In-vitro antibacterial and antibiofilm activities and in-silico analysis of a potent cyclic peptide from a novel Streptomyces sp. strain RG-5 against antibiotic-resistant and biofilm-forming pathogenic bacteria.
Streptomyces
/ chemistry
Biofilms
/ drug effects
Anti-Bacterial Agents
/ pharmacology
Peptides, Cyclic
/ pharmacology
Microbial Sensitivity Tests
Molecular Docking Simulation
Soil Microbiology
RNA, Ribosomal, 16S
/ genetics
Phylogeny
Drug Resistance, Multiple, Bacterial
/ drug effects
Bacteria
/ drug effects
Streptomyces pratensis
Antibacterial activity
Antibiofilm activity
Docking study
Multi-drug-resistant bacteria
Journal
Archives of microbiology
ISSN: 1432-072X
Titre abrégé: Arch Microbiol
Pays: Germany
ID NLM: 0410427
Informations de publication
Date de publication:
30 Oct 2024
30 Oct 2024
Historique:
received:
19
08
2024
accepted:
16
10
2024
revised:
12
10
2024
medline:
31
10
2024
pubmed:
30
10
2024
entrez:
30
10
2024
Statut:
epublish
Résumé
The proliferation of multidrug-resistant and biofilm-forming pathogenic bacteria poses a serious threat to public health. The limited effectiveness of current antibiotics motivates the search for new antibacterial compounds. In this study, a novel strain, RG-5, was isolated from desert soil. This strain exhibited potent antibacterial and antibiofilm properties against multidrug-resistant and biofilm-forming pathogenic bacteria. Through phenotypical characterizations, 16S rRNA gene sequence and phylogenetic analysis, the strain was identified as Streptomyces pratensis with 99.8% similarity. The active compound, RG5-1, was extracted, purified by reverse phase silica column HPLC, identified by ESI-MS spectrometry, and confirmed by
Identifiants
pubmed: 39476249
doi: 10.1007/s00203-024-04174-2
pii: 10.1007/s00203-024-04174-2
doi:
Substances chimiques
Anti-Bacterial Agents
0
Peptides, Cyclic
0
RNA, Ribosomal, 16S
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
450Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Al-Dhabi NA, Esmail GA, Duraipandiyan V, Arasu MV (2019) Chemical profiling of Streptomyces sp. Al-Dhabi-2 recovered from an extreme environment in Saudi Arabia as a novel drug source for medical and industrial applications. Saudi J Biol Sci 26. https://doi.org/10.1016/j.sjbs.2019.03.009
Ayuso-Sacido A, Genilloud O (2005) New PCR primers for the screening of NRPS and PKS-I systems in actinomycetes: detection and distribution of these biosynthetic gene sequences in major taxonomic groups. Microb Ecol 49. https://doi.org/10.1007/s00248-004-0249-6
Bahrami Y, Bouk S, Kakaei E, Taheri M (2022) Natural products from Actinobacteria as a potential source of new therapies against colorectal cancer. Front Pharmacol 13:929161. https://doi.org/10.3389/fphar.2022.929161
doi: 10.3389/fphar.2022.929161
pubmed: 35899111
pmcid: 9310018
Barrenechea V, Vargas-Reyes M, Quiliano M, Milón P (2021) A complementary mechanism of bacterial mRNA translation inhibition by tetracyclines. Front Microbiol 12. https://doi.org/10.3389/fmicb.2021.682682
Batoni G, Maisetta G, Esin S (2016) Antimicrobial peptides and their interaction with biofilms of medically relevant bacteria. Biochim Biophys Acta 1858(5):1044–1060. https://doi.org/10.1016/j.bbamem.2015.10.013
