Bioassay- and metabolomics-guided screening of bioactive soil actinomycetes from the ancient city of Ihnasia, Egypt

English version

Autoři: Mohamed Sebak ^aff001; Amal E. Saafan ^aff002; Sameh AbdelGhani ^aff003; Walid Bakeer ^aff003; Ahmed O. El-Gendy ^aff003; Laia Castaño Espriu ^aff001; Katherine Duncan ^aff001; RuAngelie Edrada-Ebel ^aff001
Působiště autorů: Strathclyde Institute of Pharmacy and Biomedical Sciences, Faculty of Science, University of Strathclyde, Glasgow, Scotland, United Kingdom ^aff001; Department of Pharmaceutical Microbiology, Faculty of Pharmacy, Menoufia University, Shebin Elkom, Menoufia, Egypt ^aff002; Microbiology and Immunology Department, Faculty of Pharmacy, Beni-Suef University, Beni-Suef, Egypt ^aff003
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0226959

Souhrn

Literature surveys, taxonomical differences, and bioassay results have been utilized in the discovery of new natural products to aid in Actinomycetes isolate-selection. However, no or less investigation have been done on establishing the differences in metabolomic profiles of the isolated microorganisms. The study aims to utilise bioassay- and metabolomics-guided tools that included dereplication study and multivariate analysis of the NMR and mass spectral data of microbial extracts to assist the selection of isolates for scaling-up the production of antimicrobial natural products. A total of 58 actinomycetes were isolated from different soil samples collected from Ihnasia City, Egypt and screened for their antimicrobial activities against indicator strains that included Bacillus subtilis, Escherichia coli, methicillin-resistant Staphylococcus aureus and Candida albicans. A number of 25 isolates were found to be active against B. subtilis and/or to at least one of the tested indicator strains. Principal component analyses showed chemical uniqueness for four outlying bioactive actinomycetes extracts. In addition, Orthogonal Projections to Latent Structures Discriminant Analysis (OPLS-DA) and dereplication study led us to further select two outlying anti-MRSA active isolates MS.REE.13 and 22 for scale-up work. MS.REE.13 and 22 exhibited zones of inhibition at 19 and 13 mm against MRSA, respectively. A metabolomics-guided approach provided the steer to target the bioactive metabolites (P<0.01) present in a crude extract or fraction even at nanogram levels but it was a challenge that such low-yielding bioactive natural products would be feasible to isolate. Validated to occur only on the active side of OPLS-DA loadings plot, the isolated compounds exhibited medium to weak antibiotic activity with MIC values between 250 and 800 μM. Two new compounds, P_24306 (C₁₀H₁₃N₂) and N_12799 (C₁₈H₃₂O₃) with MICs of 795 and 432 μM, were afforded from the scale-up of MS.REE. 13 and 22, respectively.

Klíčová slova:

Actinobacteria – Drug metabolism – Methicillin-resistant Staphylococcus aureus – Antibiotics – Metabolites – NMR spectroscopy – Metabolomics – Streptomyces

Zdroje

1. Newman DJ, Cragg GM. Natural products as sources of new drugs over the 30 years from 1981 to 2010. J Nat Prod. 2012;75(3):311–35. doi: 10.1021/np200906s 22316239; PubMed Central PMCID: PMC3721181.

2. Waters AL, Hill RT, Place AR, Hamann MT. The expanding role of marine microbes in pharmaceutical development. Curr Opin Biotechnol. 2010;21(6):780–6. doi: 10.1016/j.copbio.2010.09.013 20956080; PubMed Central PMCID: PMC2994104.

3. Berdy J. Bioactive microbial metabolites. J Antibiot (Tokyo). 2005;58(1):1–26. doi: 10.1038/ja.2005.1 15813176.

4. Demain AL, Sanchez S. Microbial drug discovery: 80 years of progress. J Antibiot (Tokyo). 2009;62(1):5–16. doi: 10.1038/ja.2008.16 19132062.

5. Chavan DV, Mulaje SS, Mohalkar RY. A Review on actinomycetes and their biotechnological applications. International Journal of pharmaceutical sciences and research. 2013;4(5):1730–42. http://dx.doi.org/10.13040/IJPSR.0975-8232.4(5).1730-42.

