Isolation and structure elucidation of phenazine derivative from Streptomyces sp. strain UICC B-92 isolated from Neesia altissima (Malvaceae)
,
Abstract
Background and Objectives: Endophytic actinomycetes have been known as a promising source for new antibiotics discovery against susceptible and resistant forms of pathogenic microorganisms. This study was aimed at determining antibacterial compound from Streptomyces sp. strain B-92 isolated from a medicinal plant Neesia altissima.
Materials and Methods: Streptomyces sp. strain UICC B-92 was endophytic actinomycetes of N. altissima that obtained from Universitas Indonesia Culture Collection (UICC). Isolation and determination of bioactive compound were carried out using thin layer chromatography (TLC), nuclear magnetic resonance spectroscopy (NMR), and liquid chromatography mass spectrometry (LC-MS) analyses. An in vitro antibacterial assay of pure bioactive compound from the endophytic actinomycetes strain was performed against Bacillus cereus strain ATCC 10876, Escherichia coli strain ATCC 25922, Salmonella typhimurium strain ATCC 25241, Shigella flexneri strain ATCC 12022 and Staphylococcus aureus strain ATCC 25923.
Results: The bioactive compound was identified as 4-((3S,4R,5S)-3,4,5-trihydroxy-6-(hydroxymethyl) tetrahydro-2H-pyran-2-yloxy) phenazine-1-carboxylic acid. In vitro antimicrobial assay showed that bioactive compound of Streptomyces sp. strain UICC B-92 exhibited antagonistic activities against two Gram-positive bacteria, viz, B. cereus strain ATCC 10876 and S. aureus strain ATCC 25923.
Conclusion: The findings of this research showed that, bioactive compound of Streptomyces sp. strain UICC B-92 is suggested a new compound based on glycoside structure and its position.
1. World Health Organization (2014). Antimicrobial resistance: global report on surveillance.
2. Nathan C, Cars O. Antibiotic resistance-problems, progress, and prospects. N Engl J Med 2014;371:1761-1763.
3. Strobel G, Daisy B. Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 2003;67:491-502.
4. Bérdy J. Bioactive microbial metabolites. J Antibiot (Tokyo) 2005;58:1-26.
5. Castillo U, Strobel GA, Ford EJ, Hess WM, Porter H, Jensen JB, et al. Munumbicins, wide-spectrum antibiotics produced by Streptomyces NRRL 30562, endophytic on Kennedia nigriscans. Microbiology 2002;148:2675-2685.
6. Castillo U, Harper JK, Strobel GA, Sears J, Alesi K, Ford E, et al. Kakadumycins, novel antibiotics from Streptomyces sp. NRRL 30566, an endophyte of Grevillea pteridifolia. FEMS Microbiol Lett 2003;224:183-190.
7. Ding L, Armin M, Heinz-Herbert F, Wen-Han L, Christian H. A family of multicyclic indolosesquiterpenes from a bacterial endophyte. Org Biomol Chem 2011;9:4029-4031.
8. Ezra D, Castillo UF, Strobel GA, Hess WM, Porter H. Coronamycins, peptide antibiotics produced by a verticillate Streptomyces sp. (MSU-2110) endophytic on Monstera sp. Microbiology 2004;150:785-793.
9. Chung RCK (1998). Sarcotheca diversifolia. In: Plant Resources of South-East Asia No 5(3). Timber Trees: Lesser-Known Timbers. Eds, MSM Sosef, LT Hong, S Prawirohatmodjo. Backhuys Publishers, Leiden, the Netherlands, pp. 435-448.
10. Soepadmo S (1960). A monograph of the genus Neesia Blume (Bombacaceae). In: Reinwardtia. Herbarium Bogoriense Publishing, 5th vol. Botanical Garden, Bogor, Indonesia, pp. 481-508.
11. Pratiwi RH, Hidayat I, Hanafi M, Mangunwardoyo W. Identification and characterization of three endophytic bacteria from Neesia altissima (Malvaceae) antagonistic to diarrhea-causing bacteria. Malays J Microbiol 2016;12:300-307.
12. Pratiwi RH, Hidayat I, Hanafi M, Mangunwardoyo W. Antibacterial compound produced by Pseudomonas aeruginosa strain UICC B-40, an endophytic bacterium isolated from Neesia altissima. J Microbiol 2017;55:289-295.
