Marine Sediment-Derived Streptomyces Bacteria from British Columbia, Canada Are a Promising Microbiota Resource for the Discovery of Antimicrobial Natural Products

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Dalisay, Doralyn S ^a,b   Williams, David E ^a   Wang, Xiao Ling ^a   Centko, Ryan ^a   Chen, Jessie ^a   Andersen, Raymond J ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; ANTIMYCIN A2B; BUTANOLIDE DERIVATIVE; HYDROGEN; HYDROXYBENZOIC ACID; NATURAL PRODUCT; NIGERICIN; NOVOBIOCIN DERIVATIVE; RNA 16S; UNCLASSIFIED DRUG;

ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL METABOLISM; BACTERIAL STRAIN; BACTERIUM CULTURE; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATION; CANADA; CHEMICAL ANALYSIS; CONTROLLED STUDY; DRUG STRUCTURE; MARINE SEDIMENT; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MICROFLORA; MINIMUM INHIBITORY CONCENTRATION; NEW SPECIES; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; SEDIMENT; STREPTOMYCES; STRUCTURE ACTIVITY RELATION;

ANTI-INFECTIVE AGENTS; BIOLOGICAL PRODUCTS; BRITISH COLUMBIA; DRUG DISCOVERY; EVOLUTION, MOLECULAR; GEOLOGIC SEDIMENTS; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIAL SENSITIVITY TESTS; MICROBIOTA; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S; STREPTOMYCES; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84885400514     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0077078     Document Type: Article

References (65)

1. Molinski TF, Dalisay DS, Lievens SL, Saludes JP, (2009) Drug development from marine natural products. Nat Rev Drug Discov 8: 69-85. doi:10.1038/nrd2487. PubMed: 19096380.
2. Mayer AMS, Rodríguez AD, Berlinck RGS, Fusetani N, (2011) Marine pharmacology in 2007-8: Marine compounds with antibacterial, anticoagulant, antifungal, anti-inflammatory, antimalarial, antiprotozoal, antituberculosis, and antiviral activities; affecting the immune and nervous system, and other miscellaneous mechanisms of action. Comp Biochem Physiol C Toxicol Pharmacol 153: 191-222. doi:10.1016/j.cbpc.2010.08.008. PubMed: 20826228.
3. Database M Marinlit Database.
4. Blunt JW, Copp BR, Munro MHG, Northcote PT, Prinsep MR, (2011) Marine natural products. Nat Prod Rep 28: 196-268. doi:10.1039/c005001f. PubMed: 21152619.
5. Blunt JW, Copp BR, Keyzers RA, Munro MHG, Prinsep MR, (2012) Marine natural products. Nat Prod Rep 29: 144-222. doi:10.1039/c2np00090c. PubMed: 22193773.
6. Bernan VS, Greenstein M, Maiese WM, (1997) Marine microorganisms as a source of new natural products. Adv Appl Microbiol 43: 57-90. doi:10.1016/S0065-2164(08)70223-5. PubMed: 9097412.
7. Imhoff JF, Labes A, Wiese J, (2011) Bio-mining the microbial treasures of the ocean: New natural products. Biotechnol Adv 29: 468-482. doi:10.1038/nbt0611-468. PubMed: 21419836.
8. Chater KF, (2006) Streptomyces inside-out: a new perspective on the bacteria that provide us with antibiotics. Philos Trans R Soc Lond B Biol Sci 361: 761-768. doi:10.1098/rstb.2005.1758. PubMed: 16627293.
9. Strohl WR, (1997) Industrial antibiotics: today and the future. In: WR S, editor. Biotechnology of antibiotics. New York, NY: Marcel Dekker. pp. 1-47.
10. Fenical W, Jensen PR, (2006) Developing a new resource for drug discovery: marine actinomycete bacteria. Nat Chem Biol 2: 666-673. doi:10.1038/nchembio841. PubMed: 17108984.
11. Pathom-aree W, Stach JEM, Ward AC, Horikoshi K, Bull AT, et al. (2006) Diversity of actinomycetes isolated from Challenger Deep sediment (10,898 m) from the Mariana Trench. Extremophiles 10: 181-189. doi:10.1007/s00792-005-0482-z. PubMed: 16538400.
12. Mincer TJ, Jensen PR, Kauffman CA, Fenical W, (2002) Widespread and persistent populations of a major new marine actinomycete taxon in ocean sediments. Appl Environ Microbiol 68: 5005-5011. doi:10.1128/AEM.68.10.5005-5011.2002. PubMed: 12324350.