6. Lam KS. New aspects of natural products in drug discovery. Trends in Microbiology. 2007;15(6):279–89. doi: 10.1016/j.tim.2007.04.001 17433686

7. Undabarrena A, Beltrametti F, Claverias FP, Gonzalez M, Moore ER, Seeger M, et al. Exploring the Diversity and Antimicrobial Potential of Marine Actinobacteria from the Comau Fjord in Northern Patagonia, Chile. Front Microbiol. 2016;7:1135. doi: 10.3389/fmicb.2016.01135 27486455; PubMed Central PMCID: PMC4949237.

8. Goodfellow M, Williams ST. Ecology of actinomycetes. Annu Rev Microbiol. 1983;37:189–216. doi: 10.1146/annurev.mi.37.100183.001201 6357051.

9. Ahmad MS, El-Gendy AO, Ahmed RR, Hassan HM, El-Kabbany HM, Merdash AG. Exploring the Antimicrobial and Antitumor Potentials of Streptomyces sp. AGM12-1 Isolated from Egyptian Soil. Front Microbiol. 2017;8:438. doi: 10.3389/fmicb.2017.00438 28348553; PubMed Central PMCID: PMC5346535.

10. Awad M, El-Sahed K, El-Nakkadi A. Isolation, screening and identification of newly isolated soil Streptomyces (Streptomyces sp. NRC-35) for b-Lactamase inhibitor production. World Appl Sci J. 2009;7(5):637–46.

11. Hozzein WN, Goodfellow M. Streptomyces synnematoformans sp. nov., a novel actinomycete isolated from a sand dune soil in Egypt. Int J Syst Evol Microbiol. 2007;57(Pt 9):2009–13. doi: 10.1099/ijs.0.65037-0 17766864.

12. Handelsman J, Rondon MR, Brady SF, Clardy J, Goodman RM. Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products. Chem Biol. 1998;5(10):R245–9. doi: 10.1016/s1074-5521(98)90108-9 9818143.

13. Ritacco FV, Haltli B, Janso JE, Greenstein M, Bernan VS. Dereplication of Streptomyces soil isolates and detection of specific biosynthetic genes using an automated ribotyping instrument. J Ind Microbiol Biotechnol. 2003;30(8):472–9. doi: 10.1007/s10295-003-0038-0 12687492.

14. Jensen PR, Williams PG, Oh DC, Zeigler L, Fenical W. Species-specific secondary metabolite production in marine actinomycetes of the genus Salinispora. Appl Environ Microbiol. 2007;73(4):1146–52. doi: 10.1128/AEM.01891-06 17158611; PubMed Central PMCID: PMC1828645.

15. Hou Y, Braun DR, Michel CR, Klassen JL, Adnani N, Wyche TP, et al. Microbial strain prioritization using metabolomics tools for the discovery of natural products. Anal Chem. 2012;84(10):4277–83. doi: 10.1021/ac202623g 22519562; PubMed Central PMCID: PMC3352271.

16. Abdelmohsen UR, Bayer K, Hentschel U. Diversity, abundance and natural products of marine sponge-associated actinomycetes. Nat Prod Rep. 2014;31(3):381–99. doi: 10.1039/c3np70111e 24496105.

17. Tawfike AF, Viegelmann C, Edrada-Ebel R. Metabolomics and dereplication strategies in natural products. Methods Mol Biol. 2013;1055:227–44. Epub 2013/08/22. doi: 10.1007/978-1-62703-577-4_17 23963915.

18. Forner D, Berrue F, Correa H, Duncan K, Kerr RG. Chemical dereplication of marine actinomycetes by liquid chromatography-high resolution mass spectrometry profiling and statistical analysis. Anal Chim Acta. 2013;805:70–9. doi: 10.1016/j.aca.2013.10.029 24296145.

19. Macintyre L, Zhang T, Viegelmann C, Martinez IJ, Cheng C, Dowdells C, et al. Metabolomic tools for secondary metabolite discovery from marine microbial symbionts. Mar Drugs. 2014;12(6):3416–48. doi: 10.3390/md12063416 24905482; PubMed Central PMCID: PMC4071584.

