Bacterial endosymbiont inhabiting Leucaena leucocephala leaves and their antioxidant and antidiabetic potential
-
Sridevi Chigurupati
, Shantini Vijayabalan
, Kesavanarayanan Krishnan Selvarajan
, Ahmad Alhowail
and Fatema Kauser
Abstract
Objectives
Research on endosymbionts is emerging globally and is considered as a potential source of bioactive phytochemicals. The present study examines the antioxidant and antidiabetic of the endophytic crude extract isolated from Leucaena leucocephala leaves.
Methods
Endophytic bacteria were isolated from the leaves of L. leucocephala and 16S rRNA gene sequencing was used to establish their identity. The in vitro antioxidant effect of endophytic crude extract (LL) was evaluated using 2-diphenyl-1-picrylhydrazyl (DPPH) and 2, 2′-azino-bis-3-ethylbenzthiazoline-6-sulphonic acid (ABTS) free radical scavenging methods. The in vitro antidiabetic properties of LL were evaluated using α-amylase and α-glucosidase enzyme inhibition assay.
Results
The isolated endophytic bacteria were identified as Cronobacter sakazakii. LL displayed potent free radical scavenging effect against ABTS and DPPH radicals with an inhibitory concentration 50% (IC50) value of 17.49 ± 0.06 and 11.3 ± 0.1 μg/mL respectively. LL exhibited α-amylase and α-glucosidase inhibition with an IC50 value of 23.3 ± 0.08 and 23.4 ± 0.1 μg/mL respectively compared to the standard drug (acarbose). Both glucose loaded normoglycemic rats and STZ induced diabetic rats treated with LL (200 mg/kg) exhibited a considerable reduction in blood glucose levels p<0.01 after 8 h of treatment when compared to normal and diabetic control rats respectively.
Conclusions
Thus, the study shows that LL has a wellspring of natural source of antioxidants, and antidiabetic agents and phytoconstituents present in endophytes could be the rich source for bioactive compounds.
Acknowledgments
The authors are thankful to the Deanship of Scientific Research, Qassim University for funding publication of this project.
Research funding: None.
Author contributions: SC: designed the study and wrote the manuscript; SV: collected literature, performed the study; KKS: Analyzed the data; SC, AA, and FK: performed the in vitro antioxidant and antidiabetic assays.
Competing interests: All the authors ensure that no conflict of interest is present concerning the authorship or any other matters about this manuscript.
Ethical approval: Research involving animals complied with all relevant national regulations and institutional policies (AIMST University Human and Animal Ethical Committee, Malaysia) for the care and use of animals. (AUHAEC13/FOP/2017).
References
1. Lim, TK Edible medicinal and non-medicinal plants: fruits. Springer Netherlands; 2012, vol 2:757–59 pp.10.1007/978-94-007-4053-2Search in Google Scholar
2. Chowtivannakul, P, Srichaikul, B, Talubmook, C. Antidiabetic and antioxidant activities of seed extract from Leucaena leucocephala (Lam.) de Wit. Agric Nat Resour 2016;50:357–61. https://doi.org/10.1016/j.anres.2016.06.007.Search in Google Scholar
3. Syamsudin, D, Simanjuntak, SP. The effects of Leucaena leucocephala (lmk) De Wit seeds on blood sugar levels: an experimental study. Int J Sci Res 2006;2:49–52.Search in Google Scholar
4. Kumar, N, Chaiyasut, C. Health promotion potential of vegetables cultivated in Northern Thailand: a preliminary screening of tannin and flavonoid contents, 5α- reductase inhibition, astringent activity, and antioxidant activities. Evid Base Compl Alternative Med 2017;22:573–79. https://doi.org/10.1177/2156587216686689.Search in Google Scholar
5. Sumarny, R, Simanjuntak, P. Antidiabetic activity of active fractions of Leucaena leucocephala (lmk) Dewit seeds in experiment model. Eur J Sci Res 2010;43:384–91.Search in Google Scholar