doi: 10.1016/j.bbamem.2015.10.013
pubmed: 26525663
Belghit S, Driche EH, Bijani C et al (2016) Activity of 2,4-Di-tert-butylphenol produced by a strain of Streptomyces mutabilis isolated from a Saharan soil against Candida albicans and other pathogenic fungi. J Mycol Med 26:160–169. https://doi.org/10.1016/j.mycmed.2016.03.001
doi: 10.1016/j.mycmed.2016.03.001
pubmed: 27107984
Bérdy J (2012) Thoughts and facts about antibiotics: where we are now and where we are heading. J Antibiot (Tokyo) 65:385–395. https://doi.org/10.1038/ja.2012.27
doi: 10.1038/ja.2012.27
pubmed: 22511224
Betina V (1973) Bioautography in paper and thin-layer chromatography and its scope in the antibiotic field. J Chromatogr A 78(1):41–51. https://doi.org/10.1016/s0021-9673(01)99035-1
doi: 10.1016/s0021-9673(01)99035-1
Biovia; Dassault Systèmes (2021) Discovery Studio Visualizer, v3ds; Dassault Systèmes: San Diego, CA, USA, Available online: https://discover.3ds.com/discovery-studio-visualizer-download
Buse MG (2006) Hexosamines, insulin resistance, and the complications of diabetes: current status. Am J Physiol Endocrinol Metab 290(1):E1–E8. https://doi.org/10.1152/ajpendo.00329.2005
doi: 10.1152/ajpendo.00329.2005
pubmed: 16339923
Chalita M, Kim YO, Park S et al (2024) EzBioCloud: a genome-driven database and platform for microbiome identification and discovery. Int J Syst Evol Microbiol 74. https://doi.org/10.1099/ijsem.0.006421
Daina A, Michielin O, Zoete V (2017) SwissADME: a free web tool to evaluate pharmacokinetics, drug-likeness and medicinal chemistry friendliness of small molecules. Sci Rep 7:42717. https://doi.org/10.1038/srep42717
doi: 10.1038/srep42717
pubmed: 28256516
pmcid: 5335600
Dallakyan S, Olson AJ (2015) Small-molecule Library Screening by Docking with PyRx. In: Hempel J, Williams C, Hong CC (eds) Methods in Molecular Biology, vol 1263. Humana, New York, NY, pp 243–250. https://doi.org/10.1007/978-1-4939-2269-7_19
doi: 10.1007/978-1-4939-2269-7_19
De Rosa S, Mitova M, Tommonaro G (2003) Marine bacteria associated with sponge as source of cyclic peptides. Biomol Eng 20(4):311–316. https://doi.org/10.1016/s1389-0344(03)00038-8
doi: 10.1016/s1389-0344(03)00038-8
pubmed: 12919814
Di L, Kerns EH (2016) Drug-Like Properties: Concepts, Structure Design and Methods from ADME to Toxicity Optimization, second edition, Academic Press, pp 1–529. https://doi.org/10.1016/C2013-0-18378-X
Driche EH, Belghit S, Bijani C, Zitouni A, Sabaou N, Mathieu F, Badji B (2015) A new Streptomyces strain isolated from Saharan soil produces di-(2-ethylhexyl) phthalate, a metabolite active against methicillin-resistant Staphylococcus aureus. Ann Microbiol 65:1341–1350. https://doi.org/10.1007/s13213-014-0972-2
doi: 10.1007/s13213-014-0972-2
Driche EH, Sabaou N, Bijani C, Zitouni A, Pont F, Mathieu F, Badji B (2017) Streptomyces sp. AT37 isolated from a Saharan soil produces a furanone derivative active against multidrug-resistant Staphylococcus aureus. World J Microbiol Biotechnol 33:105. https://doi.org/10.1007/s11274-017-2265-y
doi: 10.1007/s11274-017-2265-y
pubmed: 28466299
Driche EH, Badji B, Bijani C, Belghit S, Pont F, Mathieu F, Zitouni A (2022) A New Saharan strain of Streptomyces sp. GSB-11 produces Maculosin and N-acetyltyramine active against Multidrug-resistant pathogenic Bacteria. Curr Microbiol 79:298. https://doi.org/10.1007/s00284-022-02994-3
