DOI QR코드

DOI QR Code

Antibacterial Activity of Streptomyces Strains Isolated from Different Regions of Jordan

  • Hala Khyami-Horani (Department of Biological Sciences, School of Science, The University of Jordan ) ;
  • Amal Al-Aboudi (Department of Chemistry, School of Science, The University of Jordan) ;
  • Musa Abu Zarga (Department of Chemistry, School of Science, The University of Jordan) ;
  • Monther Sadder (Department of Horticulture and Crop Science, School of Agriculture, The University of Jordan) ;
  • Halima Othman (Department of Biological Sciences, School of Science, The University of Jordan )
  • Received : 2023.03.28
  • Accepted : 2023.08.16
  • Published : 2023.12.28

Abstract

Members of the genus Streptomyces produce more than 70% of antibiotics. The rise in antibiotic resistance globally enhanced the search for novel species with the ability to produce new bioactive compounds. This study was initiated to investigate different regions in Jordan for previously uncultured and rare Streptomyces species capable of producing novel antimicrobial compounds especially active against bacteria resistant to antibiotics. A total of 191 Streptomyces strains were isolated from 26 soil samples collected from different geographic regions in Jordan. Isolates were characterized based on colony and cellular morphology as well as using 16S rRNA gene sequencing. These isolates were screened for their ability to produce antibiotics by the perpendicular-cross streak method, and then tested by well diffusion method against tested pathogens. Fifty-four isolates showed potential to produce antimicrobial products especially active against resistant bacteria, 20.1% of the isolates showed inhibitory effect against Staphylococcus aureus, 16.9% against clinical MSSA strains, and 18.0% against MRSA: whereas only 4.2% against Esherichia coli, 3.2% against Klebsiella pneumonia, 2.7% against Pseudomonas aeruginosa, and 10.0% against clinical Candida albicans. Three isolates were selected for further identification due to their antibacterial activity against S. aureus, MRSA, and MSSA. These isolates were identified as follows; Streptomyces aburaviensis DSa3, Streptomyces alboniger SAb7 and Streptomyces misionensis ZAb2, based on cultural, biochemical characteristics and molecular analysis of the 16S rRNA.

Keywords

Acknowledgement

The authors would like to thank the Deanship of Scientific Research at the University of Jordan for the financial support of this work.

