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References

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    Pubmed CrossRef
  2. Ando T, Miyashiro S, Hirayama K, Kida T, Shibai H, Murai A, Udaka S. 1987. New streptothricin-group antibiotics, AN201 I, II and III. II. Chemical structures. J. Antibiot. 40: 11401145.
    CrossRef
  3. Aquino LC, Hicks CA, Scalon MC, Lima MG, Lemos MD, Paludo GR, et al. 2014. Prevalence and phylogenetic analysis of haemoplasmas from cats infected with multiple species. J. Microbiol. Methods 107: 189-196.
    Pubmed PMC CrossRef
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    Pubmed
  5. Benning VR, Mathers JJ, 1999. Comparison of agar dilution and broth microdilution methods of anaerobic antimicrobial susceptibility testing using several veterinary antibiotics against Clostridium perfringens strains originating from porcine and avian sources. Anaerobe 5: 561-569.
    CrossRef
  6. Bieber B, Nuske J, Ritzau M, Grafe U. 1998. Alnumycin a new naphthoquinone antibiotic produced by an endophytic Streptomyces sp. J. Antibiot. 51: 381-382.
    Pubmed CrossRef
  7. Bisti E, Monciardini P, Cavaletti L, Bamonte R, Lazzarini A, Sosio M, Donadio S. 2006. Antibiotic-producing ability by representatives of a newly discovered lineage of actinomycetes. Microbiology 152: 675-683.
    Pubmed CrossRef
  8. Brian P, Riggle PJ, Santos RA, Champness WC. 1996. Global negative regulation of Streptomyces coelicolor antibiotic synthesis mediated by an absA-encoded putative signal transduction system. J. Bacteriol. 178: 3221-3231.
    Pubmed PMC CrossRef
  9. Chae HJ, Kang JS, Byun JO, Han KS, Kim DU, Oh SM, et al. 2000. Molecular mechanism of staurosporine-induced apoptosis in osteoblasts. Pharmacol. Res. 42: 373-381.
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  10. Charoensopharat K, Thummabenjapone P, Sirithorn P, Thammasirirak S. 2008. Antibacterial substance produced by Streptomyces sp. No. 87. Afr. J. Biotechnol. 7: 1362-1368.
  11. Christiano RSC, Reilly CC, Miller WP, Scherm H. 2010. Oxytetracycline dynamics on peach leaves in relation to temperature, sunlight, and simulated rain. Plant Dis. 94:1213-1218.
    CrossRef
  12. Christova K, Sholeva Z, Chipeva V. 1995. Application of molecular biological methods in taxonomy of genus Streptomyces. J. Cult. Collect. 1: 3-10.
  13. Commbs JT, Franco CMM. 2003. Isolation and identification of actinobacteria from surface-sterilized wheat roots. Appl. Environ. Microbiol. 69: 5603–5608.
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  14. Cordell GA. 2008. The Alkaloids: Chemistry and Biology, pp. 3-96. Vol. 65, Academic Press, San Diego, California.
  15. Dalziel K, Dykes PJ, Marks R. 1987. The effect of tetracycline and erythromycin in a model of acne-type inflammation. Br. J. Exp. Pathol. 68: 67-70.
    Pubmed PMC
  16. Davisson JW, Tanner Jr FW, Finlay AC, Solomons IA. 1951. Rimocidin, a new antibiotic. Antibiot. Chemother. (Northfield) 1: 289-290.
  17. Djinni I, Defant A, Kecha M, Mancini I. 2014. Metabolite profile of marine-derived endophytic Streptomyces sundarbansensis WR1L1S8 by liquid chromatography–mass spectrometry and evaluation of culture conditions on antibacterial activity and mycelial growth. J. Appl. Microbiol. 116: 39-50.
    Pubmed CrossRef
  18. Deseo MA, Hunter lS, Waterman PG. 2005. Novel polyketide metabolites from Streptomyces rimosus mutant strain R1059. J. Antibiot. 58: 822-827.
    Pubmed CrossRef
  19. Dung NT, Kim JM, Kang SC. 2008. Chemical composition, antimicrobial and antioxidant activities of the essential oil and the ethanol extract of Cleistocalyx operculatus (Roxb.) Merr and Perry buds. Food Chem. Toxicol. 46: 3632-3639.
    Pubmed CrossRef
  20. El-Hendaw HH, Osman ME, Sorour NM. 2005. Biological control of bacterial spot of tomato caused by Xanthomonas campestris pv. vesicatoria by Rahnella aquatilis. Microbiol. Res. 160: 343-352.
    Pubmed CrossRef
  21. El-Hussein AA, Alhason REM, Abdelwahab SA, El-Sidig MA. 2014. Isolation and identification of Streptomyces rochei strain active against phytopathogenic fungi. Br. Microbiol. Res. J. 4: 1057-1068.
    CrossRef
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    Pubmed CrossRef
  23. Emmert EAB, Handelsman J. 1999. Biocontrol of plant disease: a (gram-) positive perspective. FEMS Microbiol. Lett. 171: 1-9.
    Pubmed CrossRef
  24. Forbes JC, Watson RD. 1992. Plants in Agriculture. Cambridge University Press, New York.
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    Pubmed CrossRef
  26. Fuente RDL, Sonawane ND, Arumainayagam D, Verkman AS. 2006. Small molecules with antimicrobial activity against E. coli and P. aeruginosa identified by high-throughput screening. Br. J. Pharmacol. 149: 551-559.