6. Agrawal, A, Garg, S, Misra, P, Jafri, S. Leucaena leucocephala (Subabul) as an economic pulpwood. Indian For 1985;111:505–16.Search in Google Scholar
7. Broom, DM, Galindo, FA, Murgueitio, E. Sustainable, efficient livestock production with high biodiversity and good welfare for animals. Proc Biol Sci 2013;280:20132025. https://doi.org/10.1098/rspb.2013.2025.Search in Google Scholar
8. Ulloa, WJ. Isolation of mimosine-degrading endophytic bacteria from the invasive plant: Leucaena leucocephala [Master’s ]. Hilo: University of Hawai’I; 2016. Available from: https://pdfs.semanticscholar.org/f80e/f6277831b259f53bdd8944de260b4a4f4cdd.pdf.Search in Google Scholar
9. Kumar, R, Sharma, P, Bamal, A, Sushma, N, Savita, C. A safe, efficient and environment-friendly biosynthesis of silver nanoparticles using Leucaena leucocephala seed extract and its antioxidant, antimicrobial, antifungal activities and potential in sensing. Green Process Synth 2017;6:449–59. https://doi.org/10.1515/gps-2016-0146.Search in Google Scholar
10. Netala, VR, Kotakadi, VS, Bobbu, P, Gaddam, SA, Tartte, V. Endophytic fungal isolate mediated biosynthesis of silver nanoparticles and their free radical scavenging activity and antimicrobial studies. 3 Biotech 2016;6:132–41. https://doi.org/10.1007/s13205-016-0433-7.Search in Google Scholar
11. Dasa, I, Pandaa, MK, Rathb, CC, Tayungc, K. Bioactivities of bacterial endophytes isolated from leaf tissues of Hyptis suaveolens against some clinically significant pathogens. J Appl Pharmaceut Sci 2017;7:131–36. https://doi.org/10.7324/JAPS.2017.70818.Search in Google Scholar
12. Chigurupati, S, Mohammad, JI, Selvarajan, KK, Vijayabalan, S, Thanasegaran, SA, Lim, YT, et al.. Cronobacter sakazakii strain AIMST. LiLe1 16S ribosomal RNA gene, partial cds. GenBank; 2017. Accession Number: MF615206. https://www.ncbi.nlm.nih.gov/nuccore/MF615206.1.Search in Google Scholar
13. Ramasamy, K, Lim, SM, Bakar, HA, Ismail, N, Ismail, MS, Ali, MF, et al.. Antimicrobial and cytotoxic activities of Malaysian endophytes. Phytother Res 2010;24:640–43. https://doi.org/10.1002/ptr.2891.Search in Google Scholar
14. Chigurupati, S, Vijayabalan, S, Karunanidhi, A, Selvarajan, KK, Nanda, SS, Satpathy, R. Antidiabetic, antioxidant and in silico studies of bacterial endosymbiont inhabiting Nephelium lappaceum L. Ovidius Univ Ann Chem 2019;30:95–100. https://doi.org/10.2478/auoc-2019-0017.Search in Google Scholar
15. Chigurupati, S, Aladhadh, HS, Alhowail, A, Selvarajan, KK, Bhatia, S. Phytochemical composition, antioxidant and antidiabetic potential of methanolic extract from Corchorus olitorius Linn. grown in Saudi Arabia. Med Plants Int J Phytomed Relat Ind 2020;12:71–6. https://doi.org/10.5958/0975-6892.2020.00010.6.Search in Google Scholar
16. Chigurupati, S, Selvaraj, M, Mani, V, Selvarajan, KK, Mohammad, JI, Kaveti, B, et al.. Identification of novel acetylcholinesterase inhibitors: indolopyrazoline derivatives and molecular docking studies. Bioorg Chem 2016;67:9–17. https://doi.org/10.1016/j.bioorg.2016.05.002.Search in Google Scholar
17. Narkhede, MB, Ajimire, PV, Wagh, AE, Mohan, M, Shivashanmugam, AT. In vitro antidiabetic activity of Caesalpina digyna (R.) methanol root extract. Asian J Plant Sci Res 2011;1:101–16.Search in Google Scholar
18. Rafique, R, Khan, KM, Chigurupati, S, Wadood, A, Rehman, AU, Salar, U, et al.. Synthesis, in vitro α-amylase inhibitory, and radicals (DPPH & ABTS) scavenging potentials of new N-sulfonohydrazide substituted indazoles. Bioorg Chem 2020;94:103410. https://doi.org/10.1016/j.bioorg.2019.103410.Search in Google Scholar