13. Gulder TAM, Moore BS, (2010) Salinosporamide natural products: Potent 20 S proteasome inhibitors as promising cancer chemotherapeutics. Angew Chem Int Ed 49: 9346-9367 doi:10.1002/anie.201000728.
14. Feling RH, Buchanan GO, Mincer TJ, Kauffman CA, Jensen PR, et al. (2003) Salinosporamide A: A highly cytotoxic proteasome inhibitor from a novel microbial source, a marine bacterium of the new genus Salinospora. Angew Chem Int Ed 42: 355-357 doi:10.1002/anie.200390115. PubMed: 12548698.
15. Fenical W, Jensen PR, Palladino MA, Lam KS, Lloyd GK, et al. (2009) Discovery and development of the anticancer agent salinosporamide A (NPI-0052). Bioorg Med Chem 17: 2175-2180. doi:10.1016/j.bmc.2008.10.075. PubMed: 19022674.
16. Gourdeau H, McAlpine JB, Ranger M, Simard B, Berger F, et al. (2008) Identification, characterization and potent antitumor activity of ECO-4601, a novel peripheral benzodiazepine receptor ligand. Cancer Chemother Pharmacol 61: 911-921. doi:10.1007/s00280-007-0544-2. PubMed: 17622531.
17. Charan RD, Schlingmann G, Janso J, Bernan V, Feng XD, et al. (2004) Diazepinomicin, a new antimicrobial alkaloid from a marine Micromonospora sp. J Nat Prod 67: 1431-1433. doi:10.1021/np040042r. PubMed: 15332871.
18. Perez Baz J, Cañedo LM, Fernández Puentes JL, Silva Elipe MV, (1997) Thiocoraline, a novel depsipeptide with antitumor activity produced by a marine Micromonospora: II. Physico-chemical properties and structure determination. J Antibiot Tokyo 50: 738-741. doi:10.7164/antibiotics.50.738. PubMed: 9360618.
19. Erba E, Bergamaschi D, Ronzoni S, Faretta M, Taverna S, et al. (1999) Mode of action of thiocoraline, a natural marine compound with anti-tumour activity. Br J Cancer 80: 971-980. doi:10.1038/sj.bjc.6690451. PubMed: 10362104.
20. Zotchev SB, (2012) Marine actinomycetes as an emerging resource for the drug development pipelines. J Biotechnol 158: 168-175. doi:10.1016/j.jbiotec.2011.06.002. PubMed: 21683100.
21. Calfee DP, (2012) Methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci, and other Gram-positives in healthcare. Curr Opin Infect Dis 25: 385-394. doi:10.1097/QCO.0b013e3283553441. PubMed: 22614523.
22. Jabes D, (2011) The antibiotic R&D pipeline: an update. Curr Opin Microbiol 14: 564-569. doi:10.1016/j.mib.2011.08.002. PubMed: 21873107.
23. Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA, (2000) Practical Streptomyces Genetics. Norwich, England: The John Innes Foundation.
24. Kataoka M, Ueda K, Kudo T, Seki T, Yoshida T, (1997) Application of the variable region in 16S rDNA to create an index for rapid species identification in the genus Streptomyces. FEMS Microbiol Lett 151: 249-255. doi:10.1111/j.1574-6968.1997.tb12578.x. PubMed: 9244758.
25. Metsä-Ketelä M, Halo L, Munukka E, Hakala J, Mäntsälä P, et al. (2002) Molecular evolution of aromatic polyketides and comparative sequence analysis of polyketide ketosynthase and 16S ribosomal DNA genes from various streptomyces species. Appl Environ Microbiol 68: 4472-4479. doi:10.1128/AEM.68.9.4472-4479.2002. PubMed: 12200302.
26. Feldgarden M, Byrd N, Cohan FM, (2003) Gradual evolution in bacteria: evidence from Bacillus systematics. MicrobiolSgm 149: 3565-3573. PubMed: 14663088.
27. Egan S, Wiener P, Kallifidas D, Wellington EMH, (2001) Phylogeny of Streptomyces species and evidence for horizontal transfer of entire and partial antibiotic gene clusters. Antonie Van Leeuwenhoek 79: 127-133. doi:10.1023/A:1010296220929. PubMed: 11519998.
28. Arcamone FM, Bertazzoli C, Ghione M, Scotti T, (1959) Melanosporin and elaiophylin, new antibiotics from Streptomyces melanosporus (sive melanosporofaciens) n.sp Giorn Microbiol 7: 207-216.
29. Fiedler HP, Wörner W, Zähner H, Kaiser HP, Keller-Schierlein W, et al. (1981) Metabolic products of microorganisms. 200 Isolation and characterization of niphithricins A, B, and elaiophylin, antibiotics produced by Streptomyces violaceoniger. J Antibiot 34: 1107-1118. doi:10.7164/antibiotics.34.1107. PubMed: 7035426.
