Killing of mycolic acid-containing bacteria aborted induction of antibiotic production by streptomyces in combined-culture

PLoS ONE

Volumn 10, Issue 11, 2015, Pages

  Asamizu, Shumpei ^a   Ozaki, Taro ^a   Teramoto, Kanae ^b   Satoh, Katsuya ^c   Onaka, Hiroyasu ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b JEOL LTD   (Japan)

^c JAPAN ATOMIC ENERGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MYCOLIC ACID; ANTIINFECTIVE AGENT; PIGMENT;

ARTICLE; BACTERIAL STRAIN; BACTERIUM; BACTERIUM COLONY; BACTERIUM CULTURE; CELL ADHESION; CELL AGGREGATION; CELL MEMBRANE; CONTROLLED STUDY; MYCELIUM; NONHUMAN; RHODOCOCCUS ERYTHROPOLIS; RHODOCOCCUS OPACUS; SCANNING ELECTRON MICROSCOPY; STREPTOMYCES LIVIDANS; TSUKAMURELLA PULMONIS; ACTINOMYCETALES; BIOSYNTHESIS; COCULTURE; CYTOLOGY; GAMMA RADIATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; RADIATION RESPONSE;

ACTINOMYCETALES; ANTI-BACTERIAL AGENTS; CELL MEMBRANE; COCULTURE TECHNIQUES; GAMMA RAYS; MYCOLIC ACIDS; PIGMENTS, BIOLOGICAL; STREPTOMYCES LIVIDANS;

EID: 84952683849     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0142372     Document Type: Article

References (55)

