Abstract
Probiotic bacteria are now becoming an effective natural medicine for alleviating many non-communicable lifestyle-related diseases. The present study was conducted to evaluate the antioxidant and antitoxicant properties of a foodborne probiotic Bifidobacterium sp. MKK4 and its rice fermented beverage. The extracts of culture broth, whole cells, fermented beverage, and it’s heat-inactivated counterparts subjected to in vitro antioxidant/antiradical assays by DPPH, ABTS, and FRAP analysis. Except for heat-inactivated states, all samples exhibited strong antioxidant activity. In the experimental rat model, both Bifidobacterium sp. MKK4 and its rice fermented beverage significantly prevented arsenic toxicity by inducing a higher level of superoxide dismutase (SOD), catalase (CAT), reduced glutathione and preventing lipid peroxidation (LPO) and DNA fragmentation, and transmembrane mitochondrial potential. Besides, the organism supported systematic protection by improving the level of serum glutamate oxaloacetate transaminase, glutamate pyruvate transaminase, alkaline phosphatase, lactate dehydrogenase, C-reactive protein, urea, creatinine, and uric acid. The inherent antioxidant nature of the isolate can be exploited as an ingredient in functional food and an effective antidote against arsenic toxicity.
Similar content being viewed by others
Availability of data and material
The authors confirm that the data supporting the findings of this study are available within the article.
Code availability
The datasets generated during the current study are available from the corresponding author on reasonable request.
References
Acharyya N, Sajed Ali S, Deb B, Chattopadhyay S, Maiti S (2015) Green tea (Camellia sinensis) alleviates arsenic-induced damages to DNA and intestinal tissues in rat and in situ intestinal loop by reinforcing antioxidant system. Environ Toxicol 30:1033–1044. https://doi.org/10.1002/tox.21977
Aebi HE (1984) Catalase in vitro. Methods Enzym 105:121–126
Banik A, Mondal J, Rakshit S, Ghosh K, Sha SP, Halder SK, Ghosh C, Mondal KC (2019) Amelioration of cold-induced gastric injury by a yeast probiotic isolated from traditional fermented foods. J Funct Foods 59:164–173
Chattopadhyay S, Khatun S, Maity M, Jana S, Perveen H, Dash M, Dey A, Jana LR, Maity PP (2019) Association of vitamin B12, lactate dehydrogenase, and regulation of NF-κB in the mitigation of sodium arsenite-induced ROS generation in uterine tissue by commercially available probiotics. Probiotics Antimicro Proteins 11:30–42. https://doi.org/10.1007/s12602-017-9333-3
Coryell M, Roggenbeck BA, Walk ST (2019) The human gut microbiome’s influence on arsenic toxicity. Curr pharmacol Rep 5:491–504. https://doi.org/10.1007/s40495-019-00206-4
Dash SK, Ghosh T, Roy S, Chattopadhyay S, Das D (2014) Zinc sulfide nanoparticles selectively induce cytotoxic and genotoxic effects on leukemic cells: involvement of reactive oxygen species and tumor necrosis factor alpha. J Appl Toxicol 34:1130–1144. https://doi.org/10.1002/jat.2976
Ghosh K, Ray M, Adak A, Dey P, Halder SK, Das A, Jana A, Parua S, Mohapatra PKD, Pati BR (2015) Microbial, saccharifying and antioxidant properties of an Indian rice based fermented beverage. Food Chem 168:196–202. https://doi.org/10.1016/j.foodchem.2014.07.042
Halder SK, Jana A, Das A, Paul T, Mohapatra PKD, Pati BR, Mondal KC (2014) Appraisal of antioxidant, anti-hemolytic and DNA shielding potentials of chitosaccharides produced innovatively from shrimp shell by sequential treatment with immobilized enzymes. Food Chem 158:325–334. https://doi.org/10.1016/j.foodchem.2014.02.115