30. Toshima K, Tatsuta K, Kinoshita M, (1986) Total synthesis of elaiophylin (azalomycin-B). Tetrahedron Lett 27: 4741-4744. doi:10.1016/S0040-4039(00)85053-4.
31. Berger I, Rachlin AI, Scott WE, Sternbach LH, Goldberg MW, (1951) The isolation of three crystalline antibiotics from Streptomyces. J Am Chem Soc 73: 5295-5298. doi:10.1021/ja01155a084.
32. Harned RL, Hidy PH, Corum CJ, Jones KL, (1951) Niegericin, a new crystalline antibiotic from an unidentified Streptomyces. Antibiot Chemother 1: 594-596.
33. Westley JW, (1983) Polyether Antibiotics. Naturally occur- ring acid zonophores. New York: MarcelDekker,Inc.
34. Harold FM, Baarda JR, (1968) Effects of nigericin and monensin on cation permeability of Streptococcus faecalis and metabolic capabilities of potassium-depleted cells. J Bacteriol 95: 816-823. PubMed: 4966827.
35. Cho KW, Lee HS, Rho JR, Kim TS, Mo SJ, et al. (2001) New lactone-containing metabolites from a marine-derived bacterium of the genus Streptomyces. J Nat Prod 64: 664-667. doi:10.1021/np000599g. PubMed: 11374972.
36. Mukku VJ, Speitling M, Laatsch H, Helmke E, (2000) New butenolides from two marine streptomycetes. J Nat Prod 63: 1570-1572. doi:10.1021/np0001676. PubMed: 11087613.
37. Abidi SL, (1988) High-performance liquid-chromatographic separation of subcomponents of antimycin-A. J Chromatogr 447: 65-79. doi:10.1016/0021-9673(88)90007-6. PubMed: 3209667.
38. Kluepfel D, Sehgal SN, Vézina C, (1970) Antimycin A components. I. Isolation and biological activity. J Antibiot Tokyo 23: 75-80. doi:10.7164/antibiotics.23.75. PubMed: 5416654.
39. Nakayama K, Okamoto F, Harada Y, (1956) Antimycin A: isolation from a new Streptomyces and activity against rice plant blast fungi. J Antibiot 9: 63-66. PubMed: 13345726.
40. Alexandre A, Lehninger AL, (1984) Bypass of the antimycin A block of mitochondrial electron-transport in relation to ubisemiquinone function. Biochim Biophys Acta 767: 120-129. doi:10.1016/0005-2728(84)90086-0. PubMed: 6091750.
41. Grimmelikhuijzen CJP, Marres CAM, Slater EC, (1975) Antimycin-insensitive mutants of Candida utilis II. The effects of antimycin on Cytochrome B. Biochim Biophys Acta 376: 533-548. doi:10.1016/0005-2728(75)90173-5. PubMed: 1168499.
42. Shunk CH, Stammer CH, Kaczka EA, Walton E, Spencer CF, et al. (1956) Novobiocin. II. Structure of Novobiocin. J Am Chem Soc 78: 1770-1771. doi:10.1021/ja01589a084.
43. Crow FW, Duholke WK, Farley KA, Hadden CE, Hahn DA, et al. (1999) Complete spectroscopic structural characterization of novobiocin, isonovobiocin, decarbamylnovobiocin, 2 ''-(O-carbamyl)novobiocin, and novobiocin-2 ',3 ''-carbonate. J Heterocyclic Chem 36: 365-370.
44. Meyers CLF, Oberthür M, Anderson JW, Kahne D, Walsh CT, (2003) Initial characterization of novobiocic acid noviosyl transferase activity of NovM in biosynthesis of the antibiotic novobiocin. Biochemistry 42: 4179-4189. doi:10.1021/bi0340088. PubMed: 12680772.
45. Meyers CLF, Oberthur M, Xu H, Heide L, Kahne D, et al. (2004) Characterization of NovP and NovN: Completion of novobiocin biosynthesis by sequential tailoring of the noviosyl ring. Angew Chem Int Ed 43: 67-70 doi:10.1002/anie.200352626.
46. Maxwell A, Lawson DM, (2003) The ATP-binding site of type II topoisomerases as a target for antibacterial drugs. Curr Top Med Chem 3: 283-303. doi:10.2174/1568026033452500. PubMed: 12570764.