1. Marmann A, Aly AH, Lin W, Wang B, Proksch P (2014) Co-cultivation-a powerful emerging tool for enhancing the chemical diversity of microorganisms. Mar Drugs 12: 1043-1065. doi: 10.3390/md12021043 PMID: 24549204
2. Bertrand S, Bohni N, Schnee S, Schumpp O, Gindro K, et al. (2014) Metabolite induction via microorganism co-culture: a potential way to enhance chemical diversity for drug discovery. Biotechnol Adv 32: 1180-1204. doi: 10.1016/j.biotechadv.2014.03.001 PMID: 24651031
3. Onaka H, Mori Y, Igarashi Y, Furumai T (2011) Mycolic acid-containing bacteria induce natural-product biosynthesis in Streptomyces species. Appl Environ Microbiol 77: 400-406. doi: 10.1128/AEM.01337-10 PMID: 21097597
4. Berdy J (2005) Bioactive microbial metabolites. J Antibiot (Tokyo) 58: 1-26.
5. Nett M, Ikeda H, Moore BS (2009) Genomic basis for natural product biosynthetic diversity in the actinomycetes. Nat Prod Rep 26: 1362-1384. doi: 10.1039/b817069j PMID: 19844637
6. Liu G, Chater KF, Chandra G, Niu G, Tan H (2013) Molecular regulation of antibiotic biosynthesis in streptomyces. Microbiol Mol Biol Rev 77: 112-143. doi: 10.1128/MMBR.00054-12 PMID: 23471619
7. Yoon V, Nodwell JR (2014) Activating secondary metabolism with stress and chemicals. J Ind Microbiol Biotechnol 41: 415-424. doi: 10.1007/s10295-013-1387-y PMID: 24326978
8. Horinouchi S, Beppu T (2007) Hormonal control by A-factor of morphological development and secondary metabolism in Streptomyces. Proc Jpn Acad Ser B Phys Biol Sci 83: 277-295. doi: 10.2183/pjab/83.277 PMID: 24367152
9. Martin JF (2004) Phosphate control of the biosynthesis of antibiotics and other secondary metabolites is mediated by the PhoR-PhoP system: an unfinished story. J Bacteriol 186: 5197-5201. PMID: 15292120
10. Rigali S, Titgemeyer F, Barends S, Mulder S, Thomae AW, et al. (2008) Feast or famine: the global regulator DasR links nutrient stress to antibiotic production by Streptomyces. EMBO Rep 9: 670-675. doi: 10.1038/embor.2008.83 PMID: 18511939
11. Recio E, Colinas A, Rumbero A, Aparicio JF, Martin JF (2004) PI factor, a novel type quorum-sensing inducer elicits pimaricin production in Streptomyces natalensis. J Biol Chem 279: 41586-41593. PMID: 15231842
12. Onaka H, Tabata H, Igarashi Y, Sato Y, Furumai T (2001) Goadsporin, a chemical substance which promotes secondary metabolism and morphogenesis in streptomycetes. I. Purification and characterization. J Antibiot (Tokyo) 54: 1036-1044.
13. Igarashi Y, Kan Y, Fujii K, Fujita T, Harada K, et al. (2001) Goadsporin, a chemical substance which promotes secondary metabolism and Morphogenesis in streptomycetes. II. Structure determination. J Antibiot (Tokyo) 54: 1045-1053.
14. Andres N, Wolf H, Zahner H (1990) Hormaomycin, a New Peptide Lactone Antibiotic Effective in Inducing Cytodifferentiation and Antibiotic Biosynthesis in Some Streptomyces Species. Zeitschrift Fur Naturforschung C-a Journal of Biosciences 45: 850-855.
15. Ahmed S, Craney A, Pimentel-Elardo SM, Nodwell JR (2013) A synthetic, species-specific activator of secondary metabolism and sporulation in Streptomyces coelicolor. Chembiochem 14: 83-91. doi: 10.1002/cbic.201200619 PMID: 23239420
16. Craney A, Ozimok C, Pimentel-Elardo SM, Capretta A, Nodwell JR (2012) Chemical perturbation of secondary metabolism demonstrates important links to primary metabolism. Chem Biol 19: 1020-1027. doi: 10.1016/j.chembiol.2012.06.013 PMID: 22921069
17. Schroeckh V, Scherlach K, Nutzmann HW, Shelest E, Schmidt-Heck W, et al. (2009) Intimate bacterialfungal interaction triggers biosynthesis of archetypal polyketides in Aspergillus nidulans. Proc Natl Acad Sci U S A 106: 14558-14563. doi: 10.1073/pnas.0901870106 PMID: 19666480
18. Netzker T, Fischer J, Weber J, Mattern DJ, Konig CC, et al. (2015) Microbial communication leading to the activation of silent fungal secondary metabolite gene clusters. Front Microbiol 6: 299. doi: 10.3389/fmicb.2015.00299 PMID: 25941517