20. Harvey AL, Edrada-Ebel R, Quinn RJ. The re-emergence of natural products for drug discovery in the genomics era. Nat Rev Drug Discov. 2015;14(2):111–29. doi: 10.1038/nrd4510 25614221.

21. Bobzin SC, Yang S, Kasten TP. LC-NMR: a new tool to expedite the dereplication and identification of natural products. J Ind Microbiol Biotechnol. 2000;25(6):342–5. doi: 10.1038/sj.jim.7000057 11320422.

22. Abdelmohsen UR, Cheng C, Viegelmann C, Zhang T, Grkovic T, Ahmed S, et al. Dereplication strategies for targeted isolation of new antitrypanosomal actinosporins A and B from a marine sponge associated-Actinokineospora sp. EG49. Mar Drugs. 2014;12(3):1220–44. doi: 10.3390/md12031220 24663112; PubMed Central PMCID: PMC3967206.

23. van der Werf MJ, Jellema RH, Hankemeier T. Microbial metabolomics: replacing trial-and-error by the unbiased selection and ranking of targets. J Ind Microbiol Biotechnol. 2005;32(6):234–52. doi: 10.1007/s10295-005-0231-4 15895265.

24. Yang JY, Sanchez LM, Rath CM, Liu X, Boudreau PD, Bruns N, et al. Molecular networking as a dereplication strategy. J Nat Prod. 2013;76(9):1686–99. doi: 10.1021/np400413s 24025162; PubMed Central PMCID: PMC3936340.

25. Kjer J, Debbab A, Aly AH, Proksch P. Methods for isolation of marine-derived endophytic fungi and their bioactive secondary products. Nat Protoc. 2010;5(3):479–90. doi: 10.1038/nprot.2009.233 20203665.

26. Robinette SL, Bruschweiler R, Schroeder FC, Edison AS. NMR in metabolomics and natural products research: two sides of the same coin. Acc Chem Res. 2012;45(2):288–97. doi: 10.1021/ar2001606 21888316; PubMed Central PMCID: PMC3284194.

27. Boroujerdi AF, Vizcaino MI, Meyers A, Pollock EC, Huynh SL, Schock TB, et al. NMR-based microbial metabolomics and the temperature-dependent coral pathogen Vibrio coralliilyticus. Environ Sci Technol. 2009;43(20):7658–64. doi: 10.1021/es901675w 19921875.

28. Tang J. Microbial metabolomics. Curr Genomics. 2011;12(6):391–403. doi: 10.2174/138920211797248619 22379393; PubMed Central PMCID: PMC3178908.

29. Tawfike AF, Abbott G, Young L, Edrada-Ebel R. Metabolomic-Guided Isolation of Bioactive Natural Products from Curvularia sp., an Endophytic Fungus of Terminalia laxiflora. Planta Med. 2018;84(3):182–90. Epub 2017/08/29. doi: 10.1055/s-0043-118807 28847019.

30. Tawfike AF, Tate R, Abbott G, Young L, Viegelmann C, Schumacher M, et al. Metabolomic Tools to Assess the Chemistry and Bioactivity of Endophytic Aspergillus Strain. Chem Biodivers. 2017;14(10). Epub 2017/07/04. doi: 10.1002/cbdv.201700040 28672096.

31. Cheng C, MacIntyre L, Abdelmohsen UR, Horn H, Polymenakou PN, Edrada-Ebel R, et al. Biodiversity, Anti-Trypanosomal Activity Screening, and Metabolomic Profiling of Actinomycetes Isolated from Mediterranean Sponges. PLoS One. 2015;10(9):e0138528. Epub 2015/09/26. doi: 10.1371/journal.pone.0138528 26407167; PubMed Central PMCID: PMC4583450.

32. Chagas-Paula DA, Zhang T, Da Costa FB, Edrada-Ebel R. A Metabolomic Approach to Target Compounds from the Asteraceae Family for Dual COX and LOX Inhibition. Metabolites. 2015;5(3):404–30. Epub 2015/07/18. doi: 10.3390/metabo5030404 26184333; PubMed Central PMCID: PMC4588803.

