Microbiology and Biotechnology Letters (한국미생물·생명공학회지)

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Bioactivity of Metabolites from Actinomycetes Isolates from Red Sea, Egypt

  • Osman, Mohamed E. (Department of Botany and Microbiology, Faculty of Science, Helwan University) ;
  • El-nasr, Amany A. Abo (Department of Botany and Microbiology, Faculty of Science, Helwan University) ;
  • Hussein, Hagar M (Department of Botany and Microbiology, Faculty of Science, Helwan University) ;
  • Hamed, Moaz M (National Institute of Oceanography and Fisheries (NIOF))
  • Received : 2022.02.07
  • Accepted : 2022.05.19
  • Published : 2022.06.28
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Abstract

Actinomycetes isolated from marine habitats represent a promising source of bioactive substances. Here, we report on the isolation, identification, productivity enhancement and application of the bioactive compounds of Streptomyces qinglanensis H4. Eighteen marine actinomycetes were isolated and tested for resistance to seven bacterial diseases. Using 16S rRNA sequencing analysis (GenBank accession number MW563772), the most powerful isolate was identified as S. qinglanensis. Although the strain produced active compound(s) against a number of Gram-negative and Gram-positive bacteria, it failed to inhibit pathogenic fungi. The obtained inhibition zones were 22.0 ± 1.5, 20.0 ± 1, 16.0 ± 1, 12.0 ± 1, 22.0 ± 1 and 24.0 ± 1 mm against Bacillus subtilis ATCC 6633, Escherichia coli ATCC 19404, Enterococcus faecalis ATCC 29212, Pseudomonas aeruginosa ATCC 9027, Candida albicans ATCC 10231 and Staphylococcus aureus ATCC6538, respectively. To maximize bioactive compound synthesis, the Plackett-Burman design was used. The productivity increased up to 0.93-fold, when S. qinglanensis was grown in optimized medium composed of: (g/l) starch 30; KNO3 0.5; K2HPO4 0.25; MgSO4 0.25; FeSO4·7H2O, 0.01; sea water concentration (%) 100; pH 8.0, and an incubation period of 9 days. Moreover, the anticancer activity of S. qinglanensis was tested against two different cell lines: HepG2 and CACO. The inhibition activities were 42.96 and 57.14%, respectively. Our findings suggest that the marine S. qinglanensis strain, which grows well on tailored medium, might be a source of bioactive substances for healthcare companies.

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References

  1. Alkershi A, Menon N. 2011. Phytoplankton in polluted waters of the Red Sea coast of Yemen. J. Mar. Biol. Ass. India 53: 161-166.
  2. Hames-Kocabas EE, Atac U. 2012. Isolation strategies of marine-derived actinomycetes from sponge and sediment samples. J. Microbiol. Methods 88: 342-347. https://doi.org/10.1016/j.mimet.2012.01.010
  3. Bukhari M, Thomas A, Wong N. 2013. Culture conditions for optimal growth of actinomycetes from marine sponges, pp. 203-210. Developments in Sustainable Chemical and Bioprocess Technology, Ed. Springer.
