Abstract
Secondary metabolites produced by myxobacterial genera are often characterized as diverse molecules with unique structural properties which drove us to search for myxobacterial source of anti-diabetic drug discovery. In the present study, from 80 soil samples, out of sixty-five observed isolates, 30 and 16 were purified as Myxococcus and non-Myxococcus, respectively. Isolated strains taxonomically belonged to the genera Myxococcus, Corallococcus and Cystobacter, Archangium, Nanocystis, and Sorangium, and some could not be attributed. Secondary metabolites of selected non-Myxococcus isolates extracted by the liquid–liquid method showed that the myxobacterium UTMC 4530 demonstrated the highest inhibition on the formation of carbonyl group and fructosamine, respectively. In addition, it showed 23% and 15.8% inhibitory activity on α-glucosides and α-amylase compared to acarbose (23%, 18%), respectively. The extract of strain UTMC 4530 showed 35% induction effect on glucose adsorption while showing no radical scavenging activity and no toxic effect on HRBC lysis and HepG2 in cytotoxicity assays. The strain UTMC 4530 (ON808962), with the multiple antidiabetic activity, showed 87.3% similarity to Corallococcus llansteffanensis which indicates its affiliation to a new genus. The results of this study revealed that secondary metabolites produced by strain UTMC 4530 can be considered a promising source to find new therapeutic and pharmaceutical applications perhaps a multi-mechanism anti-diabetic compound.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and materials
Data are presented in the manuscript text and its supplementary material.
References
Almasi F, Mohammadipanah F, Adhami H-R, Hamedi J (2018) Introduction of marine-derived Streptomycessp. UTMC 1334 as a source of pyrrole derivatives with anti-acetylcholinesterase activity. J Appl Microbiol 125:1370–1382. https://doi.org/10.1111/jam.14043
Babadi ZK, Garcia R, Ebrahimipour GH et al (2022) Corallococcus soli sp. Nov., a soil myxobacterium isolated from subtropical climate, Chalus County, Iran, and its potential to produce secondary metabolites. Microorganisms 10:1262. https://doi.org/10.3390/microorganisms10071262
Bader CD, Panter F, Müller R (2020) In depth natural product discovery - myxobacterial strains that provided multiple secondary metabolites. Biotechnol Adv 39:107480. https://doi.org/10.1016/j.biotechadv.2019.107480
Baynest HW (2015) Classification, pathophysiology, diagnosis and management of diabetes mellitus. J Diabetes Metab 6. https://doi.org/10.4172/2155-6156.1000541
Bhat MA, Mishra AK, Bhat MA et al (2021) Myxobacteria as a source of new bioactive compounds: a perspective study. Pharmaceutics 13:1265. https://doi.org/10.3390/pharmaceutics13081265
Caprioglio D, Minassi A, Avonto C et al (2020) Thiol-trapping natural products under the lens of the cysteamine assay: friends, foes, or simply alternatively reversible ligands? Phytochem Rev 19:1307–1321. https://doi.org/10.1007/s11101-020-09700-w
Chelliah R, Banan-MwineDaliri E, Oh D-H (2022) Screening of actinobacteria for enzyme inhibitor activity. Methods in Actinobacteriology 475–478
Cho NH, Shaw JE, Karuranga S et al (2018) IDF Diabetes Atlas: global estimates of diabetes prevalence for 2017 and projections for 2045. Diabetes Res Clin Pract 138:271–281. https://doi.org/10.1016/j.diabres.2018.02.023
Dai W, Liu Y, Yao D et al (2023) Phylogenetic diversity of stochasticity-dominated predatory myxobacterial community drives multi-nutrient cycling in typical farmland soils. Sci Total Environ 871:161680. https://doi.org/10.1016/j.scitotenv.2023.161680
Dariya B, Nagaraju GP (2020) Advanced glycation end products in diabetes, cancer and phytochemical therapy. Drug Discov Today 25:1614–1623. https://doi.org/10.1016/j.drudis.2020.07.003