doi: 10.1007/s00284-022-02994-3
pubmed: 36002540
Driche EH, Badji B, Bijani C, Belghit S, Pont F, Mathieu F, Zitouni A (2024) Antibacterial and antibiofilm properties of two cyclic dipeptides produced by a new desert Streptomyces sp. HG-17 strain against multidrug-resistant pathogenic bacteria. Int Microbiol. https://doi.org/10.1007/s10123-024-00533-7
doi: 10.1007/s10123-024-00533-7
pubmed: 38777925
Druzian SP, Pinheiro LN, Susin NMB, Dal Prá V, Mazutti MA, Kuhn RC, Terra LM (2020) Production of metabolites with antioxidant activity by Botryosphaeria dothidea in submerged fermentation. Bioprocess Biosyst Eng 43:13–20. https://doi.org/10.1007/s00449-019-02200-y
doi: 10.1007/s00449-019-02200-y
pubmed: 31578605
Farhana A, Khan YS, Biochemistry L (2023) In: StatPearls (ed), Treasure Island (FL): StatPearls Publishing Treasure Island, FL, USA
Fatima A, Aftab U, Shaaban KA, Thorson JS, Sajid I (2019) Spore forming Actinobacterial diversity of Cholistan Desert Pakistan: polyphasic taxonomy, antimicrobial potential and chemical profiling. BMC Microbiol 19(1):1–17. https://doi.org/10.1186/s12866-019-141
doi: 10.1186/s12866-019-141
Ferenczy GG, Kellermayer M (2022) Contribution of hydrophobic interactions to protein mechanical stability. Comput Struct Biotechnol J 20:1946–1956. https://doi.org/10.1016/j.csbj.2022.04.025
doi: 10.1016/j.csbj.2022.04.025
pubmed: 35521554
pmcid: 9062142
Fu L, Shi S, Yi J, Wang N, He Y, Wu Z, Peng J, Deng Y, Wang W, Wu C, Lyu A, Zeng X, Zhao W, Hou T, Cao D (2024) ADMETlab 3.0: an updated comprehensive online ADMET prediction platform enhanced with broader coverage, improved performance, API functionality and decision support. Nucleic Acids Res 5(52):422–431. https://doi.org/10.1093/nar/gkae236
doi: 10.1093/nar/gkae236
Giordano D (2020) Bioactive molecules from Extreme environments. Mar Drugs 18(12):640. https://doi.org/10.3390/md18120640
doi: 10.3390/md18120640
pubmed: 33327603
pmcid: 7765018
Grande R, Puca V, Muraro R (2020) Antibiotic resistance and bacterial biofilm. Expert Opin Ther Pat 30(12):897–900. https://doi.org/10.1080/13543776.2020.1830060
doi: 10.1080/13543776.2020.1830060
pubmed: 32985275
Harvey AL, Clark RL, Mackay SP, Johnston BF (2010) Current strategies for drug discovery through natural products. Expert Opin Drug Discov 5(6):559–568. https://doi.org/10.1517/17460441.2010.488263
doi: 10.1517/17460441.2010.488263
pubmed: 22823167
Horton DA, Bourne GT, Smythe ML (2000) Exploring privileged structures: the combinatorial synthesis of cyclic peptides. Mol Divers 5:289–304. https://doi.org/10.1023/A:1021365402751
doi: 10.1023/A:1021365402751
Jamal M, Ahmad W, Andleeb S, Jalil F, Imran M, Nawaz MA, Hussain T, Ali M, Rafiq M, Kamil MA (2018) Bacterial biofilm and associated infections. J Chin Med Assoc 81(1):7–11. https://doi.org/10.1016/j.jcma.2017.07.012
doi: 10.1016/j.jcma.2017.07.012
pubmed: 29042186
Jung Y, Kim H Bin (2015) Multidrug-resistant gram-positive bacterial infections. Korean J Med 88:487. https://doi.org/10.3904/kjm.2015.88.5.487
doi: 10.3904/kjm.2015.88.5.487