  4. Cheng C, MacIntyre L, Abdelmohsen UR, Horn H, Polymenakou PN, Edrada-Ebel R, et al. 2015. Biodiversity, anti-trypanosomal activity screening, and metabolomic profiling of actinomycetes isolated from Mediterranean sponges. PLoS One 10: e0138528. https://doi.org/10.1371/journal.pone.0138528
  5. Abdelmohsen UR, Bayer K, Hentschel U. 2014. Diversity, abundance and natural products of marine sponge-associated actinomycetes. Nat. Prod. Rep. 31: 381-399. https://doi.org/10.1039/c3np70111e
  6. Abdelmohsen UR, Yang C, Horn H, Hajjar D, Ravasi T, Hentschel U. 2014. Actinomycetes from Red Sea sponges: sources for chemical and phylogenetic diversity. Mar. Drugs 12: 2771-2789. https://doi.org/10.3390/md12052771
  7. Grkovic T, Abdelmohsen UR, Othman EM, Stopper H, Edrada-Ebel R, Hentschel U, et al. 2014. Two new antioxidant actionsporin analogues from the calcium alginate beads culture of sponge-associated Actinokineospora sp. strain EG49. Bioorg. Med. Chem. Lett. 24: 5089-5092. https://doi.org/10.1016/j.bmcl.2014.08.068
  8. Hamed MM, Abdelfattah LS, Fahmy NM. 2019. Antimicrobial activity of marine actinomycetes and the optimization of culture conditions for the production of antimicrobial agent (s). J. Pure Appl. Microbiol. 13: 2177-2188. https://doi.org/10.22207/jpam.13.4.30
  9. Valli S, Suvathi SS, Aysha O, Nirmala P, Vinoth KP, 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
  10. Abdelfattah MS, Elmallah MIY, Hawas UW, Abou El-Kassema LT, Eid MAG. 2016. Isolation and characterization of marine-derived actinomycetes with cytotoxic activity from the Red Sea coast. Asian Pac. J. Trop. Biomed. 6: 651-657. https://doi.org/10.1016/j.apjtb.2016.06.004
  11. Risan MH, Jafar RA, Subhi SA. 2019. Isolation, characterization and antibacterial activity of a Rare Actinomycete: Saccharopolyspora sp. In Iraq.
  12. Sarika K, Sampath G, Govindarajan RK, Ameen F, Alwakeel S, Al Gwaiz HI, et al. 2021. Antimicrobial and antifungal activity of soil actinomycetes isolated from coal mine sites. Saudi J. Biol. Sci. 28: 3553-3558. https://doi.org/10.1016/j.sjbs.2021.03.029
  13. Cizeikiene D, Juodeikiene G, Paskevicius A, Bartkiene E. 2013. Antimicrobial activity of lactic acid bacteria against pathogenic and spoilage microorganism isolated from food and their control in wheat bread. Food Control 31: 539-545. https://doi.org/10.1016/j.foodcont.2012.12.004
  14. Shirling ET, Gottlieb D. 1966. Methods for characterization of Streptomyces species1. Int. J. Syst. Evol. Microbiol. 16: 313-340.
  15. David HA, Gunnink JL. 1997. The paired t test under artificial pairing. Am. Stat. 51: 9-12. https://doi.org/10.2307/2684684
  16. Pudi N, Varikuti GD, Badana AK, Gavara MM, Singh S, Malla R. 2016. Studies on optimization of growth parameters for enhanced production of antibiotic alkaloids by isolated marine actinomycetes. J. Appl. Pharm. Sci. 6: 181-188.
  17. Sengupta S, Pramanik A, Ghosh A, Bhattacharyya M. 2015. Antimicrobial activities of actinomycetes isolated from unexplored regions of Sundarbans mangrove ecosystem. BMC Microbiol. 15: 1-16. https://doi.org/10.1186/s12866-014-0320-5
  18. Balachandar R, Karmegam N, Saravanan M, Subbaiya R, Gurumoorthy P. 2018. Synthesis of bioactive compounds from vermicast isolated actinomycetes species and its antimicrobial activity against human pathogenic bacteria. Microb. Pathog. 121: 155-165. https://doi.org/10.1016/j.micpath.2018.05.027
  19. Gomha SM, Riyadh SM, Mahmmoud EA. 2015. Synthesis and anticancer activities of thiazoles, 1, 3-thiazines, and thiazolidine using chitosan-grafted-poly (vinylpyridine) as basic catalyst. Chem. Heterocycl. Compd. 91: 1227-1243.
  20. Naorungrote S, Chunglok W, Lertcanawanichakul M, Bangrak P. 2011. Actinomycetes producing anti-methicillin resistant Staphylococcus aureus from soil samples in Nakhon Si Thammarat. Walailak J. Sci. Technol. 8: 131-138.