13. Remali J, Sarmin NM, Ng CL, Tiong JJL, Aizat WM, Keong LK, et al. Genomic characterization of a new endophytic Streptomyces kebangsaanensis identifies biosynthetic pathway gene clusters for novel phenazine antibiotic production. PeerJ 2017;5:e3738.
14. Luo Q, Hu H, Peng H, Zhang X, Wang W. Isolation and structural identification two bioactive phenazines from Streptomyces griseoluteus P510. Chin J Chem Eng 2015;23:699-703.
15. Johnson LE, Dietz A. Lomofungin, a new antibiotic produced by Streptomyces lomondensis sp. Appl Microbiol 1969;17:755-759.
16. Gebhardt K, Schimana J, Krastel P, Dettner L, Rheinheimer J, Zeeck A, et al. Endophenazines, A.-D., new phenazine antibiotics from the arthropod associated endosymbiont Streptomyces anulatus. I. Taxonomy, fermentation, isolation and biological activities. J Antibiot 2002;55:794-800.
17. Song Y, Huang H, Chen Y, Ding J. Cytotoxic and antibacterial marfiraquinocins from the deep South China Sea-derived Streptomyces niveus SCSIO 3406. J Nat Prod 2013;76:2263-2268.
18. Abdelfattah MS, Toume K, Ishibashi M. Izumiphenazines A-C: isolation and structure elucidation of phenazine derivatives from Streptomyces sp. IFM 11204. J Nat Prod 2010;73:1999-2002.
19. Abdelfattah MS, Toume K, Ishibashi M. Isolation and structure elucidation of izuminosides A-C: a rare phenazine glycosides from Streptomyces sp. IFM 11260. J Antibiot 2011;64:271-275.
20. Pratiwi RH, Hidayat I, Mangunwardoyo W (2018). Molecular identification of endophytic bacteria from Neesia altissima Bl. (Malvaceae) antagonistic to diarrhea-causing bacteria. In: Proceedings of the 18th Science Council of Asia Conference: “Role of Science for Society: Strategies towards SDGs in Asia”. Tokyo, Japan. pp. 6.
21. Cao L, Qiu Z, You J, Tan H, Zhou S. Isolation and characterization of endophytic Streptomycetes antagonists of fusarium wilt pathogen from surface sterilized banana roots. FEMS Microbiol Lett 2005;247:147-152.
22. Saha BC, Cotta MA. Comparison of pretreatment strategies for enzymatic saccharification and fermentation of barley straw to ethanol. N Biotechnol 2010;27:10-16.
23. Pratiwi RH, Hanafi M, Artanti N, Pratiwi RD. Bioactivity of antibacterial compounds produced by endophytic actinomycetes from Neesia altissima. J Trop Life Science 2018;8:37-42.
24. Narayana KJP, Prabhakar P, Vijayalakshmi M, Venkateswarlu Y, Krishna PSJ. Study on bioactive compounds from Streptomyces sp. ANU 6277. Pol J Microbiol 2008;57:35-39.
25. Schwalbe R, Steele-Moore L, Goodwin AC (2007). Antimicrobial Susceptibility Testing Protocols. 1st ed. CRC Press. New York pp. 75-79.
26. Kai J, Matoh M, Tsukidate K. A new method for preparing electron microscopic specimens of Helicobacter pylori. Med Electron Microsc 1999;32:62-65.
27. Hui J, Wang W, Hu H, Peng H, Zhang X. Streptomyces griseoruber Y1B, a novel Streptomyces for 1-Hydroxyphenazine production. J Appl Biotechnol 2014;2:13-31.
28. Bunbamrung N, Dramae A, Srichomthong K, Supothina S, Pittayakhajonwut P. Streptophenazines I–L from Streptomyces sp. BCC21835. Phytochem Lett 2014;10:91-94.
29. Kennedy RK, Naik PR, Veena V, Lakshmi BS, Lakshmi P, et al. 5-methyl phenazine-1-carboxylic acid: a novel bioactive metabolite by a rhizosphere soil bacterium that exhibits potent antimicrobial and anticancer activities. Chem Biol Interact 2015;231:71-82.
