus strains to enhance the bioactive potential of hull-less pumpkin oil cake. Molecules. 2020;25:5782. DOI: https://doi.org/10.3390/molecules25245782

Yuksekdag Z, Acar BC, Aslim B, Tukenmez U. β-Glucosidase activity and bioconversion of isoflavone glycosides to aglycones by potential probiotic bacteria. Int J Food Prop. 2017;20:S2878-86. DOI: https://doi.org/10.1080/10942912.2017.1382506

Soka S, Suwanto A, Sajuthi D, Rusmana I. Impact of tempeh supplementation on gut microbiota composition in sprague-dawley rats. Res J Microbiol. 2014;9:189-98. DOI: https://doi.org/10.3923/jm.2014.189.198

Guadamuro L, Azcárate-Peril MA, Tojo R, Mayo B, Delgado S. Use of high throughput amplicon sequencing and ethidium monoazide dye to track microbiota changes in an equol-producing menopausal woman receiving a long-term isoflavones treatment. AIMS Microbiol. 2019;5(1):102-16. https://doi.org/10.3934/microbiol.2019.1.102 PMid:31384706 DOI: https://doi.org/10.3934/microbiol.2019.1.102

Vacca M, Celano G, Calabrese FM, Portincasa P, Gobbetti M, de Angelis M. The controversial role of human gut lachnospiraceae. Microorganisms. 2020;8(4):573. https://doi.org/10.3390/microorganisms8040573 PMid:32326636 DOI: https://doi.org/10.3390/microorganisms8040573

Mayo B, Vázquez L, Flórez AB. Equol: A bacterial metabolite from the daidzein isoflavone and its presumed beneficial health effects. Nutrients. 2019;11(9):2231. https://doi.org/10.3390/nu11092231 PMid:31527435 DOI: https://doi.org/10.3390/nu11092231

de Filippo C, Cavalieri D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci USA. 2010;107(33):14691-6. https://doi.org/10.1073/pnas.1005963107 PMid:20679230 DOI: https://doi.org/10.1073/pnas.1005963107

Ruengsomwong S, La-ongkham O, Jiang J, Wannissorn B, Nakayama J, Nitisinprasert S. Microbial community of healthy thai vegetarians and non-vegetarians, their core gut microbiota, and pathogen risk. J Microbiol Biotechnol. 2016;26(10):1723-35. https://doi.org/10.4014/jmb.1603.03057 PMid:27381339 DOI: https://doi.org/10.4014/jmb.1603.03057

Jain A, Li XH, Chen WN. Similarities and differences in gut microbiome composition correlate with dietary patterns of Indian and Chinese adults. AMB Express. 2018;8:104. https://doi.org/10.1186/s13568-018-0632-1 PMid:29936607 DOI: https://doi.org/10.1186/s13568-018-0632-1

Kovatcheva-Datchary P, Nilsson A, Akrami R, Lee YS, de Vadder F, Arora T, et al. Dietary fiber-induced improvement in glucose metabolism is associated with increased abundance of prevotella. Cell Metab. 2015;22(6):971-82. https://doi.org/10.1016/j.cmet.2015.10.001 PMid:26552345 DOI: https://doi.org/10.1016/j.cmet.2015.10.001

Tomova A, Bukovsky I, Rembert E, Yonas W, Alwarith J, Barnard ND, et al. The effects of vegetarian and vegan diets on gut microbiota. Front Nutr. 2019;6:47. https://doi.org/10.3389/fnut.2019.00047 PMid:31058160 DOI: https://doi.org/10.3389/fnut.2019.00047