  21. Shinde U, Phadke A, Nair A, Mungantiwar A, Dikshit V, Saraf M. 1999. Membrane stabilizing activity-a possible mechanism of action for the anti-inflammatory activity of Cedrus deodara wood oil. Fitoterapia 70: 251-257. https://doi.org/10.1016/S0367-326X(99)00030-1
  22. Snedecor G, William G. 1989. Statistical methods/george w. Snedecor and william g. Cochran. pp. 84-86, Lowa State UN Press, Ames.
  23. Behzad H, Ibarra MA, Mineta K, Gojobori T. 2016. Metagenomic studies of the Red Sea. Gene 576: 717-723. https://doi.org/10.1016/j.gene.2015.10.034
  24. Hamed M, Abdrabo M, Fahmy N. 2021. Distribution and characterization of actinomycetes in mangrove habitats (Red Sea, Egypt) with special emphasis on Streptomyces mutabilis M3MT483919. J. Pure Appl. Microbiol. 15: 246-261. https://doi.org/10.22207/JPAM.15.1.19
  25. Blunt JW, Copp BR, Keyzers RA, Munro MH, Prinsep MR. 2015. Marine natural products. Nat. Prod. Rep. 32: 116-211. https://doi.org/10.1039/c4np00144c
  26. Lu S, Wang J, Sheng R, Fang Y, Guo R. 2020. Novel bioactive polyketides isolated from marine actinomycetes: an update review from 2013 to 2019. Chem. Biodivers. 17: e2000562.
  27. Patel JD, Parmar M, Patel P, Rohit P, Taviyad R, Ansari P, et al. 2014. Dynamism of antimicrobial activity of actinomycetes-a case study from undisturbed microbial niche. Adv. Microbiol. 4: 45817.
  28. Abd-Elnaby H, Abo-Elala G, Abdel-Raouf U, Abd-elwahab 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
  29. Mustafa GA, Abd-Elgawad A, Abdel Haleem AM, Siam R. 2014. Egypt's Red Sea coast: phylogenetic analysis of cultured microbial consortia in industrialized sites. Front. Microbiol. 5: 363. https://doi.org/10.3389/fmicb.2014.00363
  30. Fahmy NM. 2020. Isolation and characterization of Streptomyces sp. NMF76 with potential antimicrobial activity from mangrove sediment, Red Sea, Egypt. Egyptian J. Aquatic. Biol. Fisheries 24: 479-495. https://doi.org/10.21608/ejabf.2020.117578
  31. Selim MSM, Abdelhamid SA, Mohamed SS. 2021. Secondary metabolites and biodiversity of actinomycetes. J. Genet. Eng. Biotechnol. 19: 72. https://doi.org/10.1186/s43141-021-00156-9
  32. Xu D, Tian E, Kong F, Hong K. 2020. Bioactive molecules from mangrove Streptomyces qinglanensis 172205. Mar. Drugs 18: 255. https://doi.org/10.3390/md18050255
  33. Hassan SWM, El Sersy NA, Abdelwahab AE-S, Ali MA-R. 2017. Statistical optimization and valuable applications of bioactive compounds produced by marine Pseudoalteromonas piscicida. J. Appl. Pharm. Sci. 7: 084-093.
  34. Pal D, Patel G, Dobariya P, Nile SH, Pande AH, Banerjee UC. 2021. Optimization of medium composition to increase the expression of recombinant human interferon-β using the Plackett-Burman and central composite design in E. coli SE1. 3 Biotech. 11: 1-10.
  35. Wefky S, Abou-Elela G, El-Bestawy E. 2009. Optimization of fermentation conditions for bioactive compounds production by marine bacterium Enterococcus faecium. J. Appl. Sci. Res. 5: 1445-1454.
  36. Aliero AA, Adam AS, Ntulume I, Bagudo AI, Kudu AAB, Ondieki MC, et al. 2018. Molecular characterization and optimization of bioactive compounds production of three Actinomycetes spp isolated from waste dump soil from Western Uganda. Curr. Trends Biotechnol. Pharm. 12: 230-244.
  37. El-Sersy NA, Abou-Elela GM. 2006. Antagonistic effect of marine Nocardia brasiliensis against the fish pathogen Vibrio damsela: Application of Plackett- Burman experimental design to evaluate factors affecting the production of the antibacterial agent. Int. J. Ocean. Oceanography 1: 141-150.