30. Guttenberger N, Blankenfeldt W, Breinbauer R. Recent developments in the isolation, biological function, biosynthesis, and synthesis of phenazine natural products. Bioorg Med Chem 2017;25:6149-6166.
31. Sarmin NIM, Tan GYA, Franco CMM, Edrada-Ebel R, Latip J, Zin NM. Streptomyces kebangsaanensis sp. nov., an endophytic actinomycete isolated from an ethnomedicinal plant, which produces phenazine-1-carboxylic acid. Int J Syst Evol Microbiol 2013;63:3733-3738.
32. Umezawa H, Hayano S, Maeda K, Ogata Y, Okami Y. On a new antibiotic, griseolutein, produced by Streptomyces. Jpn Med J (Natl Inst Health Jpn) 1950;3:111-117.
33. Mavrodi DV, Blankenfeldt W, Thomashow LS. Phenazine compounds in fluorescent Pseudomonas spp. biosynthesis and regulation. Annu Rev Phytopathol 2006;44:417-445.
34. Diver JM, Wise R. Morphological and biochemical changes in Escherichia coli after exposure to ciprofloxacin. J Antimicrob Chemother 1986;18 Suppl D:31-41.
35. Sasidharan S, Darah I, Jain K. Antimicrobial activity and wound healing potential on infected rat of Gracilaria changii methanolic extract. Pharmacologyonline 2008;2:661-670.
36. Delaney SM, Mavrodi DV, Bonsall RF, Thomashow LS. phzO, a gene for biosynthesis of 2-hydroxylated phenazine compounds in Pseudomonas aureofaciens 30-84. J Bacteriol 2001;183:318-327.
37. Mavrodi DV, Peever TL, Mavrodi OV, Parejko JA, Raaijmakers JM, Lemanceau P, et al. Diversity and evolution of the phenazine biosynthesis pathway. Appl Environ Microbiol 2010;76:866-879.
38. Sakhtah H, Price-Whelan A, Dietrich LEP (2013). Regulation of phenazine biosynthesis. In: Microbial Phenazines: Biosynthesis, Agriculture and Health. Eds, S Chincholkar, L Thomashow. Springer-Verlag, Heidelberg, Berlin, pp. 19-42.
39. Pierson III LS, Pierson EA. Metabolism and function of phenazines in bacteria: impacts on the behavior of bacteria in the environment and biotechnological processes. Appl Microbiol Biotechnol 2010;86:1659-1670.
40. Haagen Y, Glück K, Fay K, Heide L. A gene cluster for prenylated phenazine biosynthesis in Streptomyces cinnamonensis DSM 1042. Chembiochem 2006;7:2016-2027.
41. Laursen J, Nielsen J. Phenazine natural products: biosynthesis, synthetic analogues, and biological activity. Chem Rev 2004;104:1663-1686.
2. Nathan C, Cars O. Antibiotic resistance-problems, progress, and prospects. N Engl J Med 2014;371:1761-1763.
3. Strobel G, Daisy B. Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 2003;67:491-502.
4. Bérdy J. Bioactive microbial metabolites. J Antibiot (Tokyo) 2005;58:1-26.
5. Castillo U, Strobel GA, Ford EJ, Hess WM, Porter H, Jensen JB, et al. Munumbicins, wide-spectrum antibiotics produced by Streptomyces NRRL 30562, endophytic on Kennedia nigriscans. Microbiology 2002;148:2675-2685.
6. Castillo U, Harper JK, Strobel GA, Sears J, Alesi K, Ford E, et al. Kakadumycins, novel antibiotics from Streptomyces sp. NRRL 30566, an endophyte of Grevillea pteridifolia. FEMS Microbiol Lett 2003;224:183-190.
7. Ding L, Armin M, Heinz-Herbert F, Wen-Han L, Christian H. A family of multicyclic indolosesquiterpenes from a bacterial endophyte. Org Biomol Chem 2011;9:4029-4031.
8. Ezra D, Castillo UF, Strobel GA, Hess WM, Porter H. Coronamycins, peptide antibiotics produced by a verticillate Streptomyces sp. (MSU-2110) endophytic on Monstera sp. Microbiology 2004;150:785-793.