References

  1. Williams ST, Goodfellow M, Alderson G, Wellington EMH, Sneath PHA, Sackin MJ. 1983. Numerical classification of Streptomyces and related genera.J. Gen. Microbiol. 129: 1743-1813. https://doi.org/10.1099/00221287-129-6-1743
  2. Williams ST, Goodfellow M, Wellington EMH, Vickers JC, Alderson G, Sneath PHA, et al. 1983. A probability matrix for identification of Streptomyces. J. Gen. Microbiol. 129: 1815-1830. https://doi.org/10.1099/00221287-129-6-1815
  3. Goodfellow M, Kampfer P, Busse HJ, Trujillo ME, Suzuki K, Ludwig W, Whitman WB (ed). 2012. Bergey's manual of systematic bacteriology, vol 5. The Actinobacteria, part A and B. Springer, New York, NY.
  4. Salam N, Jiao JY, Zhang XT, Li WJ. 2020. Update on the classification of higher ranks in the phylum Actinobacteria. Int. J. Syst. Evol. Microbiol. 70: 1331-1355. https://doi.org/10.1099/ijsem.0.003920
  5. Lacey H, Rutledge J. 2022. Recently discovered secondary metabolites from Streptomyces species. Molecules 27: 887.
  6. Ayswaria R, Vasu V, Krishna R. 2020. Diverse endophytic Streptomyces species with dynamic metabolites and their meritorious applications: a critical review. Crit. Rev. Microbiol. 46: 750-758. https://doi.org/10.1080/1040841X.2020.1828816
  7. Sivalingam P, Hong K, Pote J, Prakbakar K. 2019. Extreme environment Streptomyces: Potential sources for new antibacterial and anticancer drug leads. Int. J. Microbiol. https://doi.org/10.1155/2019/5283948. Accessed on Oct. 9, 2022.
  8. Chater KF. 2016. Recent advances in understanding Streptomyces. F1000Res. 5: 2795.
  9. Hui M, Tan L, Letchumanan V, He Y-W, Fang C-M, Chan KJ, et al. 2021. The extremophilic actinobacteria: From microbes to medicine. Antibiotics 10: 682.
  10. Jones S, Ho L, Rees C, Hill J, Nodwell J, Elliot M. 2017. Streptomyces exploration is triggered by fungal interactions and volatile signals. ELife 6: e21738.
  11. Humberto EO, Ferreira LLG, Melo WGP, Oliveira ALL, Ramos Alvarenga RF, Lopes NP, et al. 2019. Antifungal compounds from Streptomyces associated with attine ants also inhibit Leishmania donovani. PLoS Negl. Trop. Dis. 13: e0007643.
  12. Harir M, Bendif H, Bellahcene M, Fortas Z Pogni R. 2018. Streptomyces secondary Metabolites. Basic Biology and Applications of Actinobacteria. Enany, S (ed.), IntechOpen, London.
  13. Law W, Chan G, He W, Yw H, Khan T, Ab Mutalib N, et al. 2019. Diversity of Streptomyces spp. from mangrove forest of Sarawak (Malaysia) and screening of their antioxidant and cytotoxic activities. Sci. Rep. 9: 15262.
  14. Fangfang L, Daiwei C, Shengsheng L, Guang Y, Xiaoling Z, Zhao C, et al. 2018. Anti-influenza A viral butenolide from Streptomyces sp. Smu03 inhabiting the intestine of Elephas maximus. Viruses 10: 356.
  15. Bergeijk D, Terlouw B, Medema M, Wezel G. 2020. Ecology and genomics of actinobacteria: new concepts for natural product discovery. Nat. Rev. Microbiol. 18: 546-558. https://doi.org/10.1038/s41579-020-0379-y
  16. Nguyen HT, Pokhrel AR, Nguyen CT, PhamVTT, Dhakal D, Lim HN, et al. 2020. Streptomyces sp. VN1, a producer of diverse metabolites including non-natural furan-type anticancer compound. Sci. Rep. 10: 1756.
  17. Singh B, Kumar P, Haque S, Jawed A, Dubey K. 2017. Improving production of tacrolimus in streptomyces tacrolimicus (atcc 55098) through development of novel mutant by dual mutagenesis. Braz. Arch. Biol. Technol. 60: e17160366.