  38. Tresner H, Hayes JA, Backus E. 1968. Differential tolerance of streptomycetes to sodium chloride as a taxonomic aid. Appl. Microbiol. 16: 1134-1136. https://doi.org/10.1128/am.16.8.1134-1136.1968
  39. Akond MA, Jahan MN, Sultana N, Rahman F. 2016. Effect of temperature, pH and NaCl on the isolates of Actinomycetes from straw and compost samples from Savar, Dhaka, Bangladesh. Am. J. Microbiol. Immunol. 1: 10-15.
  40. Akond MA, Khan ZU. 2005. Role of carbon sources and heavy metals on growth and nitrogen fixing potential of Azospirillum and the effect of Azospirillum strains on vegetative growth of rice. J. Environ. Sci. 3: 1-8.
  41. Khalifa SA, Elias N, Farag MA, Chen L, Saeed A, Hegazy M-EF, et al. 2019. Marine natural products: A source of novel anticancer drugs. Mar. Drugs 17: 491. https://doi.org/10.3390/md17090491
  42. Yip WK, Cheenpracha S, Chang LC, Ho CC, Seow HF. 2010. Anti-proliferative and anti-invasive properties of a purified fraction from Streptomyces sp. H7372. Int. J. Oncol. 37: 1229-1241.
  43. Procopio REdL, Silva IRd, Martins MK, Azevedo JLd, Araujo JMd. 2012. Antibiotics produced by Streptomyces. Braz. J. Infect. Dis. 16: 466-471. https://doi.org/10.1016/j.bjid.2012.08.014
  44. Law JW-F, Law LN-S, Letchumanan V, Tan LT-H, Wong SH, Chan K-G, et al. 2020. Anticancer drug discovery from microbial sources: the unique mangrove streptomycetes. Molecules 25: 5365. https://doi.org/10.3390/molecules25225365
  45. Fahmy NM, Abdel-Tawab AM. 2021. Isolation and characterization of marine sponge-associated Streptomyces sp. NMF6 strain producing secondary metabolite (s) possessing antimicrobial, antioxidant, anticancer, and antiviral activities. J. Genet. Eng. Biotechnol. 19: 102. https://doi.org/10.1186/s43141-021-00203-5
  46. Xu D, Ma M, Liu Y, Zhou T, Wang K, Deng Z, Hong K. 2015. PreQ0 base, an unusual metabolite with anti-cancer activity from Streptomyces qinglanensis 172205. Anti-Cancer Agents Med. Chem. 15: 285-290. https://doi.org/10.2174/1871520614666141027144653
  47. Yoganandam GP, Ilango K, Sucharita D. 2010. Evaluation of anti-inflammatory and membrane stabilizing properties of various extracts of Punica granatum L.(Lythraceae). Int. J. PharmTech Res. 2: 1260-1263.
  48. Pooja S, Aditi T, Naine SJ, Devi CS. 2017. Bioactive compounds from marine Streptomyces sp. VITPSA as therapeutics. Front. Biol. 12: 280-289. https://doi.org/10.1007/s11515-017-1459-x
  49. Thosar A, Satpathy P, Devi CS. 2020. Marine Streptomyces sp. VITASP as a source of new bioactive secondary metabolites. Curr. Bioactive Compounds 16: 611-617. https://doi.org/10.2174/1573407214666180904100049
  50. Girao M, Ribeiro I, Ribeiro T, Azevedo IC, Pereira F, Urbatzka R, et al. 2019. Actinobacteria isolated from Laminaria ochroleuca: a source of new bioactive compounds. Front. Microbiol. 10: 683. https://doi.org/10.3389/fmicb.2019.00683
  51. Dholakiya RN, Kumar R, Mishra A, Mody KH, Jha B. 2017. Antibacterial and antioxidant activities of novel actinobacteria strain isolated from Gulf of Khambhat, Gujarat. Front. Microbiol. 8: 2420. https://doi.org/10.3389/fmicb.2017.02420