33. Chagas-Paula DA, Oliveira TB, Zhang T, Edrada-Ebel R, Da Costa FB. Prediction of Anti-inflammatory Plants and Discovery of Their Biomarkers by Machine Learning Algorithms and Metabolomic Studies. Planta Med. 2015;81(6):450–8. Epub 2015/01/24. doi: 10.1055/s-0034-1396206 25615275.

34. Viegelmann C, Margassery LM, Kennedy J, Zhang T, O'Brien C, O'Gara F, et al. Metabolomic profiling and genomic study of a marine sponge-associated Streptomyces sp. Mar Drugs. 2014;12(6):3323–51. Epub 2014/06/04. doi: 10.3390/md12063323 24893324; PubMed Central PMCID: PMC4071579.

35. Kamal N, Viegelmann CV, Clements CJ, Edrada-Ebel R. Metabolomics-Guided Isolation of Anti-trypanosomal Metabolites from the Endophytic Fungus Lasiodiplodia theobromae. Planta Med. 2017;83(6):565–73. Epub 2016/10/21. doi: 10.1055/s-0042-118601 27760442.

36. Raheem DJ, Tawfike AF, Abdelmohsen UR, Edrada-Ebel R, Fitzsimmons-Thoss V. Application of metabolomics and molecular networking in investigating the chemical profile and antitrypanosomal activity of British bluebells (Hyacinthoides non-scripta). Sci Rep. 2019;9(1):2547. Epub 2019/02/24. doi: 10.1038/s41598-019-38940-w 30796274; PubMed Central PMCID: PMC6385288.

37. Tawfike AF, Romli M, Clements C, Abbott G, Young L, Schumacher M, et al. Isolation of anticancer and anti-trypanosome secondary metabolites from the endophytic fungus Aspergillus flocculus via bioactivity guided isolation and MS based metabolomics. J Chromatogr B Analyt Technol Biomed Life Sci. 2019;1106–1107:71–83. Epub 2019/01/19. doi: 10.1016/j.jchromb.2018.12.032 30658264.

38. Rabah FL, Elshafei A, Saker M, Cheikh B, Hocine H. Screening, isolation and characterization of a novel antimicrobial producing actinomycete, strain RAF10. Biotechnology. 2007;6(4):489–96.

39. El-Shatoury S, El-Kraly O, El-Kazzaz W, Dewedar A. Antimicrobial activities of actinomycetes inhabiting achillea fragrantissima (family: compositae). Egyptian J Nat Tox. 2009;6(2):1–15.

40. Hozzein WN, Rabie W, Ali MIA. Screening the Egyptian desert actinomycetes as candidates for new antimicrobial compounds and identification of a new desert Streptomyces strain. African Journal of Biotechnology. 2011;10(12):2295–301.

41. Amin DH, Tolba S, Abolmaaty A, Abdallah NA, Wellington E. Phylogenetic and antimicrobial characteristics of a novel Streptomyces sp. Ru87 isolated from Egyptian soil. Int J Curr Microbiol App Sci. 2017;6(8):2524–41.

42. Ahmad MS, El-Gendy AO, Ahmed RR, Hassan HM, El-Kabbany HM, Merdash AG. Exploring the antimicrobial and antitumor potentials of Streptomyces sp. AGM12-1 isolated from Egyptian soil. Frontiers in microbiology. 2017;8:438. doi: 10.3389/fmicb.2017.00438 28348553

43. Elbendary AA, Hessain AM, El-Hariri MD, Seida AA, Moussa IM, Mubarak AS, et al. Isolation of antimicrobial producing actinobacteria from soil samples. Saudi journal of biological sciences. 2018;25(1):44–6. doi: 10.1016/j.sjbs.2017.05.003 29379355

44. Abdel-Aziz MS, Hathout AS, El-Neleety AA, Hamed AA, Sabry BA, Aly SE, et al. Molecular identification of actinomycetes with antimicrobial, antioxidant and anticancer properties. Comunicata Scientiae. 2019;10(2):218–31.

45. Williams ST, Goodfellow M, Wellington EM, Vickers JC, Alderson G, Sneath PH, et al. A probability matrix for identification of some Streptomycetes. J Gen Microbiol. 1983;129(6):1815–30. doi: 10.1099/00221287-129-6-1815 6688823.