    Pubmed PMC CrossRef
  27. Gerrettson-Cornell L. 2005. Note on the Actinomycetes of the Streptomyces hygroscopicus-like Complex in Tradition Taxonomy, pp 1-18. Vol. 70, Forest Resources Research, Sydney.
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    CrossRef
  29. Hosoya T, Yamamoto Y, Uehara Y, Hayashi M, Komiyama K, Ishibashi M. 2005. New cytotoxic bisindole alkaloids with protein tyrosine kinase inhibitory activity from a myxomycete Lycogala epidendrum. Bioorg. Med. Chem. Lett. 15: 2776-2780.
    Pubmed CrossRef
  30. Igarashi M, Shida T, Sasaki Y, Kinoshita N, Naganawa H, Hamada M, Takeuchi T. 1999. Vinylamycin, a new depsipeptide antibiotic, from Streptomyces sp. J. Antibiot. (Tokyo) 52: 873-879.
    CrossRef
  31. Igarashi Y, Ogawa M, Sato Y, Saito N, Yoshida R, Kunoh H, et al. 2000. Fistupyrone, a novel inhibitor of the infection of Chinese cabbage by Alternaria brassicicola, from Streptomyces sp. TP-A0569. J. Antibiot. 53: 1117-1122.
    Pubmed CrossRef
  32. Jensen PR, Williams PG, Oh DC, Zeigler L, Fenical W. 2007. Species-specific secondary metabolite production in marine actinomycetes of the genus Salinispora. Appl. Environ. Microbiol. 73: 1146-1152.
    Pubmed PMC CrossRef
  33. Kaluzna M, Pulawska J, Waleron M, Sobiczewski P. 2014. The genetic characterization of Xanthomonas arboricola pv. juglandis, the causal agent of walnut blight in Poland. Plant Pathol. 63: 1404-1416.
    CrossRef
  34. Kim JD, Han JW, Lee SC, Lee D, Hwang IC, Kim BS. 2011. Disease control effect of strevertenes produced by Streptomyces psammoticus against tomato Fusarium wilt. J. Agric. Food Chem. 95: 1893-1899.
    Pubmed CrossRef
  35. King RR, Lawrence CH, Calhoun LA. 1992. Chemistry of phytotoxins associated with Streptomyces scabies, the causal organism of potato common scab. J. Agric. Food Chem. 40:834-837.
    CrossRef
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    CrossRef
  38. Li J, Wang N. 2014. Foliar application of biofilm formationinhibiting compounds enhances control of citrus canker caused by Xanthomonas citri subsp. citri. Phytopathology 104:134-142.
    Pubmed CrossRef
  39. Li XB, Tang JS, Gao H, Ding R, Li J, Hong K, Yao XS. 2011. A new staurosporine analog from Actinomycetes Streptomyces sp. (172614). J. Asian Nat. Prod. Res. 13: 765-769.
    Pubmed CrossRef
  40. Nasher MA, Hay RJ, Mahgoub ES, Gumaa SA. 1989. In vitro studies of antibiotic sensitivities of Streptomyces somaliensis a cause of human actinomycetoma. Trans. R Soc. Trop. Med. Hyg. 83: 265-268.
    CrossRef
  41. Ndonde MJM, Semu E. 2001. Preliminary characterization of some Streptomyces species from four Tanzanian soils and their antimicrobial potential against selected plant and animal pathogenic bacteria. World J. Microbiol. Biotechnol. 16:595-599.
    CrossRef
  42. Omura S, Iwai Y, Hirano A, Nakagawa A, Awaya J, Tsuchya H, et al. 1977. A new alkaloid AM-2282 of Streptomyces origin: taxonomy, fermentation, isolation and preliminary characterization. J. Antibiot. 30: 275-282.
    Pubmed CrossRef
  43. Omura S, Iwai Y, Takahashi Y, Sadakane N, Nakagawa A, Oiwa H, et al. 1979. Herbimycin, a new antibiotic produced by a strain of Streptomyces. J. Antibiot. 32: 255-261.
    Pubmed CrossRef
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    CrossRef
  45. Peng FJ, Zhou LJ, Ying GG, Liu YS, Zhao JL. 2014. Antibacterial activity of the soil-bound antimicrobials oxytetracycline and ofloxacin. Environ. Toxicol. Chem. 33:776-783.
    Pubmed CrossRef
  46. Petkovic H, Cullum J, Hranueli D, Hunter IS, Peric-Concha N, Pigac J, et al. 2006. Genetics of Streptomyces rimosus, the oxytetracycline producer. Microbiol. Mol. Biol. Rev. 70: 704-728.
    Pubmed PMC CrossRef
  47. Pickens LB, Tang Y. 2010. Oxytetracycline biosynthesis. J. Biol. Chem. 285: 27509-27515.
    Pubmed PMC CrossRef
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    CrossRef
  49. Quintana ET, Wierzbicka K, Mackiewicz P, Osman A, Fahal AH, Hamid ME, et al. 2008. Streptomyces sudanensis sp. nov., a new pathogen isolated from patients with actinomycetoma. Antonie Van Leeuwenhoek 93: 305-313.
    Pubmed CrossRef
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  51. Rao M , Feng L, R uan L , Ge M , Sheng X. 2 013. U PLC- MSbased metabolomic study of Streptomyces strain HCCB10043 under different pH conditions reveals important pathways affecting the biosynthesis of A21978C compounds. Anal. Lett. 46: 2305-2318.
    CrossRef
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    CrossRef
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    Pubmed CrossRef
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Article