19. Traxler MF, Kolter R (2015) Natural products in soil microbe interactions and evolution. Nat Prod Rep.
20. Vargas-Bautista C, Rahlwes K, Straight P (2014) Bacterial competition reveals differential regulation of the pks genes by Bacillus subtilis. J Bacteriol 196: 717-728. doi: 10.1128/JB.01022-13 PMID: 24187085
21. Traxler MF, Watrous JD, Alexandrov T, Dorrestein PC, Kolter R (2013) Interspecies interactions stimulate diversification of the Streptomyces coelicolor secreted metabolome. MBio 4.
22. Wu C, Zacchetti B, Ram AF, van Wezel GP, Claessen D, et al. (2015) Expanding the chemical space for natural products by Aspergillus-Streptomyces co-cultivation and biotransformation. Sci Rep 5: 10868. doi: 10.1038/srep10868 PMID: 26040782
23. Luti KJ, Mavituna F (2011) Elicitation of Streptomyces coelicolor with dead cells of Bacillus subtilis and Staphylococcus aureus in a bioreactor increases production of undecylprodigiosin. Appl Microbiol Biotechnol 90: 461-466. doi: 10.1007/s00253-010-3032-2 PMID: 21222119
24. Luti KJ, Mavituna F (2011) Streptomyces coelicolor increases the production of undecylprodigiosin when interacted with Bacillus subtilis. Biotechnol Lett 33: 113-118. doi: 10.1007/s10529-010-0401-y PMID: 20878541
25. Nutzmann HW, Reyes-Dominguez Y, Scherlach K, Schroeckh V, Horn F, et al. (2011) Bacteria-induced natural product formation in the fungus Aspergillus nidulans requires Saga/Ada-mediated histone acetylation. Proc Natl Acad Sci U S A 108: 14282-14287. doi: 10.1073/pnas.1103523108 PMID: 21825172
26. Straight PD, Kolter R (2009) Interspecies chemical communication in bacterial development. Annu Rev Microbiol 63: 99-118. doi: 10.1146/annurev.micro.091208.073248 PMID: 19566421
27. Taga ME, Bassler BL (2003) Chemical communication among bacteria. Proc Natl Acad Sci U S A 100 Suppl 2: 14549-14554. PMID: 12949263
28. Igarashi Y, Kim Y, In Y, Ishida T, Kan Y, et al. (2010) Alchivemycin A, a bioactive polycyclic polyketide with an unprecedented skeleton from Streptomyces sp. Org Lett 12: 3402-3405. doi: 10.1021/ol1012982 PMID: 20670006
29. Hoshino S, Zhang L, Awakawa T, Wakimoto T, Onaka H, et al. (2014) Arcyriaflavin E, a new cytotoxic indolocarbazole alkaloid isolated by combined-culture of mycolic acid-containing bacteria and Streptomyces cinnamoneus NBRC 13823. J Antibiot (Tokyo).
30. Hoshino S, Wakimoto T, Onaka H, Abe I (2015) Chojalactones A-C, Cytotoxic Butanolides Isolated from Streptomyces sp. Cultivated with Mycolic Acid Containing Bacterium. Org Lett.
31. Sugiyama R, Nishimura S, Ozaki T, Asamizu S, Onaka H, et al. (2015) 5-Alkyl-1,2,3,4-tetrahydroquinolines, New Membrane-Interacting Lipophilic Metabolites Produced by Combined Culture of Streptomyces nigrescens and Tsukamurella pulmonis. Org Lett.
32. Derewacz DK, Covington BC, McLean JA, Bachmann BO (2015) Mapping Microbial Response Metabolomes for Induced Natural Product Discovery. ACS Chem Biol.
33. Smith I (2003) Mycobacterium tuberculosis pathogenesis and molecular determinants of virulence. Clin Microbiol Rev 16: 463-496. PMID: 12857778
34. Kimura E (2003) Metabolic engineering of glutamate production. Adv Biochem Eng Biotechnol 79: 37-57. PMID: 12523388
35. Martinkova L, Uhnakova B, Patek M, Nesvera J, Kren V (2009) Biodegradation potential of the genus Rhodococcus. Environ Int 35: 162-177. doi: 10.1016/j.envint.2008.07.018 PMID: 18789530
36. Marrakchi H, Laneelle MA, Daffe M (2014) Mycolic acids: structures, biosynthesis, and beyond. Chem Biol 21: 67-85. doi: 10.1016/j.chembiol.2013.11.011 PMID: 24374164
37. Bansal-Mutalik R, Nikaido H (2014) Mycobacterial outer membrane is a lipid bilayer and the inner membrane is unusually rich in diacyl phosphatidylinositol dimannosides. Proc Natl Acad Sci U S A 111: 4958-4963. doi: 10.1073/pnas.1403078111 PMID: 24639491