9. Chung RCK (1998). Sarcotheca diversifolia. In: Plant Resources of South-East Asia No 5(3). Timber Trees: Lesser-Known Timbers. Eds, MSM Sosef, LT Hong, S Prawirohatmodjo. Backhuys Publishers, Leiden, the Netherlands, pp. 435-448.
10. Soepadmo S (1960). A monograph of the genus Neesia Blume (Bombacaceae). In: Reinwardtia. Herbarium Bogoriense Publishing, 5th vol. Botanical Garden, Bogor, Indonesia, pp. 481-508.
11. Pratiwi RH, Hidayat I, Hanafi M, Mangunwardoyo W. Identification and characterization of three endophytic bacteria from Neesia altissima (Malvaceae) antagonistic to diarrhea-causing bacteria. Malays J Microbiol 2016;12:300-307.
12. Pratiwi RH, Hidayat I, Hanafi M, Mangunwardoyo W. Antibacterial compound produced by Pseudomonas aeruginosa strain UICC B-40, an endophytic bacterium isolated from Neesia altissima. J Microbiol 2017;55:289-295.
13. Remali J, Sarmin NM, Ng CL, Tiong JJL, Aizat WM, Keong LK, et al. Genomic characterization of a new endophytic Streptomyces kebangsaanensis identifies biosynthetic pathway gene clusters for novel phenazine antibiotic production. PeerJ 2017;5:e3738.
14. Luo Q, Hu H, Peng H, Zhang X, Wang W. Isolation and structural identification two bioactive phenazines from Streptomyces griseoluteus P510. Chin J Chem Eng 2015;23:699-703.
15. Johnson LE, Dietz A. Lomofungin, a new antibiotic produced by Streptomyces lomondensis sp. Appl Microbiol 1969;17:755-759.
16. Gebhardt K, Schimana J, Krastel P, Dettner L, Rheinheimer J, Zeeck A, et al. Endophenazines, A.-D., new phenazine antibiotics from the arthropod associated endosymbiont Streptomyces anulatus. I. Taxonomy, fermentation, isolation and biological activities. J Antibiot 2002;55:794-800.
17. Song Y, Huang H, Chen Y, Ding J. Cytotoxic and antibacterial marfiraquinocins from the deep South China Sea-derived Streptomyces niveus SCSIO 3406. J Nat Prod 2013;76:2263-2268.
18. Abdelfattah MS, Toume K, Ishibashi M. Izumiphenazines A-C: isolation and structure elucidation of phenazine derivatives from Streptomyces sp. IFM 11204. J Nat Prod 2010;73:1999-2002.
19. Abdelfattah MS, Toume K, Ishibashi M. Isolation and structure elucidation of izuminosides A-C: a rare phenazine glycosides from Streptomyces sp. IFM 11260. J Antibiot 2011;64:271-275.
20. Pratiwi RH, Hidayat I, Mangunwardoyo W (2018). Molecular identification of endophytic bacteria from Neesia altissima Bl. (Malvaceae) antagonistic to diarrhea-causing bacteria. In: Proceedings of the 18th Science Council of Asia Conference: “Role of Science for Society: Strategies towards SDGs in Asia”. Tokyo, Japan. pp. 6.
21. Cao L, Qiu Z, You J, Tan H, Zhou S. Isolation and characterization of endophytic Streptomycetes antagonists of fusarium wilt pathogen from surface sterilized banana roots. FEMS Microbiol Lett 2005;247:147-152.
22. Saha BC, Cotta MA. Comparison of pretreatment strategies for enzymatic saccharification and fermentation of barley straw to ethanol. N Biotechnol 2010;27:10-16.
23. Pratiwi RH, Hanafi M, Artanti N, Pratiwi RD. Bioactivity of antibacterial compounds produced by endophytic actinomycetes from Neesia altissima. J Trop Life Science 2018;8:37-42.
24. Narayana KJP, Prabhakar P, Vijayalakshmi M, Venkateswarlu Y, Krishna PSJ. Study on bioactive compounds from Streptomyces sp. ANU 6277. Pol J Microbiol 2008;57:35-39.
25. Schwalbe R, Steele-Moore L, Goodwin AC (2007). Antimicrobial Susceptibility Testing Protocols. 1st ed. CRC Press. New York pp. 75-79.