46. Reddy NG, Ramakrishna DPN, Gopal SVR. A morphological, physiological and biochemical studies of marine Streptomyces rochei (MTCC 10109) showing antagonistic activity against selective human. Asian J Biol Sci. 2011;10(3):57–65. doi: 10.3923/ajbs.2011.1.14

47. Aghamirian MR, Ghiasian SA. Isolation and characterization of medically important aerobic actinomycetes in soil of Iran (2006–2007). Open Microbiol J. 2009;3:53–7. doi: 10.2174/1874285800903010053 19440253; PubMed Central PMCID: PMC2681176.

48. Gavin JJ. Analytical microbiology. II. The diffusion methods. Appl Microbiol. 1957;5(1):25–33. 13403634; PubMed Central PMCID: PMC1057248.

49. Romankova AG, Zurabova ER, Fursenko MV, Sukharevich VI, Pronina MI. [Selection of strains of some antibiotic producing Actinomycetes during repeated passages in submerged cultures]. Antibiotiki. 1971;16(7):579–83. 5168223.

50. Selvameenal L, Radhakrishnan M, Balagurunathan R. Antibiotic pigment from desert soil actinomycetes; biological activity, purification and chemical screening. Indian J Pharm Sci. 2009;71(5):499–504. doi: 10.4103/0250-474X.58174 20502566; PubMed Central PMCID: PMC2866339.

51. Chambers MC, Maclean B, Burke R, Amodei D, Ruderman DL, Neumann S, et al. A cross-platform toolkit for mass spectrometry and proteomics. Nat Biotechnol. 2012;30(10):918–20. doi: 10.1038/nbt.2377 23051804; PubMed Central PMCID: PMC3471674.

52. Pluskal T, Castillo S, Villar-Briones A, Oresic M. MZmine 2: modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data. BMC Bioinformatics. 2010;11:395. doi: 10.1186/1471-2105-11-395 20650010; PubMed Central PMCID: PMC2918584.

53. Eriksson L, Johansson E, Kettaneh-Wold N, Wold S. Multi and megavariate data analysis. Umea˚: Umetrics AB; 2006.

54. Weisburg WG, Barns SM, Pelletier DA, Lane DJ. 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol. 1991;173(2):697–703. doi: 10.1128/jb.173.2.697-703.1991 1987160; PubMed Central PMCID: PMC207061.

55. Benson DA, Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW. GenBank. Nucleic Acids Res. 2015;43(Database issue):D30–5. doi: 10.1093/nar/gku1216 25414350; PubMed Central PMCID: PMC4383990.

56. Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol. 2007;24(8):1596–9. doi: 10.1093/molbev/msm092 17488738.

57. Savic S, Tapia C, Grilli B, Rufle A, Bihl MP, de Vito Barascud A, et al. Comprehensive epidermal growth factor receptor gene analysis from cytological specimens of non-small-cell lung cancers. Br J Cancer. 2008;98(1):154–60. doi: 10.1038/sj.bjc.6604142 18087280; PubMed Central PMCID: PMC2359717.

58. Tan LT, Ser HL, Yin WF, Chan KG, Lee LH, Goh BH. Investigation of Antioxidative and Anticancer Potentials of Streptomyces sp. MUM256 Isolated from Malaysia Mangrove Soil. Front Microbiol. 2015;6:1316. doi: 10.3389/fmicb.2015.01316 26635777; PubMed Central PMCID: PMC4659911.

59. Jonsbu E, McIntyre M, Nielsen J. The influence of carbon sources and morphology on nystatin production by Streptomyces noursei. J Biotechnol. 2002;95(2):133–44. Epub 2002/03/26. doi: 10.1016/s0168-1656(02)00003-2 11911923.

60. Zainal Abidin ZA, Abdul Malek N, Zainuddin Z, Chowdhury AJK. Selective isolation and antagonistic activity of actinomycetes from mangrove forest of Pahang, Malaysia. Frontiers in Life Science. 2016;9(1):24–31. doi: 10.1080/21553769.2015.1051244

61. Masand M, Sivakala KK, Menghani E, Thinesh T, Anandham R, Sharma G, et al. Biosynthetic Potential of Bioactive Streptomycetes Isolated From Arid Region of the Thar Desert, Rajasthan (India). Front Microbiol. 2018;9:687. Epub 2018/05/04. doi: 10.3389/fmicb.2018.00687 29720968; PubMed Central PMCID: PMC5915549.