Kämpfer P (2012) Genus I. Streptomyces Waksman and Henrici 1943, 339 emend. Witt and Stackebrandt 1990, 370 emend. Wellington, Stackebrandt, Sanders, Wolstrup and Jorgensen 1992, 159. In Bergey’s Manual of Systematic Bacteriology, vol. 5. The Actinobacteria, Part B, 2nd. In: New York (ed). Springer, pp 1446–1454
Kola I, Landis J (2004) Can the pharmaceutical industry reduce attrition rates? Nat Rev Drug Discov 3:711–715. https://doi.org/10.1038/nrd1470
doi: 10.1038/nrd1470
pubmed: 15286737
Kumar P (2017) Pharmacology of Specific Drug groups: Antibiotic Therapy. In Pharmacology and therapeutics for Dentistry: Seventh Edition (pp. 457–487). Elsevier. https://doi.org/10.1016/B978-0-323-39307-2.00033-3
Lipinski CA, Lombardo F, Dominy BW, Feeney PJ (2001) Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv Drug Deliv Rev 46:3–26. https://doi.org/10.1016/S0169-409X(00)00129-0
doi: 10.1016/S0169-409X(00)00129-0
pubmed: 11259830
Lipinski CA, Lombardo F, Dominy BW, Feeney PJ (2012) Experimental and computational approaches to Estimate Solubility and Permeability in Drug Discovery and Development Settings. Adv Drug Deliv Rev 64:4–17. https://doi.org/10.1016/j.addr.2012.09.019
doi: 10.1016/j.addr.2012.09.019
Locci R (1989) (1989) Streptomycetes and related genera. Bergey’s manual of systematic bacteriology, Williams & Wilkins, Baltimore, pp 2451–2508. In: Streptomycetes and related genera In: Williams ST, Sharpe ME, Holt JG (eds). Williams Wilkins, Baltimore, pp 2451–2508
Lu X, Shen Y, Zhu Y, Xu Q, Liu X, Ni K, Cao X, Zhang, Jiao B (2009) Diketopiperazine constituents of marine Bacillus subtilis. Chem Nat Compd 45:290–292. https://doi.org/10.1007/s10600-009-9270-9
doi: 10.1007/s10600-009-9270-9
Mancuso G, Midiri A, Gerace E, Biondo C (2021) Bacterial antibiotic resistance: the most critical pathogens. Pathogens 10(10):1310. https://doi.org/10.3390/pathogens10101310
doi: 10.3390/pathogens10101310
pubmed: 34684258
pmcid: 8541462
Meng X-Y, Zhang H-X, Mezei M, Cui M (2012) Molecular docking: a powerful Approach for structure-based drug Discovery. Curr Comput Aided-Drug Des 7(2):146–157. https://doi.org/10.2174/157340911795677602
doi: 10.2174/157340911795677602
Metsä-Ketelä M, Salo V, Halo L, Hautala A, Hakala J, Mäntsälä P, Ylihonko K (1999) An efficient approach for screening minimal PKS genes from Streptomyces. FEMS Microbiol Lett 180(1):1–6. https://doi.org/10.1016/S0378-1097(99)00453-X
doi: 10.1016/S0378-1097(99)00453-X
pubmed: 10547437
O’Toole GA (2011) Microtiter dish biofilm formation assay. J Visualized Experiments 30(47):2437. https://doi.org/10.3791/2437
doi: 10.3791/2437
Oki T (1992) Pradimicin, A Novel Antifungal Agent. In: New Approaches for Antifungal Drugs. Birkhäuser, Boston, MA, pp 64–87. https://doi.org/10.1007/978-1-4899-6729-9_5
doi: 10.1007/978-1-4899-6729-9_5
Olson H, Betton G, Robinson D, Thomas K, Monro A, Kolaja G, Lilly P, Sanders J, Sipes G, Bracken W, Dorato M, Van Deun K, Smith P, Berger B, Heller A (2000) Concordance of the toxicity of pharmaceuticals in humans and in animals. Regul Toxicol Pharmacol 32(1):56–67. https://doi.org/10.1006/rtph.2000.1399
doi: 10.1006/rtph.2000.1399
pubmed: 11029269
Pettersen EF, Goddard TD, Huang CC et al (2004) UCSF Chimera - A visualization system for exploratory research and analysis. J Comput Chem 25(13):1605–1612. https://doi.org/10.1002/jcc.20084