  18. Tran T, Ameye M, Devlieghere F, De Saeger S, Eeckhout M, Audenaert K. 2021. Streptomyces strains promote plant growth and induce resistance against Fusarium verticillioides via transient regulation of auxin signaling and archetypal defense pathways in maize plants. Front. Plant Sci. 12: 755733.
  19. Howard T. 1953. The Production of Neomycin by Streptomyces fradiae in synthetic media. Appl. Microbiol, 1: 103-106. https://doi.org/10.1128/am.1.2.103-106.1953
  20. Akagawa H, Okanishi M, Umezawa H. 1975. A plasmid involved in chloramphenicol production in Streptomyces venezuelae: Evidence from genetic mapping. J. Gen. Microbiol. 90: 336-346. https://doi.org/10.1099/00221287-90-2-336
  21. Sankaran L, Pogell B. 1975. Biosynthesis of puromycin in Streptomyces alboniger: regulation and properties of O-demethylpuromycin O-methyltransferase. Antimicrob. Agents Chemother. 8: 721-732. https://doi.org/10.1128/AAC.8.6.721
  22. Distler J, Ebert A, Mansouri K, Pissowotzki K, Stockmann M. 1987. Gene cluster for streptomycin biosynthesis in Streptomyces griseus: Nucleotide sequence of three genes and analysis of transcriptional activity. Nucleic Acids Res. 15: 8041-8056. https://doi.org/10.1093/nar/15.19.8041
  23. Swan DG, Rodriguez A, Vilches M, Mendez C, Salas JA. 1994. Characterisation of a Streptomyces antibioticus gene encoding a type I polyketide synthase which has an unusual coding sequence. Mol. Gen. Genet. 242: 358-362. https://doi.org/10.1007/BF00280426
  24. Peschke U, Schmidt H, Zhang Z, Piepersberg W. 1995. Molecular characterization of the lincomycin-production gene cluster of Streptomyces lincolnensis. Mol. Microbiol. 16: 1137-1156. https://doi.org/10.1111/j.1365-2958.1995.tb02338.x
  25. Nelson M, Hillen, W, Greenwald R. 2001. Tetracyclines in biology, chemistry and medicine. Birkhauser Basel. pp. 8. doi: 10.1007/978-3-0348-8306-1.
  26. Miao V. 2005. Daptomycin biosynthesis in Streptomyces roseosporus: Cloning and analysis of the gene cluster and revision of peptide stereochemistry. Microbiology 151(Pt 5): 1507-1523. https://doi.org/10.1099/mic.0.27757-0
  27. Woodyer R, Shao Z, Thomas P, Kelleher N, Blodgett J, Metcalf W, et al. 2006. Heterologous production of Fosfomycin and identification of the minimal biosynthetic gene cluster. Chem. Biol. 13: 1171-1182. https://doi.org/10.1016/j.chembiol.2006.09.007
  28. Atta H. 2010. Biochemical studies on antibiotic production from Streptomyces sp.: Taxonomy, fermentation, isolation and biological property. J. Saudi. Chem. Soc. 19: 12-22. https://doi.org/10.1016/j.jscs.2011.12.011
  29. Wu C, Zhu H, van Wezel GP, Choi YH. 2016. Metabolomics-guided analysis of isocoumarins production by Streptomyces species MBT76 and biotransformation of flavonoids and phenylpropanoids. Metabolomics 12: 90.
  30. Xie F, Pathom-Aree W. 2021. Actinobacteria from desert: Diversity and biotechnological applications. Front. Microbiol, 12: 765531.
  31. Palmer C. 2013. Biogeography. Atlas of Jordan. Ed. Myriam Ababsa, Publications de l'Institut francais du Proche-Orient Contemporary publications | CP 32 Beirut pp. 77-87. DOI: 10.4000/books.ifpo.4560. https://books.openedition.org/ifpo/4871.
  32. Schlatter D, Fubuh A, Xiao K, Hernandez D, Hobbie S, Kinkel L. 2009. Resource amendments influence density and competitive phenotypes of Streptomyces in soil. Microb. Ecol. 57: 413-420. https://doi.org/10.1007/s00248-008-9433-4
  33. Law J, Ser H-L, Khan T, Chuah LH, Pusparajah P, Chan KG, et al. 2017. The potential of Streptomyces as biocontrol agents against the rice blast fungus, Magnaporthe oryzae (Pyricularia oryzae). Front. Microbiol, 8: 3.