62. Forar R, Elshafei A, Mahmoud S, Bengraa C, Hacene H. Screening, Isolation and Characterization of a Novel Antimicrobial Producing Actinomycete, Strain RAF10. Biotechnology (Faisalabad). 2007;6:489–96. doi: 10.3923/biotech.2007.489.496

63. Zhu Q, Li J, Ma J, Luo M, Wang B, Huang H, et al. Discovery and engineered overproduction of antimicrobial nucleoside antibiotic A201A from the deep-sea marine actinomycete Marinactinospora thermotolerans SCSIO 00652. Antimicrob Agents Chemother. 2012;56(1):110–4. Epub 2011/11/09. doi: 10.1128/AAC.05278-11 22064543; PubMed Central PMCID: PMC3256081.

64. Bizuye A, Moges F, Andualem B. Isolation and screening of antibiotic producing actinomycetes from soils in Gondar town, North West Ethiopia. Asian Pacific J Trop Disease. 2013;3(5):375–81. doi: 10.1016/S2222-1808(13)60087-0

65. Thakur D, Yadav A, Gogoi BK, Bora TC. Isolation and screening of Streptomyces in soil of protected forest areas from the states of Assam and Tripura, India, for antimicrobial metabolites. Journal de Mycologie Médicale. 2007;17(4):242–9. https://doi.org/10.1016/j.mycmed.2007.08.001.

66. Fu P, Liu P, Qu H, Wang Y, Chen D, Wang H, et al. Alpha-pyrones and diketopiperazine derivatives from the marine-derived actinomycete Nocardiopsis dassonvillei HR10-5. J Nat Prod. 2011;74(10):2219–23. doi: 10.1021/np200597m 21958359.

67. Reading C, Cole M. Clavulanic acid: a beta-lactamase-inhiting beta-lactam from Streptomyces clavuligerus. Antimicrob Agents Chemother. 1977;11(5):852–7. doi: 10.1128/aac.11.5.852 879738; PubMed Central PMCID: PMC352086.

68. Li JL, Huang L, Liu J, Song Y, Gao J, Jung JH, et al. Acetylcholinesterase inhibitory dimeric indole derivatives from the marine actinomycetes Rubrobacter radiotolerans. Fitoterapia. 2015;102:203–7. doi: 10.1016/j.fitote.2015.01.014 25655350

69. Guo JP, Tan JL, Wang YL, Wu HY, Zhang CP, Niu XM, et al. Isolation of talathermophilins from the thermophilic fungus Talaromyces thermophilus YM3-4. J Nat Prod. 2011;74(10):2278–81. doi: 10.1021/np200365z 21967034.

70. Dumas A. 8-Substituted-2’-Deoxyguanosines as Internal Probes for DNA Folding and Energy Transfer.: University of Zurich; 2011.

71. Nisic F. Stereoselective Synthesis of Glycosyl Amides by Traceless Staudinger Ligation of Glycosyl Azides: Universita’ Degli Studi di Milano; 2010.

72. Lavanya A, Sribalan R, Padmini V. Synthesis and biological evaluation of new benzofuran carboxamide derivatives. J Saudi Chem Soc. 2017;21(3):277–85. https://doi.org/10.1016/j.jscs.2015.06.008.

73. Ugale V, Patel H, Patel B, Bari S. Benzofurano-isatins: Search for antimicrobial agents. Arabian J Chem. 2017;10:S389–S96. doi: https://doi.org/10.1016/j.arabjc.2012.09.011

74. Soldatenkov AT, Levov AN, Mobio IG, Polyakova EV, Kutyakov SV, An' LT, et al. Synthesis and biological activity of N- and O-acyl derivatives of 2,6, diphenyl-4-hydroxypiperidines and tetrahydropyridines Pharm Chem Journal 2003;37:16–8.

75. Padmavathi V, Reddy BJM, Baliah A, Padmaja A, Reddy DB. Synthesis of some novel spiro heterocycles. Part II. ARKIVOC. 2005;14:1–13.