doi: 10.1002/jcc.20084
pubmed: 15264254
Pham JV, Yilma MA, Feliz A, Majid MT, Maffetone N, Walker JR, Kim E, Cho HJ, Reynolds JM, Song MC, Park SR, Yoon YJ. A (2019) Review of the Microbial production of Bioactive Natural products and Biologics. Front Microbiol 20(10):1404. https://doi.org/10.3389/fmicb.2019.01404
doi: 10.3389/fmicb.2019.01404
Pinzi L, Rastelli G (2019) Molecular Docking: shifting paradigms in Drug Discovery. Int J Mol Sci 20(18):4331. https://doi.org/10.3390/ijms20184331
doi: 10.3390/ijms20184331
pubmed: 31487867
pmcid: 6769923
Pletzer D, Coleman SR, Hancock REW (2016) Anti-biofilm peptides as a new weapon in antimicrobial warfare. Curr Opin Microbiol 33:35–40. https://doi.org/10.1016/j.mib.2016.05.01
doi: 10.1016/j.mib.2016.05.01
pubmed: 27318321
pmcid: 5069134
Rasamiravaka T, Labtani Q, Duez P, El Jaziri M (2015) The formation of biofilms by pseudomonas aeruginosa: A review of the natural and synthetic compounds interfering with control mechanisms. Biomed Res Int 2015:14. https://doi.org/10.1155/2015/759348
Saadi SA, Meklat A, Mokrane S, Yaiche Achour H, Holtz MD, Klenk HP, Bouras N (2021) isolation and characterization of a new Saccharothrix strain ah023 with antimicrobial activity from an unexploited Algerian Saharan region. Analele Universitatii din Oradea, Fascicula Biologie 28:71–77
Saleem M, Hassan A, Li F, Lu Q, Ponomareva LV, Parkin S, Sun C, Thorson JS, Shaaban KA, Sajid I (2023) Bioprospecting of desert actinobacteria with special emphases on griseoviridin, mitomycin C and a new bacterial metabolite producing Streptomyces sp. PU-KB10–4. BMC Microbiol 23:69. https://doi.org/10.1186/s12866-023-02770-8
doi: 10.1186/s12866-023-02770-8
pubmed: 36922786
pmcid: 10015687
Satpathy S, Sen SK, Pattanaik S, Raut S (2016) Review on bacterial biofilm: An universal cause of contamination. Biocatal Agric Biotechnol 7(5):56–66. https://doi.org/10.1016/j.bcab.2016.05.002
Sauvage E, Kerff F, Terrak M, Ayala JA, et al (2008) The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis. FEMS Microbiol Rev 32(2):234–58. https://doi.org/10.1111/j.1574-6976.2008.00105.x
Sayed AM, Hassan MHA, Alhadrami HA, Hassan HM, Goodfellow M, Rateb ME (2020) Extreme environments: microbiology leading to specialized metabolites. J Appl Microbiol 128(3):630–657. https://doi.org/10.1111/jam.14386
doi: 10.1111/jam.14386
pubmed: 31310419
Scior T, Bender A, Tresadern G, Medina-Franco JL, Martínez-Mayorga K, Langer T, Cuanalo-Contreras K, Agrafiotis DK (2012) Recognizing pitfalls in virtual screening: a critical review. J Chem Inf Model 52(4):867–881. https://doi.org/10.1021/ci200528d
doi: 10.1021/ci200528d
pubmed: 22435959
Sharma M, Bharti S, Goswami A, Mallubhotla S (2023) Diversity, Antimicrobial, antioxidant, and Anticancer Activity of Culturable Fungal Endophyte communities in Cordia dichotoma. Molecules 28(19):6926. https://doi.org/10.3390/molecules28196926
doi: 10.3390/molecules28196926
pubmed: 37836769
pmcid: 10574381
Shirling EB, Gottlieb D (1966) Methods for characterization of Streptomyces species. Int J Syst Bacteriol 16:313–340. https://doi.org/10.1099/00207713-16-3-313
doi: 10.1099/00207713-16-3-313