  34. Saadoun I, Ananbeh H, Ababneh Q, Jaradat Z. 2017. Comparative distribution of soil Streptomyces flora in different Jordanian habitats and their enzymatic and antibiotic activities. Res. J. Pharm. Biol. Chem. Sci. 8: 1285-1297.
  35. Suneetha V, Raj, Prathusha K. 2011. Isolation and identification of Streptomyces ST1 and ST2 strains from Tsunami affected soils: Morphological and biochemical studies. J. Oceanogr. Mar. Sci. 2: 96-101.
  36. Saadoun I, Hameed KM, Moussauui A. 1999. Characterization and analysis of antibiotic activity of some aquatic actinomycetes. Microbios 99: 173-179.
  37. Kuster E, Williams S. 1964. Selection of media for isolation of Streptomycetes. Nature 202: 928-929. https://doi.org/10.1038/202928a0
  38. Shirling E, Gottlieb D. 1966. Methods, classification, identification and description of genera and species. The Williams and Wilkins Company, Baltimore. 2: 61-292.
  39. Dal Pizzol M, Freitas E, Locatelli C, Guareze F, Reginatto P, Machado G, et al. 2021. Antifungal efficacy and safety of cycloheximide as a supplement in optisol-GS. Drug Des. Devel. Ther. 15: 2091-2098. https://doi.org/10.2147/DDDT.S298059
  40. Oskay M. 2009. Comparison of Streptomyces diversity between agricultural and non-agricultural soils by using various culture media. Sci. Res. Essay 4 : 997-1005.
  41. Madigan MT, Martinko JM, Parker J. 1997. Brock Biology of Microorganisms. 8th Edition, Prentice Hall International, Inc., New York.
  42. Le Page S, van Belkum A, Fulchiron C, Huguet R, Raoult D, Rolain J. 2015. Evaluation of the PREVI® Isola automated seeder system compared to reference manual inoculation for antibiotic susceptibility testing by the disk diffusion method. Eur. J. Clin. Microbiol. Infect. Dis. 34: 1859-1869. https://doi.org/10.1007/s10096-015-2424-8
  43. Shirling E, Gottlieb D. 1966. Methods for characterization of Streptomyces species. Int. J. Syst. Evol. Microbiol. 16: 313-340. https://doi.org/10.1099/00207713-16-3-313
  44. Saadoun I, Al-Momani F. 1997. Studies on soil Streptomycetes from Jordan. Actinomycetes 8: 42-48.
  45. Saadoun I, Gharaibeh R. 2002. The Streptomyces flora of Jordan and its' potential as a source of antibiotics active against antibiotic-resistant Gram-negative bacteria. World J. Microbiol. Biotechnol. 18: 465-470. https://doi.org/10.1023/A:1015531205871
  46. Saadoun I, Gharaibeh R. 2003. The Streptomyces flora of Badia region of Jordan and its potential as a source of antibiotic-resistant bacteria. J. Arid. Environ. 53: 365-371. https://doi.org/10.1006/jare.2002.1043
  47. Saadoun I, Al-Momani F, Malkawi H, Mohammad M. 1999. Isolation, identification and analysis of antibacterial activity of soil Streptomycetes isolates from north Jordan, Microbios, 100: 41-46.
  48. Saadoun I, Hameed K, Al-Momani F, Malkawi H, Meqdam M, Mohammad M. 2000. Characterization and analysis of antifungal activity of soil Streptomycetes isolated from North Jordan. Egypt J. Microbiol. 35: 463-471.
  49. Saadoun I, Muhana A. 2008. Optimal production conditions, extraction, partial purification and characterization of inhibitory compound(s) produced by Streptomyces Ds-104 isolate against multi-drug resistant Candida albicans, Curr. Trends Biotechnol. Pharm. 2: 402-420.
  50. Kouadri F, Al-Aboudi A, Khyami-Horani H. 2014. Antimicrobial activity of Streptomyces sp. isolated from the gulf of Aqaba-Jordan and screening for NRPS, PKS-I, and PKS-II genes. Afr. J. Biotechnol. 13: 3505-3515. https://doi.org/10.5897/AJB2014.13869