76. AKos. N',N''-[(2-Oxo-1H-benzimidazole-1,3(2H)-diyl)bis(methylene)]diacetohydrazide. AKOS024357626. AKos Consulting & Solutions GmbH 2014 [18 December 2018]. Available from: http://www.chemspider.com/Chemical-Structure.3460733.html?rid=6ba4f9b4-3363-4535-9e94-2672b4ee2f69.

77. Garg G. Design, Synthesis and Biological Evaluation of Ring-constrained and Biphemyl Derivatives as Hsp20 C-terminal Inhibitors: The University of Kansas; 2014.

78. Khalifa ME, Gobouri AA, Kabli FM, Altalhi TA, Almalki ASA, Mohamed MA. Synthesis, Antibacterial, and Anti HepG2 Cell Line Human Hepatocyte Carcinoma Activity of Some New Potentially Benzimidazole-5-(Aryldiazenyl)Thiazole Derivatives. Molecules. 2018;23(12):3285–301. doi: 10.3390/molecules23123285 30544987.

79. Woese C. Bacterial evolution background. Microbiology. 1987;51(2):221–71. doi: 10.1139/m88-093

80. Song J, Lee SC, Kang JW, Baek HJ, Suh JW. Phylogenetic analysis of Streptomyces spp. isolated from potato scab lesions in Korea on the basis of 16S rRNA gene and 16S-23S rDNA internally transcribed spacer sequences. Int J Syst Evol Microbiol. 2004;54(Pt 1):203–9. doi: 10.1099/ijs.0.02624-0

81. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4(4):406–25. doi: 10.1093/oxfordjournals.molbev.a040454 3447015.

82. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980;16(2):111–20. doi: 10.1007/bf01731581 7463489.

83. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol. 2016;33(7):1870–4. doi: 10.1093/molbev/msw054 27004904.

84. Zheng K, Shen D, Hong R. Biomimetic synthesis of lankacidin antibiotics. J Am Chem Soc. 2017;139(37):12939–42. doi: 10.1021/jacs.7b08500 28853876.

85. Harada S. Studies on lankacidin-group (T-2636) antibiotics. VI. Chemical structures of lankacidin-group antibiotics. II. Chem Pharm Bull (Tokyo). 1975;23(10):2201–10. doi: 10.1248/cpb.23.2201 1212749.

86. Lumb M, Macey PE, Spyvee J, Whitmarsh JM, Wright RD. Isolation of vivomycin and borrelidin, two antibiotics with anti-viral activity, from a species of Streptomyces (C2989). Nature. 1965;206(981):263–5. doi: 10.1038/206263a0 5840561.

87. Maehr H, Evans RH. Identity of borrelidin with treponemycin. J Antibiot (Tokyo). 1987;40(10):1455–6. doi: 10.7164/antibiotics.40.1455 3680012.

88. Arakawa K, Kodama K, Tatsuno S, Ide S, Kinashi H. Analysis of the loading and hydroxylation steps in lankamycin biosynthesis in Streptomyces rochei. Antimicrob Agents Chemother. 2006;50(6):1946–52. doi: 10.1128/AAC.00016-06 16723550; PubMed Central PMCID: PMC1479134.

89. Omura S, Muro T, Namiki S, Shibata M, Sawada J. Studies on the antibiotics from Streptomyces spinichromogenes var. kujimyceticus. 3. The structure of kujimycin A and kujimycin B. J Antibiot (Tokyo). 1969;22(12):629–34. doi: 10.7164/antibiotics.22.629 5367395.

90. Sheu CW, Salomon D, Simmons JL, Sreevalsan T, Freese E. Inhibitory Effects of Lipophilic Acids and Related Compounds on Bacteria and Mammalian Cells. Antimicrobial Agents and Chemotherapy. 1975;7(3):349–63. doi: 10.1128/aac.7.3.349 1137388

Bioassay- and metabolomics-guided screening of bioactive soil actinomycetes from the ancient city of Ihnasia, Egypt

Souhrn

Klíčová slova:

Zdroje

PLOS One

Aktuální možnosti diagnostiky a léčby litiáz