19. Yousuf, H, Shamim, S, Khan, KM, Chigurupati, S, Hameed, S, Khan, MN, et al.. Dihydropyridines as potential α-amylase and α-glucosidase inhibitors: synthesis, in vitro and in silico studies. Bioorg Chem 2020;96:103581. https://doi.org/10.1016/j.bioorg.2020.103581.Search in Google Scholar
20. Mathappan, R, Selvarajan, KK, Sujeet, S, Tribedi, S. Evaluation of antitumor activity of Urena lobata against Ehrlich ascites carcinoma treated mice. Orient Pharm Exp Med 2019;19:21–6. https://doi.org/10.1007/s13596-018-0342-x.Search in Google Scholar
21. Habbu, PV, Patil, BS, Salagare, MV, Madagundi, SD, Vankudri, RV, Shukla, ST, et al.. Antidiabetic potential of endophytic bacterial fraction of Murraya koenigii (L.) Spreng. in rats. Spatula DD 2014;4:139–50. https://doi.org/10.5455/spatula.20140826011114.Search in Google Scholar
22. Navghare, VV, Dhawale, SC. In vitro antioxidant, hypoglycemic and oral glucose tolerance test of banana peels. Alexandria J Med 2017;53:237–43. https://doi.org/10.1016/j.ajme.2016.05.003.Search in Google Scholar
23. Strobel, G, Daisy, B. Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 2003;67:491–502. https://doi.org/10.1128/mmbr.67.4.491-502.2003.Search in Google Scholar
24. McKinnon, AC. Plant tissue preparation for the detection of an endophytic fungus in planta. In: Glare, T, Moran-Dies, M, editors. Microbial-based biopesticides. New York: Humana Press; 2016, vol 147:167–73 pp.10.1007/978-1-4939-6367-6_13Search in Google Scholar PubMed
25. Potshangbam, M, Devi, SI, Sahoo, D, Strobel, GA. Functional characterization of endophytic fungal community associated with Oryza sativa L. and Zea mays L. Front Microbiol 2017;8:325. https://doi.org/10.3389/fmicb.2017.00325.Search in Google Scholar
26. Chigurupati, S, Vijayabalan, S, Selvarajan, KK, Aldubayan, M, Alhowail, A, Mani, V, et al.. Antimicrobial exploration between counterpart endosymbiont and host plant (Tamarindus indica Linn.). Curr Pharmaceut Biotechnol 2020;21:384–89. https://doi.org/10.2174/1389201020666191028105325.Search in Google Scholar
27. Ogrodzki, P, Forsythe, SJ. DNA-sequence based typing of the Cronobacter genus using MLST, CRISPR-cas array and capsular profiling. Front Microbiol 2017;8:1875. https://doi.org/10.3389/fmicb.2017.01875.Search in Google Scholar
28. Stephan, R, Grim, CJ, Gopinath, GR, Mammel, MK, Sathyamoorthy, V, Trach, LH, et al.. Re-examination of the taxonomic status of Enterobacter helveticus, Enterobacter pulveris and Enterobacter turicensis as members of the genus Cronobacter and their reclassification in the genera Franconibacter gen. nov. and Siccibacter gen. nov as Franconibacter helveticus comb. nov., Franconibacter pulveris comb. nov and Siccibacter turicensis comb. nov., respectively. Int J Syst Evol Microbiol 2014;64:3402. https://doi.org/10.1099/ijs.0.059832-0.Search in Google Scholar
29. Jackson, EE, Masood, N, Ibrahim, K, Urvoy, N, Hariri, S, Forsythe, SJ. Description of Siccibacter colletis sp. nov., a novel species isolated from plant material, and emended description of Siccibacter turicensis. Int J Syst Evol Microbiol 2015;65:1335–41. https://doi.org/10.1099/ijs.0.000108.Search in Google Scholar
30. Re, R, Pellegrini, N, Proteggente, A, Pannala, A, Yang, M, Rice-Evans, C. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med 1999;26:1231–37. https://doi.org/10.1016/s0891-5849(98)00315-3.Search in Google Scholar
31. Sekhon-Loodu, S, Rupasinghe, HP. Evaluation of antioxidant, antidiabetic and antiobesity potential of selected traditional medicinal plants. Front Nutr 2019;6:53. https://doi.org/10.3389/fnut.2019.00053.Search in Google Scholar
32. Huang, WY, Cai, YZ, Xing, J, Corke, H, Sun, M. A potential antioxidant resource: endophytic fungi from medicinal plants. Econ Bot 2007;61:14. https://doi.org/10.1663/0013-0001(2007)61[14:aparef]2.0.co;2.10.1663/0013-0001(2007)61[14:APAREF]2.0.CO;2Search in Google Scholar