38. Ohno M, Okano I, Watsuji T, Kakinuma T, Ueda K, et al. (1999) Establishing the independent culture of a strictly symbiotic bacterium Symbiobacterium thermophilum from its supporting Bacillus strain. Biosci Biotechnol Biochem 63: 1083-1090. PMID: 10427695
39. Na KS, Kuroda A, Takiguchi N, Ikeda T, Ohtake H, et al. (2005) Isolation and characterization of benzene-tolerant Rhodococcus opacus strains. J Biosci Bioeng 99: 378-382. PMID: 16233805
40. Yamazaki H, Ohnishi Y, Horinouchi S (2003) Transcriptional switch on of ssgA by A-factor, which is essential for spore septum formation in Streptomyces griseus. J Bacteriol 185: 1273-1283. PMID: 12562798
41. Yano I, Saito K, Furukawa Y, Kusunose M (1972) Structural analysis of molecular species of nocardomycolic acids from Nocardia erythropolis by the combined system of gas chromatography and mass spectrometry. FEBS Lett 21: 215-219. PMID: 11946513
42. Kieser T, Bibb MJ, Buttner MJ, Chater KF, Hopwood DA (2000) Practical Streptomyces Genetics. Norwich, UK: John Innes Foundation.
43. Chao Y, Zhang T (2011) Optimization of fixation methods for observation of bacterial cell morphology and surface ultrastructures by atomic force microscopy. Appl Microbiol Biotechnol 92: 381-392. doi: 10.1007/s00253-011-3551-5 PMID: 21881891
44. Puchtler H, Meloan SN (1985) On the chemistry of formaldehyde fixation and its effects on immunohistochemical reactions. Histochemistry 82: 201-204. PMID: 3997553
45. Teramoto K, Tamura T, Hanada S, Sato T, Kawasaki H, et al. (2013) Simple and rapid characterization of mycolic acids from Dietzia strains by using MALDI spiral-TOFMS with ultra high mass-resolving power. J Antibiot (Tokyo) 66: 713-717.
46. Teramoto K, Suga M, Sato T, Wada T, Yamamoto A, et al. (2015) Characterization of mycolic acids in total fatty acid methyl ester fractions from Mycobacterium species by high resolution MALDI-TOFMS. Mass Spectrom (Tokyo) 4: A0035.
47. Butler WR, Guthertz LS (2001) Mycolic acid analysis by high-performance liquid chromatography for identification of Mycobacterium species. Clin Microbiol Rev 14: 704-726, table of contents. PMID: 11585782
48. Min J, Lee CW, Gu MB (2003) Gamma-radiation dose-rate effects on DNA damage and toxicity in bacterial cells. Radiat Environ Biophys 42: 189-192. PMID: 13680259
49. Krisko A, Radman M (2010) Protein damage and death by radiation in Escherichia coli and Deinococcus radiodurans. Proc Natl Acad Sci U S A 107: 14373-14377. doi: 10.1073/pnas.1009312107 PMID: 20660760
50. Winn M, Casey E, Habimana O, Murphy CD (2014) Characteristics of Streptomyces griseus biofilms in continuous flow tubular reactors. FEMS Microbiol Lett 352: 157-164. doi: 10.1111/1574-6968.12378 PMID: 24417230
51. Elias S, Banin E (2012) Multi-species biofilms: living with friendly neighbors. FEMS Microbiol Rev 36: 990-1004. doi: 10.1111/j.1574-6976.2012.00325.x PMID: 22229800
52. Kolenbrander PE, Palmer RJ Jr., Periasamy S, Jakubovics NS (2010) Oral multispecies biofilm development and the key role of cell-cell distance. Nat Rev Microbiol 8: 471-480. doi: 10.1038/nrmicro2381 PMID: 20514044
53. Bendinger B, Rijnaarts HH, Altendorf K, Zehnder AJ (1993) Physicochemical cell surface and adhesive properties of coryneform bacteria related to the presence and chain length of mycolic acids. Appl Environ Microbiol 59: 3973-3977. PMID: 16349100
54. Antunes CA, Sanches dos Santos L, Hacker E, Kohler S, Bosl K, et al. (2015) Characterization of DIP0733, a multi-functional virulence factor of Corynebacterium diphtheriae. Microbiology 161: 639-647. doi: 10.1099/mic.0.000020 PMID: 25635272
55. Zhang Z, Pen Y, Edyvean RG, Banwart SA, Dalgliesh RM, et al. (2010) Adhesive and conformational behaviour of mycolic acid monolayers. Biochim Biophys Acta 1798: 1829-1839. doi: 10.1016/j.bbamem.2010.05.024 PMID: 20529662