Dawid W (2000) Biology and global distribution of myxobacteria in soils. FEMS Microbiol. Rev. 24(4):403–427. https://doi.org/10.1111/j.1574-6976.2000.tb00548.x
Ding X, Zhang J, Jiang P et al (2004) Structural features and hypoglycaemic activity of an exopolysaccharide produced by Sorangium cellulosum. Lett Appl Microbiol 38:223–228. https://doi.org/10.1111/j.1472-765x.2004.01465.x
Galushko A, Kuever J (2020) Desulfovibrionaceae. Bergey’s Man. Syst Archaea Bact 1–13
Herrmann J, Fayad AA, Müller R (2017) Natural products from myxobacteria: novel metabolites and bioactivities. Nat Prod Rep 34:135–160. https://doi.org/10.1039/c6np00106h
Hong Son B, Van Nga V, Thi Diem Hong L, Thi Quynh D (2022) Potent natural inhibitors of alpha-glucosidase and the application of Aspergillus spp. in diabetes type 2 drugs: a review. VNU J Sci Med Pharm Sci 38. https://doi.org/10.25073/2588-1132/vnumps.4334
Improta G, Luciano MA, Vecchione D et al (2021) Management of the diabetic patient in the diagnostic care pathway. 8th European Medical and Biological Engineering Conference: Proceedings of the EMBEC 2020, November 29–December 3, 2020 Portorož, Slovenia. pp 784–792
Indupalli M, Muvva V, Mangamuri U, Munaganti R K and Naragani K (2018) Bioactive compounds from mangrove derived rare actinobacterium Saccharomonospora oceani VJDS-3. 3 Biotech 8:1–9. https://doi.org/10.1007/s13205-018-1093-6
Jayaprakashvel M (2012) Therapeutically active biomolecules from marine actinomycetes. J Mod Biotechnol 1:1–7
Kamiloglu S, Sari G, Ozdal T, Capanoglu E (2020) Guidelines for cell viability assays. Food Front 1:332–349. https://doi.org/10.1002/fft2.44
Kaur S, Singh B, Kaur N, Kaur S (2018) Pharmacognostic investigations on leaves of grewia asiatica linn. Int Res J Pharm 9:85–90. https://doi.org/10.7897/2230-8407.09578
Khan MAB, Hashim MJ, King JK et al (2020) Epidemiology of type 2 diabetes - global burden of disease and forecasted trends. J Epidemiol Glob Health 10:107–111. https://doi.org/10.2991/jegh.k.191028.001
Khanal P, Patil BM, Mandar BK et al (2019) Network pharmacology-based assessment to elucidate the molecular mechanism of anti-diabetic action of Tinospora cordifolia. Clin Phytoscience 5. https://doi.org/10.1186/s40816-019-0131-1
Kulkarni-Almeida AA, Brahma MK, Padmanabhan P et al (2011) Fermentation, isolation, structure, and antidiabetic activity of NFAT-133 produced by Streptomyces strain PM0324667. AMB Express 1:42. https://doi.org/10.1186/2191-0855-1-42
Kumar SRS, Rao KVB (2018) Efficacy of alpha glucosidase inhibitor from marine Actinobacterium in the control of postprandial hyperglycaemia in Streptozotocin (STZ) induced diabetic male albino Wister rats. Iran J Pharm Res IJPR 17:202
Paul S, Majumdar M (2020) In-vitro antidiabetic propensities, phytochemical analysis, and mechanism of action of commercial antidiabetic polyherbal formulation “Mehon”. 1st Int Electron Conf Biomol Nat Bio-Inspired Ther Hum Dis
Petters S, Groß V, Söllinger A et al (2021) The soil microbial food web revisited: predatory myxobacteria as keystone taxa? ISME J 15:2665–2675. https://doi.org/10.1038/s41396-021-00958-2
Ratte M, Batubara I, Lestari Y (2022) Morphological characterization and antioxidant activity of actinobacteria from Xylocarpus granatum growing in mangrove habitat. Biotropika J Trop Biol 10
Ravi L, Ragunathan A, Krishnan K (2017) Antidiabetic and antioxidant potential of GancidinW from streptomyces paradoxus VITALK03. Open Bioact Compd J 5:31–42. https://doi.org/10.2174/1874847301705010031
Rehman G, Hamayun M, Iqbal A et al (2018) In vitro antidiabetic effects and antioxidant potential of Cassia nemophila pods. Biomed Res Int 2018:1824790. https://doi.org/10.1155/2018/1824790
Saadatpour F, Mohammadipanah F (2020) Bioprospecting of indigenous myxobacteria from Iran and potential of Cystobacter as a source of anti-MDR compounds. Folia Microbiol (praha) 65:639–648