Research article

J. Microbiol. Biotechnol. 2015; 25(8): 1265-1274

Published online August 28, 2015 https://doi.org/10.4014/jmb.1503.03005

Copyright © The Korean Society for Microbiology and Biotechnology.

Metabolomics-Based Chemotaxonomic Classification of Streptomyces spp. and Its Correlation with Antibacterial Activity

Mee Youn Lee 1, Hyang Yeon Kim 1, Sarah Lee 1, Jeong-Gu Kim 2, Joo-Won Suh 3 and Choong Hwan Lee 1*

1Department of Bioscience and Biotechnology, Konkuk University, Seoul 143-701, Republic of Korea, 2Genomics Division, National Academy of Agricultural Science, Rural Development Administration, Jeonju 560-500, Republic of Korea, 3Center for Nutraceutical and Pharmaceutical Materials, Myongji University, Yongin 449-728, Republic of Korea

Received: March 4, 2015; Accepted: April 10, 2015

Abstract

Secondary metabolite-based chemotaxonomic classification of Streptomyces (8 species, 14
strains) was performed using ultraperformance liquid chromatography-quadrupole-time-offlight-
mass spectrometry with multivariate statistical analysis. Most strains were generally
well separated by grouping under each species. In particular, S. rimosus was discriminated
from t he r emaining s ev en s pecies ( S. coelicolor, S. griseus, S. indigoferus, S. peucetius,
S. rubrolavendulae, S. scabiei, and S. virginiae) in partial least squares discriminant analysis, and
oxytetracycline and rimocidin were identified as S. rimosus-specific metabolites. S. rimosus also
showed high antibacterial activity against Xanthomonas oryzae pv. oryzae, the pathogen
responsible for rice bacterial blight. This study demonstrated that metabolite-based
chemotaxonomic classification is an effective tool for distinguishing Streptomyces spp. and for
determining their species-specific metabolites.