26. Kai J, Matoh M, Tsukidate K. A new method for preparing electron microscopic specimens of Helicobacter pylori. Med Electron Microsc 1999;32:62-65.
27. Hui J, Wang W, Hu H, Peng H, Zhang X. Streptomyces griseoruber Y1B, a novel Streptomyces for 1-Hydroxyphenazine production. J Appl Biotechnol 2014;2:13-31.
28. Bunbamrung N, Dramae A, Srichomthong K, Supothina S, Pittayakhajonwut P. Streptophenazines I–L from Streptomyces sp. BCC21835. Phytochem Lett 2014;10:91-94.
29. Kennedy RK, Naik PR, Veena V, Lakshmi BS, Lakshmi P, et al. 5-methyl phenazine-1-carboxylic acid: a novel bioactive metabolite by a rhizosphere soil bacterium that exhibits potent antimicrobial and anticancer activities. Chem Biol Interact 2015;231:71-82.
30. Guttenberger N, Blankenfeldt W, Breinbauer R. Recent developments in the isolation, biological function, biosynthesis, and synthesis of phenazine natural products. Bioorg Med Chem 2017;25:6149-6166.
31. Sarmin NIM, Tan GYA, Franco CMM, Edrada-Ebel R, Latip J, Zin NM. Streptomyces kebangsaanensis sp. nov., an endophytic actinomycete isolated from an ethnomedicinal plant, which produces phenazine-1-carboxylic acid. Int J Syst Evol Microbiol 2013;63:3733-3738.
32. Umezawa H, Hayano S, Maeda K, Ogata Y, Okami Y. On a new antibiotic, griseolutein, produced by Streptomyces. Jpn Med J (Natl Inst Health Jpn) 1950;3:111-117.
33. Mavrodi DV, Blankenfeldt W, Thomashow LS. Phenazine compounds in fluorescent Pseudomonas spp. biosynthesis and regulation. Annu Rev Phytopathol 2006;44:417-445.
34. Diver JM, Wise R. Morphological and biochemical changes in Escherichia coli after exposure to ciprofloxacin. J Antimicrob Chemother 1986;18 Suppl D:31-41.
35. Sasidharan S, Darah I, Jain K. Antimicrobial activity and wound healing potential on infected rat of Gracilaria changii methanolic extract. Pharmacologyonline 2008;2:661-670.
36. Delaney SM, Mavrodi DV, Bonsall RF, Thomashow LS. phzO, a gene for biosynthesis of 2-hydroxylated phenazine compounds in Pseudomonas aureofaciens 30-84. J Bacteriol 2001;183:318-327.
37. Mavrodi DV, Peever TL, Mavrodi OV, Parejko JA, Raaijmakers JM, Lemanceau P, et al. Diversity and evolution of the phenazine biosynthesis pathway. Appl Environ Microbiol 2010;76:866-879.
38. Sakhtah H, Price-Whelan A, Dietrich LEP (2013). Regulation of phenazine biosynthesis. In: Microbial Phenazines: Biosynthesis, Agriculture and Health. Eds, S Chincholkar, L Thomashow. Springer-Verlag, Heidelberg, Berlin, pp. 19-42.
39. Pierson III LS, Pierson EA. Metabolism and function of phenazines in bacteria: impacts on the behavior of bacteria in the environment and biotechnological processes. Appl Microbiol Biotechnol 2010;86:1659-1670.
40. Haagen Y, Glück K, Fay K, Heide L. A gene cluster for prenylated phenazine biosynthesis in Streptomyces cinnamonensis DSM 1042. Chembiochem 2006;7:2016-2027.
41. Laursen J, Nielsen J. Phenazine natural products: biosynthesis, synthetic analogues, and biological activity. Chem Rev 2004;104:1663-1686.
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| Issue | Vol 12 No 2 (2020) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v12i2.2618 | |
| Keywords | ||
| Actinomycetes; Antibacterial; Endophyte; Gram-positive bacteria | ||
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How to Cite
1.
Pratiwi R, Hidayat I, Hanafi M, Mangunwardoyo W. Isolation and structure elucidation of phenazine derivative from Streptomyces sp. strain UICC B-92 isolated from Neesia altissima (Malvaceae). Iran J Microbiol. 2020;12(2):127-137.