Saggu SK, Nath A, Kumar S (2023) Myxobacteria: biology and bioactive secondary metabolites. Res Microbiol 104079
Salimi F, Jafari-Nodooshan S, Zohourian N et al (2018) Simultaneous anti-diabetic and anti-vascular calcification activity of Nocardia sp. UTMC 751. Lett Appl Microbiol 66:110–117. https://doi.org/10.1111/lam.12833
Savych AO, Marchyshyn S, Kozyr H, Yarema N (2021) Determination of inulin in the herbal mixtures by GC-MS method. Pharmacia 68(1):181–187. https://doi.org/10.3897/pharmacia.68.e55051
Shrivastava A, Sharma RK (2021) Myxobacteria and their products: current trends and future perspectives in industrial applications. Folia Microbiol (praha). https://doi.org/10.1007/s12223-021-00875-z
Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 38:3022–3027
Tupe RS, Kemse NG, Khaire AA, Shaikh SA (2017) Attenuation of glycation-induced multiple protein modifications by Indian antidiabetic plant extracts. Pharm Biol 55:68–75. https://doi.org/10.1080/13880209.2016.1228683
Waite DW, Chuvochina M, Pelikan C et al (2020) Proposal to reclassify the proteobacterial classes Deltaproteobacteria and Oligoflexia, and the phylum Thermodesulfobacteria into four phyla reflecting major functional capabilities. Int J Syst Evol Microbiol 70:5972–6016. https://doi.org/10.1099/ijsem.0.004213
Wang K-J, Zhao J-L (2019) Corn silk (Zea mays L.), a source of natural antioxidants with α-amylase, α-glucosidase, advanced glycation and diabetic nephropathy inhibitory activities. Biomed Pharmacother 110:510–517. https://doi.org/10.1016/j.biopha.2018.11.126
Wang P, Jiang X, Jiang Y et al (2007) In vitro antioxidative activities of three marine oligosaccharides. Nat Prod Res 21:646–654
Wang W, Xu H, Chen H et al (2016) In vitro antioxidant, anti-diabetic and antilipemic potentials of quercetagetin extracted from marigold (Tagetes erecta L.) inflorescence residues. J Food Sci Technol 53:2614–2624. https://doi.org/10.1007/s13197-016-2228-6
Weissman KJ, Müller R (2009) A brief tour of myxobacterial secondary metabolism. Bioorganic Med Chem 17:2121–2136. https://doi.org/10.1016/j.bmc.2008.11.025
Whang A, Nagpal R, Yadav H (2019) Bi-directional drug-microbiome interactions of anti-siabetics. Ebiomedicine 39:591–602. https://doi.org/10.1016/j.ebiom.2018.11.046
Wu Z-H, Jiang D-M, Li P, Li Y-Z (2005) Exploring the diversity of myxobacteria in a soil niche by myxobacteria-specific primers and probes. Environ Microbiol 7:1602–1610. https://doi.org/10.1111/j.1462-2920.2005.00852.x
Yoon S-H, Ha S-M, Kwon S et al (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617. https://doi.org/10.1099/ijsem.0.001755
Yoon S-Y, Lee SR, Hwang JY et al (2019) Fridamycin A, a microbial natural product, stimulates glucose uptake without inducing adipogenesis. Nutrients 11:765. https://doi.org/10.3390/nu11040765
Ziolkowska S, Binienda A, Jabłkowski M et al (2021) The interplay between insulin resistance, inflammation, oxidative stress, base excision repair and metabolic syndrome in nonalcoholic fatty liver disease. Int J Mol Sci 22:11128. https://doi.org/10.3390/ijms222011128
Funding
The support of Agence Universitaire de la Francophonie is appreciated.
Author information
Authors and Affiliations
Contributions
FS: lab experiments and manuscript writing, MHN: lab experiments, FS: data analysis and manuscript writing, and FM: conceptualization and manuscript edition.
Corresponding author
Ethics declarations
Conflict of interests
The authors declare no conflict of interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Saadatpour, F., Nikzad, M.H., Salimi, F. et al. Mining the soil myxobacteria and finding sources of anti-diabetic metabolites. Folia Microbiol 69, 109–119 (2024). https://doi.org/10.1007/s12223-023-01074-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12223-023-01074-8