Keywords: Streptomyces, Chemotaxonomy, Antibacterial activity

References

  1. Anderson AS, Wellington EMH. 2001. The taxonomy of Streptomyces and related genera. Int. J. Syst. Evol. Microbiol. 51: 797-814.
    Pubmed CrossRef
  2. Ando T, Miyashiro S, Hirayama K, Kida T, Shibai H, Murai A, Udaka S. 1987. New streptothricin-group antibiotics, AN201 I, II and III. II. Chemical structures. J. Antibiot. 40: 11401145.
    CrossRef
  3. Aquino LC, Hicks CA, Scalon MC, Lima MG, Lemos MD, Paludo GR, et al. 2014. Prevalence and phylogenetic analysis of haemoplasmas from cats infected with multiple species. J. Microbiol. Methods 107: 189-196.
    Pubmed KoreaMed CrossRef
  4. Barashkova NP, Shenin ID, Myasnikova LG. 1976. Actinomyces pneumonicus var. altamicus var. nov., a producer of new altamycin antibiotics. Antibiotiki 21: 487-491.
    Pubmed
  5. Benning VR, Mathers JJ, 1999. Comparison of agar dilution and broth microdilution methods of anaerobic antimicrobial susceptibility testing using several veterinary antibiotics against Clostridium perfringens strains originating from porcine and avian sources. Anaerobe 5: 561-569.
    CrossRef
  6. Bieber B, Nuske J, Ritzau M, Grafe U. 1998. Alnumycin a new naphthoquinone antibiotic produced by an endophytic Streptomyces sp. J. Antibiot. 51: 381-382.
    Pubmed CrossRef
  7. Bisti E, Monciardini P, Cavaletti L, Bamonte R, Lazzarini A, Sosio M, Donadio S. 2006. Antibiotic-producing ability by representatives of a newly discovered lineage of actinomycetes. Microbiology 152: 675-683.
    Pubmed CrossRef
  8. Brian P, Riggle PJ, Santos RA, Champness WC. 1996. Global negative regulation of Streptomyces coelicolor antibiotic synthesis mediated by an absA-encoded putative signal transduction system. J. Bacteriol. 178: 3221-3231.
    Pubmed KoreaMed CrossRef
  9. Chae HJ, Kang JS, Byun JO, Han KS, Kim DU, Oh SM, et al. 2000. Molecular mechanism of staurosporine-induced apoptosis in osteoblasts. Pharmacol. Res. 42: 373-381.
    Pubmed CrossRef
  10. Charoensopharat K, Thummabenjapone P, Sirithorn P, Thammasirirak S. 2008. Antibacterial substance produced by Streptomyces sp. No. 87. Afr. J. Biotechnol. 7: 1362-1368.
  11. Christiano RSC, Reilly CC, Miller WP, Scherm H. 2010. Oxytetracycline dynamics on peach leaves in relation to temperature, sunlight, and simulated rain. Plant Dis. 94:1213-1218.
    CrossRef
  12. Christova K, Sholeva Z, Chipeva V. 1995. Application of molecular biological methods in taxonomy of genus Streptomyces. J. Cult. Collect. 1: 3-10.
  13. Commbs JT, Franco CMM. 2003. Isolation and identification of actinobacteria from surface-sterilized wheat roots. Appl. Environ. Microbiol. 69: 5603–5608.
    KoreaMed CrossRef
  14. Cordell GA. 2008. The Alkaloids: Chemistry and Biology, pp. 3-96. Vol. 65, Academic Press, San Diego, California.
  15. Dalziel K, Dykes PJ, Marks R. 1987. The effect of tetracycline and erythromycin in a model of acne-type inflammation. Br. J. Exp. Pathol. 68: 67-70.
    Pubmed KoreaMed
  16. Davisson JW, Tanner Jr FW, Finlay AC, Solomons IA. 1951. Rimocidin, a new antibiotic. Antibiot. Chemother. (Northfield) 1: 289-290.
  17. Djinni I, Defant A, Kecha M, Mancini I. 2014. Metabolite profile of marine-derived endophytic Streptomyces sundarbansensis WR1L1S8 by liquid chromatography–mass spectrometry and evaluation of culture conditions on antibacterial activity and mycelial growth. J. Appl. Microbiol. 116: 39-50.
    Pubmed CrossRef
  18. Deseo MA, Hunter lS, Waterman PG. 2005. Novel polyketide metabolites from Streptomyces rimosus mutant strain R1059. J. Antibiot. 58: 822-827.
    Pubmed CrossRef