Silva GC, Kitano IT, Ribeiro IAF, Lacava PT (2022) The potential use of actinomycetes as microbial inoculants and biopesticides in agriculture. Front Soil Sci 2:833181. https://doi.org/10.3389/fsoil.2022.833181
doi: 10.3389/fsoil.2022.833181
Srivastava A, Verma N, Kumar V, Apoorva V, Agarwal V (2024) Biofilm inhibition/eradication: exploring strategies and confronting challenges in combatting biofilm. Arch Microbiol 206:212. https://doi.org/10.1007/s00203-024-03938-0
doi: 10.1007/s00203-024-03938-0
pubmed: 38616221
Stefaniak J, Nowak MG, Wojciechowski M, Milewski S, Skwarecki AS (2022) Inhibitors of glucosamine-6-phosphate synthase as potential antimicrobials or antidiabetics–synthesis and properties. J Enzyme Inhib Med Chem 37(1):1928–1956. https://doi.org/10.1080/14756366.2022.2096018
doi: 10.1080/14756366.2022.2096018
pubmed: 35801410
pmcid: 9272926
Sun S, Chen X (2024) Mechanism-guided strategies for combating antibiotic resistance. World J Microbiol Biotechnol 40:295. https://doi.org/10.1007/s11274-024-04106-8
doi: 10.1007/s11274-024-04106-8
pubmed: 39122871
Tacconelli E, Pezzani MD (2019) Public health burden of antimicrobial resistance in Europe. Lancet Infect Dis 19(1):4–6. https://doi.org/10.1016/S1473-3099(18)30648-0
doi: 10.1016/S1473-3099(18)30648-0
pubmed: 30409682
Tamura K, Stecher G, Kumar S (2021) MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Mol Biol Evol 38(7):3022–3028. https://doi.org/10.1093/molbev/msab120
doi: 10.1093/molbev/msab120
pubmed: 33892491
pmcid: 8233496
Tarín-Pelló A, Suay-García B, Pérez-Gracia MT (2022) Antibiotic resistant bacteria: current situation and treatment options to accelerate the development of a new antimicrobial arsenal. Expert Rev Anti Infect Ther 20(8):1095–1108. https://doi.org/10.1080/14787210.2022.2078308
doi: 10.1080/14787210.2022.2078308
pubmed: 35576494
Thériault JF, Poirier D, Lin SX (2021) The multi-specific human 17 beta-hydroxysteroid dehydrogenase type 7: non-competitive inhibitors can target different catalyses to facilitate breast cancer treatment. J Steroid Biochem Mol Biol 214:105963. https://doi.org/10.1016/j.jsbmb.2021.105963
doi: 10.1016/j.jsbmb.2021.105963
pubmed: 34400276
Von Ahsen U, Davies J, Schroeder R (1992) Non-competitive inhibition of group I intron RNA self-splicing by aminoglycoside antibiotics. J Mol Biol 226(4):935–941. https://doi.org/10.1016/0022-2836(92)91043-O
doi: 10.1016/0022-2836(92)91043-O
Wink JM (1990) Methods for the taxonomic description of the Actinobacteria. Compendium Actinobacteria 49: https://www.dsmz.de/microorganisms/wink_pdf/Actinomethods.pdf
Yang EJ, Chang HC (2010) Purification of a new antifungal compound produced by Lactobacillus plantarum AF1 isolated from kimchi. Int J Food Microbiol 139(1–2):56–63. https://doi.org/10.1016/j.ijfoodmicro.2010.02.012
doi: 10.1016/j.ijfoodmicro.2010.02.012
pubmed: 20226553
Zerouki C, Bensalah F, Kuittinen S, Pappinen A, Turunen O (2021) Whole-genome sequencing of two Streptomyces strains isolated from the sand dunes of Sahara. BMC Genomics 22(1):578. https://doi.org/10.1186/s12864-021-07866-x
doi: 10.1186/s12864-021-07866-x
pubmed: 34315408
pmcid: 8317367
Zorzi A, Deyle K, Heinis C (2017) Cyclic peptide therapeutics: past, present and future. Curr Opin Chem Biol 38:24–29. https://doi.org/10.1016/j.cbpa.2017.02.006
doi: 10.1016/j.cbpa.2017.02.006
pubmed: 28249193