47. Lewis RJ, Singh OMP, Smith CV, Skarzynski T, Maxwell A, et al. (1996) The nature of inhibition of DNA gyrase by the coumarins and the cyclothialidines revealed by X-ray crystallography. EMBO J 15: 1412-1420. PubMed: 8635474.
48. Holdgate GA, Tunnicliffe A, Ward WHJ, Weston SA, Rosenbrock G, et al. (1997) The entropic penalty of ordered water accounts for weaker binding of the antibiotic novobiocin to a resistant mutant of DNA gyrase: A thermodynamic and crystallographic study. Biochemistry 36: 9663-9673. doi:10.1021/bi970294+ PubMed: 9245398.
49. Marcu MG, Chadli A, Bouhouche I, Catelli M, Neckers LM, (2000) The heat shock protein 90 antagonist novobiocin interacts with a previously unrecognized ATP-binding domain in the carboxyl terminus of the chaperone. J Biol Chem 275: 37181-37186. doi:10.1074/jbc.M003701200. PubMed: 10945979.
50. Zhao RM, Houry WA, (2005) Hsp90: a chaperone for protein folding and gene regulation. Biochem Cell Biol 83: 703-710. doi:10.1139/o05-158. PubMed: 16333321.
51. Chiosis G, Vilenchik M, Kim J, Solit D, (2004) Hsp90: the vulnerable chaperone. Drug Discov Today 9: 881-888. doi:10.1016/S1359-6446(04)03245-3. PubMed: 15475321.
52. Heide L, (2009) The aminocoumarins: biosynthesis and biology. Nat Prod Rep 26: 1241-1250. doi:10.1039/b808333a. PubMed: 19779639.
53. Flatman RH, Eustaquio A, Li SM, Heide L, Maxwell A, (2006) Structure-activity relationships of aminocoumarin-type gyrase and topoisomerase IV inhibitors obtained by combinatorial biosynthesis. Antimicrob Agents Chemother 50: 1136-1142. doi:10.1128/AAC.50.4.1136-1142.2006. PubMed: 16569821.
54. Burlison JA, Neckers L, Smith AB, Maxwell A, Blagg BSJ, (2006) Novobiocin: Redesigning a DNA gyrase inhibitor for selective inhibition of Hsp90. J Am Chem Soc 128: 15529-15536. doi:10.1021/ja065793p. PubMed: 17132020.
55. Yu XM, Shen G, Neckers L, Blake H, Holzbeierlein J, et al. (2005) Hsp90 inhibitors identified from a library of novobiocin analogues. J Am Chem Soc 127: 12778-12779. doi:10.1021/ja0535864. PubMed: 16159253.
56. Lafitte D, Lamour V, Tsvetkov PO, Makarov AA, Klich M, et al. (2002) DNA gyrase interaction with coumarin-based inhibitors: The role of the hydroxybenzoate isopentenyl moiety and the 5 '-methyl group of the noviose. Biochemistry 41: 7217-7223. doi:10.1021/bi0159837. PubMed: 12044152.
57. Williams DE, Dalisay DS, Patrick BO, Matainaho T, Andrusiak K, et al. (2011) Padanamides A and B, highly modified linear tetrapeptides produced in culture by a Streptomyces sp isolated from a marine sediment. Org Lett 13: 3936-3939. doi:10.1021/ol2014494. PubMed: 21749075.
58. Williams DE, Dalisay DS, Li F, Amphlett J, Maneerat W, et al. (2012) Nahuoic Acid A produced by a Streptomyces sp. isolated from a marine Sediment is a selective SAM-competitive inhibitor of the histone methyltransferase SETD8. Org Lett 18: 414-417. PubMed: 23272941.
59. Mincer TJ, Fenical W, Jensen PR, (2005) Culture-dependent and culture-independent diversity within the obligate marine actinomycete genus Salinispora. Appl Environ Microbiol 71: 7019-7028. doi:10.1128/AEM.71.11.7019-7028.2005. PubMed: 16269737.
60. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. J Mol Biol 215: 403-410. doi:10.1016/S0022-2836(05)80360-2. PubMed: 2231712.
61. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG, (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882. doi:10.1093/nar/25.24.4876. PubMed: 9396791.
62. Saitou N, Nei M, (1987) The neighbor-joining method- a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425. PubMed: 3447015.
63. Jukes TH, Cantor CR, (1969) Evolution of protein molecules. In: HNMeds. Mammalian Protein Metabolism. New York: Academic Press. pp. pp. 21-132.
64. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739. doi:10.1093/molbev/msr121. PubMed: 21546353.
65. Laatsch H, (2007) Antibase 2007 SciDex - the natural products identifier. Weinheim, Germany: Wiley-VCH Verlag.