Hor PK, Ray M, Pal S, Ghosh K, Soren JP, Maiti S, Bera D, Singh S, Dwivedi S, Tako M, Das Mohapatra PK, Mondal KC (2019) Some functional properties of Khambir, an ethnic fermented cereal based of western Himalayas. Front Microbiol 10:730. https://doi.org/10.3389/fmicb.2019.00730
Ighodaro OM, Akinloye OA (2018) First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): their fundamental role in the entire antioxidant defence grid. Alexandria J Med 54:287–293. https://doi.org/10.1016/j.ajme.2017.09.001
Jan G, Leverrier P, Proudy I, Roland N (2002) Survival and beneficial effects of propionibacteria in the human gut: in vivo and in vitro investigations. LeLait 82:131–144. https://doi.org/10.1051/lait:2001012
Jollow DJ, Mitchell JR, Zampaglione NA, Gillette JR (1974) Bromobenzene-induced liver necrosis. Protective role of glutathione and evidence for 3,4-bromobenzene oxide as the hepatotoxic metabolite. Pharmacol 11:151–169. https://doi.org/10.1159/000136485
Kau AL, Ahern PP, Griffin NW, Goodman AL, Gordon JI (2012) Human nutrition, the gut microbiome, and the immune system: envisioning the future. Nature 474:327–336. https://doi.org/10.1038/nature10213
Kleniewska P, Pawliczak R (2017) Influence of synbiotics on selected oxidative stress parameters. Oxid Med Cell Longev. https://doi.org/10.1155/2017/9315375
Lin MY, Chang FJ (2000) Antioxidative effect of intestinal bacteria Bifidobacterium longum ATCC 15708 and Lactobacillus acidophilus ATCC 4356. Dig Dis Sci 45:1617–1622. https://doi.org/10.1023/a:1005577330695
Lobo V, Patil A, Phatak A, Chandra N (2010) Free radicals, antioxidants and functional foods: impact on human health. Pharmacogn Rev 4:118–126
Mandal A, Paul T, Roy S, Mandal S, Pradhan S, Das K, Mondal K, Nandi D (2013) Therapeutic potential of Lactobacillus ingluviei ADK10, a newly established probiotic organism against acetaminophen induced uremic rats. Biologia 68:1072–1078
Mikelsaar M, Zilmer M (2009) Lactobacillus fermentum ME-3–an antimicrobial and antioxidative probiotic. Microb Ecol Health Dis 21:1–27. https://doi.org/10.1080/08910600902815561
Mishra V, Shah C, Mokashe N, Chavan R, Yadav H, Prajapati J (2015) Probiotics as potential antioxidants: a systematic review. J Agric Food Chem 63:3615–3626. https://doi.org/10.1021/jf506326t
Pal S, Chatterjee AK (2006) Possible beneficial effects of melatonin supplementation on arsenic-induced oxidative stress in wistar rats. Drug Chem Toxicol 29:423–433. https://doi.org/10.1080/01480540600837993
Patra A, Mandal S, Samanta A, Mondal KC, Nandi DK (2018) Therapeutic potential of probiotic Lactobacillus plantarum AD3 on acetaminophen induced uremia in experimental rats. Clin Nutr Exp 19:12–22
Pham-Huy LA, He H, Pham-Huy C (2008) Free radicals, antioxidants in disease and health. Int J Biomed Sci 4:89–96
Phaniendra A, Jestadi DB, Periyasamy L (2015) Free radicals: properties, sources, targets, and their implication in various diseases. Ind J Clin Biochem 30:11–26
Ray M, Ghosh K, Har PK, Singh SN, Mondal KC (2017) Fortification of rice gruel into functional beverage and establishment as a carrier of newly isolated Bifidobacterium sp. MKK4. Res J Microbiol 12:102–117
Ray M, Ghosh K, Har PK, Ojha D, Soren JP, Singh SN, Mondal KC (2018) Bifidobacteria and its rice fermented products on diet induced obese mice: analysis of physical status, serum profile and gene expressions. Benef Microbes 9:441–452
Sharma A, Bruce KL, Chen B, Gyoneva S, Behrens SH, Bommarius AS, Chernoff YO (2016) Contributions of the prion protein sequence, strain, and environment to the species barrier. J Biol Chem 291:1277–1288. https://doi.org/10.1074/jbc.M115.684100
Shen Q, Shang N, Li P (2011) In vitro and in vivo antioxidant activity of Bifidobacterium animalis 01 isolated from centenarians. Curr Microbiol 62:1097–1103. https://doi.org/10.1007/s00284-010-9827-7