  19. Dung NT, Kim JM, Kang SC. 2008. Chemical composition, antimicrobial and antioxidant activities of the essential oil and the ethanol extract of Cleistocalyx operculatus (Roxb.) Merr and Perry buds. Food Chem. Toxicol. 46: 3632-3639.
    Pubmed CrossRef
  20. El-Hendaw HH, Osman ME, Sorour NM. 2005. Biological control of bacterial spot of tomato caused by Xanthomonas campestris pv. vesicatoria by Rahnella aquatilis. Microbiol. Res. 160: 343-352.
    Pubmed CrossRef
  21. El-Hussein AA, Alhason REM, Abdelwahab SA, El-Sidig MA. 2014. Isolation and identification of Streptomyces rochei strain active against phytopathogenic fungi. Br. Microbiol. Res. J. 4: 1057-1068.
    CrossRef
  22. Embley TM, Stackebrandt E. 1994. The molecular phylogeny and systematics of the actinomycetes. Annu. Rev. Microbiol. 48: 257-289.
    Pubmed CrossRef
  23. Emmert EAB, Handelsman J. 1999. Biocontrol of plant disease: a (gram-) positive perspective. FEMS Microbiol. Lett. 171: 1-9.
    Pubmed CrossRef
  24. Forbes JC, Watson RD. 1992. Plants in Agriculture. Cambridge University Press, New York.
  25. Forner D, Berrue F, Correa H, Duncan K, Kerr RG. 2013. Chemical dereplication of marine actinomycetes by liquid chromatography-high resolution mass spectrometry profiling and statistical analysis. Anal. Chim. Acta 805: 70-79.
    Pubmed CrossRef
  26. Fuente RDL, Sonawane ND, Arumainayagam D, Verkman AS. 2006. Small molecules with antimicrobial activity against E. coli and P. aeruginosa identified by high-throughput screening. Br. J. Pharmacol. 149: 551-559.
    Pubmed KoreaMed CrossRef
  27. Gerrettson-Cornell L. 2005. Note on the Actinomycetes of the Streptomyces hygroscopicus-like Complex in Tradition Taxonomy, pp 1-18. Vol. 70, Forest Resources Research, Sydney.
  28. Halling-Sorensen B, Lykkeberg A, Ingerslev F, Blackwell P, Tjornelund J. 2003. Characterisation of the abiotic degradation pathways of oxytetracyclines in soil interstitial water using LC-MS-MS. Chemosphere 50: 1331-1342.
    CrossRef
  29. Hosoya T, Yamamoto Y, Uehara Y, Hayashi M, Komiyama K, Ishibashi M. 2005. New cytotoxic bisindole alkaloids with protein tyrosine kinase inhibitory activity from a myxomycete Lycogala epidendrum. Bioorg. Med. Chem. Lett. 15: 2776-2780.
    Pubmed CrossRef
  30. Igarashi M, Shida T, Sasaki Y, Kinoshita N, Naganawa H, Hamada M, Takeuchi T. 1999. Vinylamycin, a new depsipeptide antibiotic, from Streptomyces sp. J. Antibiot. (Tokyo) 52: 873-879.
    CrossRef
  31. Igarashi Y, Ogawa M, Sato Y, Saito N, Yoshida R, Kunoh H, et al. 2000. Fistupyrone, a novel inhibitor of the infection of Chinese cabbage by Alternaria brassicicola, from Streptomyces sp. TP-A0569. J. Antibiot. 53: 1117-1122.
    Pubmed CrossRef
  32. Jensen PR, Williams PG, Oh DC, Zeigler L, Fenical W. 2007. Species-specific secondary metabolite production in marine actinomycetes of the genus Salinispora. Appl. Environ. Microbiol. 73: 1146-1152.
    Pubmed KoreaMed CrossRef
  33. Kaluzna M, Pulawska J, Waleron M, Sobiczewski P. 2014. The genetic characterization of Xanthomonas arboricola pv. juglandis, the causal agent of walnut blight in Poland. Plant Pathol. 63: 1404-1416.
    CrossRef
  34. Kim JD, Han JW, Lee SC, Lee D, Hwang IC, Kim BS. 2011. Disease control effect of strevertenes produced by Streptomyces psammoticus against tomato Fusarium wilt. J. Agric. Food Chem. 95: 1893-1899.
    Pubmed CrossRef
  35. King RR, Lawrence CH, Calhoun LA. 1992. Chemistry of phytotoxins associated with Streptomyces scabies, the causal organism of potato common scab. J. Agric. Food Chem. 40:834-837.
    CrossRef
  36. Komoda T, Morimitsu Y, Hirota H, Hirota A. 1995. USF19A, a new lipoxygenase inhibitor from Streptomyces sp. 59:924-926.