33. Pavithra, N, Sathish, L, Babu, N, Venkatarathanamma, V, Pushpalatha, H, Reddy, GB, et al.. Evaluation of α-amylase, α-glucosidase and aldose reductase inhibitors in ethyl acetate extracts of endophytic fungi isolated from antidiabetic medicinal plants. Int J Pharm Sci Res 2014;5:5334–41. https://doi.org/10.13040/IJPSR.0975-8232.5(12).5334-41.Search in Google Scholar
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Articles in the same Issue
- Frontmatter
- Reviews
- The effect of Nigella sativa on oxidative stress and inflammatory biomarkers: a systematic review and meta-analysis
- Effect of fennel on primary dysmenorrhea: a systematic review and meta-analysis
- Raising burden of non-communicable diseases: importance of integrating Yoga and Naturopathy at primary care level
- Research Articles Basic
- Marketing and legal status of phytomedicines and food supplements in Morocco
- Hydrogen sulfide as a mediator of endothelium-dependent relaxation evoked by Moringa oleifera leaf extract in mesenteric arterial beds isolated from L-NAME hypertensive rats
- Acute and sub-acute toxicity assessment of aqueous leaves extract of Crassocephalum crepidioides (Asteraceae) in Wistar rats
- Zingerone improves the immune responses in an animal model of breast cancer
- Evaluation of efficacy of Bombax ceiba extract and its major constituent, mangiferin in streptozotocin (STZ)-induced diabetic rats
- Bacterial endosymbiont inhabiting Leucaena leucocephala leaves and their antioxidant and antidiabetic potential
- Ameliorative effect of morin on dutasteride-tamsulosin-induced testicular oxidative stress in rat
- The potentiation of beta-lactam and anti-bacterial activities of lipophilic constituents from Mesua ferrae leaves against methicillin-resistant Staphylococcus aureus
- Influence of irisin on diet-induced metabolic syndrome in experimental rat model
- Modulatory effect of methanol extract of Annona muricata stem bark on mitochondrial membrane permeability transition pore in normal rat liver and monosodium glutamate-induced uterine hyperplasia
- Research Articles Clinical
- Functional status in adhesive capsulitis – yoga vs. physiotherapy: a quasi experimental study
- Okada Purifying Therapy in combination with duloxetine vs. duloxetine alone in patients with TMD and fibromyalgia: a randomized clinical study
- The FIFA 11+ does not alter performance in amateur female basketball players—a randomized control trial
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- Immediate effect of interscapular cupping on blood pressure, oxygen saturation, pulse rate and chest expansion in sedentary smoker students
- The effects of an olive-oil massage on hemodialysis patients suffering from fatigue at a hemodialysis unit in southern India – a randomized controlled trial
- Effects of epigallocatechin-3-gallate of Camellia sinensis leaves on blood pressure, lipid profile, atherogenic index of plasma and some inflammatory and antioxidant markers in type 2 diabetes mellitus patients: a clinical trial
- The effect of practicing yoga during pregnancy on labor stages length, anxiety and pain: a randomized controlled trial
- Effect of lumbar stabilization exercises and thoracic mobilization with strengthening exercises on pain level, thoracic kyphosis, and functional disability in chronic low back pain
- A prospective controlled study on Ramadan fasting in the healthy young males in summer in Germany: effect on cytokines
- Tualang honey versus steroid impregnated nasal dressing following endoscopic sinus surgery: a randomized controlled trial
- Short Communications
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