  51. Rawashdeh R, Saadoun I, Mahasneh A. 2005. Effect of cultural conditions on xylanase production by Streptomyces sp. (strain Ib 24D) and its potential to utilize tomato pomace Afr. J. Biotechol. 4: 251-255.
  52. Martinez-Castro M, Barreiro C, Romero F, Fernandez-Chimeno R, Martin J. 2011. Streptomyces tacrolimicus sp. nov., a low producer of the immunosuppressant tacrolimus (FK506). Int. J. Syst. Evol. Microbiol. 61: 1084-1088. https://doi.org/10.1099/ijs.0.024273-0
  53. Yao JY, Yin WL, Li XC, Li G, et al. 2014. Anti-parasitic activities of specific bacterial extracellular products of Streptomyces griseus SDX-4 against Ichthyophthirius multifiliis. Parasitol. Res. 113: 3111-3117. https://doi.org/10.1007/s00436-014-4020-8
  54. Abd-Elnaby H, Abo-Elala G, Abdel-Raouf U, Abdelwahab A, Hamed M. 2016. Antibacterial and anticancer activity of marine Streptomyces parvus: Optimization and application. Biotechnol. Biotechnol. Equip. 30: 180-191. https://doi.org/10.1080/13102818.2015.1086280
  55. Silambarasan S, Praveen E, Murugan T, Saravanan D, Balagurunathan R. 2012. Antibacterial and antifungal activities of actinobacteria isolated from Rathnagiri hills. J. Appl. Pharm. Sci. 2: 99-103. https://doi.org/10.7324/JAPS.2012.21020
  56. Valli S, Svathi Sugasini S, Aysha OS, Nirmala P, Vinoth Kumar P, Reena A. 2012. Antimicrobial potential of Actinomycetes species isolated from marine environment. Asian Pac. J. Trop. Biomed. 2: 469-473. https://doi.org/10.1016/S2221-1691(12)60078-1
  57. Al-Ansari M, Alkubaisi N, Vijayaragavan P, Murugan K. 2019. Antimicrobial potential of Streptomyces sp. to the Gram positive and Gram-negative pathogens. J. Infect. Public Health 12: 861-866. https://doi.org/10.1016/j.jiph.2019.05.016
  58. Jalal K, Hasan A. 2021. Molecular and phenotypic characterization of novel Streptomyces species isolated from Kurdistan soil and its antibacterial activity against human pathogens. Jordan J. Biol. Sci. 14: 441-451. https://doi.org/10.54319/jjbs/140309
  59. Meliani M, Denis F, Mohamed-Benkada M, Gabed N, et al. 2022. Characterization of Actinomycetes strains isolated from Cheliff Estuary in the North-West of Algeria. Jordan J. Biol. Sci. 15: 7-14. https://doi.org/10.54319/jjbs/150102
  60. Tenebro CP, Trono DJ, Vicera, CV, Sabido EM, Ysulat JA, Macaspac JM, et al. 2021. Multiple strain analysis of Streptomyces species from Philippine marine sediments reveals intraspecies heterogeneity in antibiotic activities. Sci. Rep. 11: 17544.
  61. Magaldi S, Mata-Essayag S, Hartung de Capriles, C. 2004. Well diffusion for antifungal susceptibility testing. Int. J. Infect. Dis. 8: 39-45. https://doi.org/10.1016/j.ijid.2003.03.002
  62. Valgas C, De Souza S, Smania E, Smania Jr A. 2007. Screening methods to determine antibacterial activity of natural products. Braz. J. Microbiol. 38: 369-380. https://doi.org/10.1590/S1517-83822007000200034
  63. Thumar JT, Dhulia K, Singh SP. 2010. Isolation and partial purification of an antimicrobial agent from halotolerant alkaliphilic Streptomyces aburaviensis strain Kut-8. World. J. Microbiol. Biotechnol. 26: 2081-2087. https://doi.org/10.1007/s11274-010-0394-7
  64. Vara J, Perez-Gonzalez JA, Jimenez A. 1985. Biosynthesis of puromycin by Streptomyces alboniger: Characterization of puromycin N-acetyltransferase. Biochemistry 24: 8074-8081. https://doi.org/10.1021/bi00348a036
  65. Yoon BD, Park CS, Kim MS, Ahn GH, Yang HJ. 2009. Microbial preparation, containing Streptomyces misonensis CJS-70, for resisting plant pathogens. Republic of Korea, KR2009129181 A 2009-12-16.