Shila S, Subathra M, Devi MA, Panneerselvam C (2005) Arsenic intoxication-induced reduction of glutathione level and of the activity of related enzymes in rat brain regions: reversal by dl-α-lipoic acid. Arch Toxicol 79:140–146
Sinha D, Prasad P (2020) Health effects inflicted by chronic low-level arsenic contamination in groundwater: a global public health challenge. J Appl Toxicol 40:87–131. https://doi.org/10.1002/jat.3823
Sun J, Hu XL, Le GW, Shi YH (2013) Inhibition of Fe-induced colon oxidative stress by Lactobacilli in mice. World J Microbiol Biotechnol 29:209–216. https://doi.org/10.1007/s11274-012-1172-5
Thorat ID, Jagtap DD, Mohapatra D, Joshi DC, Sutar RF, Kapdi SS (2013) Antioxidants, their properties, uses in food products and their legal implications. Int J Food Stud 2:81–104. https://doi.org/10.7455/ijfs/2.1.2013.a7
Wang Y, Wu Y, Wang Y, Xu H, Mei X, Yu D, Wang Y, Li W (2017) Antioxidant properties of probiotic bacteria. Nutrients 9:521. https://doi.org/10.3390/nu9050521
Wei W, McCusker JH, Hyman RW, Jones T, Ning Y, Cao Z, Gu Z, Bruno D, Miranda M, Nquyen M, Wilhelmy J, Komp C, Tamse R, Wang X, Jia P, Luedi P, Oefner PJ, David L, Dietrich FS, Li Y, Davis RW, Steinmetz LM (2007) Genome sequencing and comparative analysis of Saccharomyces cerevisiae strain YJM789. Proc Natl Acad Sci USA 104:12825–12830. https://doi.org/10.1073/pnas.0701291104
Wright JR, Colby HD, Miles PR (1981) Cytosolic factors which affect microsomal lipid peroxidation in lung and liver. Arch Biochem Biophys 206:296–304. https://doi.org/10.1016/0003-9861(81)90095-3
Zarrati M, Salehi E, Nourijelyani K, Mofid V, Zadeh MJ, Najafi F, Ghaflati Z, Bidad K, Chamari M, Karimi M, Shidfar F (2014) Effects of probiotic yogurt on fat distribution and gene expression of proinflammatory factors in peripheral blood mononuclear cells in overweight and obese people with or without weight-loss diet. J Am Coll Nutr 33:417–425. https://doi.org/10.1080/07315724.2013.874937
Zhang Y, Li L, Guo C, Mu D, Feng B, Zuo X, Li Y (2016) Effects of probiotic type, dose and treatment duration on irritable bowel syndrome diagnosed by Rome III criteria: a meta-analysis. BMC Gastroenterol 16:62. https://doi.org/10.1186/s12876-016-0470-z
Acknowledgements
The authors are thankful to the Department of Science and Technology, Government of West Bengal, West Bengal, India for financial assistance [1169(Sanc.)/ST/P/S&T/1G-12/2015] for fellowships and funding. However, funder had no role in experimental designing or in manuscript preparation.
Funding
Department of Science and Technology, Government of West Bengal, West Bengal, India for financial assistance [1169(Sanc.)/ST/P/S&T/1G-12/2015] for fellowships and funding.
Author information
Authors and Affiliations
Contributions
The trial was conceived by MR and PH. KM designed the study. MR and PH conducted the research. SS and KM prepared the manuscript. KM had the primary responsibility of the final content. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Ethical approval
The animal experiment was carried out by taken Vidyasagar University Animal Ethical clearance (ICE/7-8/6-8/16 dt. 26.08.2016).
Consent to participate
Not applicable (as experiments carried out with experimental animal by taking appropriate ethical clearance).
Consent for publication
All authors given the consent for preparation of this manuscript and submission to JFST for publication. The manuscript contains only experimental data/results.
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
Ray, M., Hor, P., Singh, S.N. et al. Multipotent antioxidant and antitoxicant potentiality of an indigenous probiotic Bifidobacterium sp. MKK4. J Food Sci Technol 58, 4795–4804 (2021). https://doi.org/10.1007/s13197-021-04975-z
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13197-021-04975-z