  37. Lechevalier MP, Lechevalier H. 1970. Chemical composition as a criterion in the classification of aerobic actinomycetes. Int. J. Syst. Bacteriol. 20: 435-443.
    CrossRef
  38. Li J, Wang N. 2014. Foliar application of biofilm formationinhibiting compounds enhances control of citrus canker caused by Xanthomonas citri subsp. citri. Phytopathology 104:134-142.
    Pubmed CrossRef
  39. Li XB, Tang JS, Gao H, Ding R, Li J, Hong K, Yao XS. 2011. A new staurosporine analog from Actinomycetes Streptomyces sp. (172614). J. Asian Nat. Prod. Res. 13: 765-769.
    Pubmed CrossRef
  40. Nasher MA, Hay RJ, Mahgoub ES, Gumaa SA. 1989. In vitro studies of antibiotic sensitivities of Streptomyces somaliensis a cause of human actinomycetoma. Trans. R Soc. Trop. Med. Hyg. 83: 265-268.
    CrossRef
  41. Ndonde MJM, Semu E. 2001. Preliminary characterization of some Streptomyces species from four Tanzanian soils and their antimicrobial potential against selected plant and animal pathogenic bacteria. World J. Microbiol. Biotechnol. 16:595-599.
    CrossRef
  42. Omura S, Iwai Y, Hirano A, Nakagawa A, Awaya J, Tsuchya H, et al. 1977. A new alkaloid AM-2282 of Streptomyces origin: taxonomy, fermentation, isolation and preliminary characterization. J. Antibiot. 30: 275-282.
    Pubmed CrossRef
  43. Omura S, Iwai Y, Takahashi Y, Sadakane N, Nakagawa A, Oiwa H, et al. 1979. Herbimycin, a new antibiotic produced by a strain of Streptomyces. J. Antibiot. 32: 255-261.
    Pubmed CrossRef
  44. Park SB, Lee CH, Kim TJ, Kang LW, Lee BM, Kim JG. 2012. Development of a method for high throughput screening of antagonistic substances against rice pathogens using rice leaf explants. Korean J. Microbiol. Biotechnol. 40: 39-42.
    CrossRef
  45. Peng FJ, Zhou LJ, Ying GG, Liu YS, Zhao JL. 2014. Antibacterial activity of the soil-bound antimicrobials oxytetracycline and ofloxacin. Environ. Toxicol. Chem. 33:776-783.
    Pubmed CrossRef
  46. Petkovic H, Cullum J, Hranueli D, Hunter IS, Peric-Concha N, Pigac J, et al. 2006. Genetics of Streptomyces rimosus, the oxytetracycline producer. Microbiol. Mol. Biol. Rev. 70: 704-728.
    Pubmed KoreaMed CrossRef
  47. Pickens LB, Tang Y. 2010. Oxytetracycline biosynthesis. J. Biol. Chem. 285: 27509-27515.
    Pubmed KoreaMed CrossRef
  48. Pindur U, Kim YS, Mehrabani F. 1999. Advances in indolo [2,3-a] carbazole chemistry: design and synthesis of protein kinase C and topoisomerase I inhibitors. Curr. Med. Chem. 6:29-69.
    CrossRef
  49. Quintana ET, Wierzbicka K, Mackiewicz P, Osman A, Fahal AH, Hamid ME, et al. 2008. Streptomyces sudanensis sp. nov., a new pathogen isolated from patients with actinomycetoma. Antonie Van Leeuwenhoek 93: 305-313.
    Pubmed CrossRef
  50. Rahmam AU. 2000. Bioactive Natural Products (Part B), pp. 373-456. Vol. 21. Elsevier, AE Amsterdam, Netherlands.
  51. Rao M , Feng L, R uan L , Ge M , Sheng X. 2 013. U PLC- MSbased metabolomic study of Streptomyces strain HCCB10043 under different pH conditions reveals important pathways affecting the biosynthesis of A21978C compounds. Anal. Lett. 46: 2305-2318.
    CrossRef
  52. Schlingmann G, Miline L, Borders DB, Carter GT. 1999. Strevertenes, antifungal pentaene macrolides produced by Streptoverticillcum LL-30F8488. Tetrahedron 55: 5977-5990.
    CrossRef
  53. Seco EM, Perez-Zuniga FJ, Rolon MS, Malpartida F. 2004. Starter unit choice determines the production of two tetraene macrolides, rimocidin and CE-108, in Streptomyces diastaticus var. 108. Chem. Biol. 11: 357-366.
    Pubmed CrossRef
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