Specialised metabolites regulating antibiotic biosynthesis in Streptomyces spp.

FEMS Microbiology Reviews

Volumn 40, Issue 4, 2016, Pages 554-573

  Niu, Guoqing ^a   Chater, Keith F ^b   Tian, Yuqing ^a   Zhang, Jihui ^a   Tan, Huarong ^a  

^a INSTITUTE OF MICROBIOLOGY   (China)

^b NORWICH RESEARCH PARK   (United Kingdom)

Author keywords

Antibiotic biosynthesis; Interspecies communication; Regulation; Signalling molecules; Streptomyces; butyrolactones

Indexed keywords

ANTIBIOTIC AGENT; BINDING PROTEIN; DRUG METABOLITE; GAMMA BUTYROLACTONE; LIGAND; REGULATOR PROTEIN; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; PROTEIN BINDING;

ADPA GENE; ANTIBIOTIC BIOSYNTHESIS; ANTIBIOTIC RESISTANCE; ARTICLE; AUTOREGULATION; BACTERIAL GENOME; CELL COMMUNICATION; GENE CLUSTER; MICROBIAL COMMUNITY; NONHUMAN; PROTEIN INTERACTION; REGULATOR GENE; SECONDARY METABOLISM; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; STREPTOMYCES; STREPTOMYCES LAVENDULAE; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; ORGANISMAL INTERACTION; PHYSIOLOGY;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; LIGANDS; MICROBIAL INTERACTIONS; PROTEIN BINDING; SIGNAL TRANSDUCTION; STREPTOMYCES;

EID: 84977109304     PISSN: 01686445     EISSN: 15746976     Source Type: Journal    
DOI: 10.1093/femsre/fuw012     Document Type: Article

References (187)

1. Abrudan MI, Smakman F, Grimbergen AJ et al. Socially mediated induction and suppression of antibiosis during bacterial coexistence. P Natl Acad Sci USA 2015;112:11054-9.
2. Ahmed S, Craney A, Pimentel-Elardo SM et al. A synthetic, species-specific activator of secondary metabolism and sporulation in Streptomyces coelicolor. Chembiochem 2013;14:83-91.
3. Ahmer BM. Cell-to-cell signalling in Escherichia coli and Salmonella enterica. Mol Microbiol 2004;52:933-45.
4. Amano S,Morota T, Kano YK et al. Promomycin, a polyether promoting antibiotic production in Streptomyces spp. J Antibiot 2010;63:486-91.
5. Aminov RI. The role of antibiotics and antibiotic resistance in nature. Environ Microbiol 2009;11:2970-88.
6. Andersson DI, Hughes D. Microbiological effects of sublethal levels of antibiotics. Nat Rev Microbiol 2014;12:465-78.
7. Ando N, Matsumori N, Sakuda S et al. Involvement of afsA in Afactor biosynthesis as a key enzyme. J Antibiot 1997;50:847-52.
8. Arakawa K. Genetic and biochemical analysis of the antibiotic biosynthetic gene clusters on the Streptomyces linear plasmid. Biosci Biotech Bioch 2014;78:183-9.
9. Arakawa K, Tsuda N, Taniguchi A et al. The butenolide signaling molecules SRB1 and SRB2 induce lankacidin and lankamycin production in Streptomyces rochei. Chembiochem 2012;13:1447-57.
10. Arias AA, Lambert S,Martinet L et al. Growth of desferrioxaminedeficient Streptomyces mutants through xenosiderophore piracy of airborne fungal contaminations. FEMS Microbiol Ecol 2015;91, DOI: 10.1093/femsec/fiv080.
11. Bakker MG, Schlatter DC, Otto-Hanson L et al. Diffuse symbioses: roles of plant-plant, plant-microbe and microbemicrobe interactions in structuring the soil microbiome. Mol Ecol 2014;23:1571-83.
12. Balagadde FK, You L, Hansen CL et al. Long-term monitoring of bacteria undergoing programmed population control in amicrochemostat. Science 2005;309:137-40.
13. Barger SR, Hoefler BC, Cubillos-Ruiz A et al. Imaging secondary metabolism of Streptomyces sp. Mg1 during cellular lysis and colony degradation of competing Bacillus subtilis. Anton Leeuw 2012;102:435-45.
14. Behrens S, Lösekann T, Pett-Ridge J et al. Linking microbial phylogeny to metabolic activity at the single-cell level by using enhanced element labeling-catalyzed reporter deposition fluorescence in situ hybridization (EL-FISH) and NanoSIMS. Appl Environ Microb 2008;74:3143-50.
15. Bertrand S, Bohni N, Schnee S et al. Metabolite induction via microorganism co-culture: a potentialway to enhance chemical diversity for drug discovery. Biotechnol Adv 2014;32:1180-204.
16. Bhukya H, Bhujbalrao R, Bitra A et al. Structural and functional basis of transcriptional regulation by TetR family protein CprB from S. coelicolor A3(2). Nucleic Acids Res 2014;42:10122-33. Biarnes-Carrera M, Breitling R, Takano E. Butyrolactone signalling circuits for synthetic biology. Curr Opin Chem Biol 2015;28:91-8.
17. Biarnes-Carrera M, Breitling R, Takano E. Butyrolactone signalling circuits for synthetic biology. Curr Opin Chem Biol 2015;28:91-8
18. Bibb MJ. Regulation of secondary metabolism in streptomycetes. Curr Opin Microbiol 2005;8:208-15.
19. Birko Z, Bialek S, Buzas K et al. The secreted signaling protein factor C triggers the A-factor response regulon in Streptomyces griseus: overlapping signaling routes. Mol Cell Proteomics 2007;6:1248-56.
20. Birko Z, Sumegi A, Vinnai A et al. Characterization of the gene for factor C, an extracellular signal protein involved in morphological differentiation of Streptomyces griseus. Microbiology 1999;145:2245-53.
21. Biro S, Bekesi I, Vitalis S et al. A substance effecting differentiation in Streptomyces griseus. Purification and properties. Eur J Biochem 1980;103:359-63.
22. Biswas A, Swarnkar RK, Hussain B et al. Fluorescence quenching studies of gamma-butyrolactone binding protein (CprB) from Streptomyces coelicolor A3(2). J Phys Chem B 2014;118:10035-42.
23. Bleich R,Watrous JD, Dorrestein PC et al. Thiopeptide antibiotics stimulate biofilm formation in Bacillus subtilis. P Natl Acad Sci USA 2015;112:3086-91.
24. Brachmann AO, Brameyer S, Kresovic D et al. Pyrones as bacterial signaling molecules. Nat Chem Biol 2013;9:573-8.
25. Butcher RA, Schroeder FC, Fischbach MA et al. The identification of bacillaene, the product of the PksX megacomplex in Bacillus subtilis. P Natl Acad Sci USA 2007;104:1506-9.
26. Chandra G, Chater KF. Developmental biology of Streptomyces from the perspective of 100 actinobacterial genome sequences. FEMS Microbiol Rev 2014;38:345-79.
27. Chater KF, Biro S, Lee KJ et al. The complex extracellular biology of Streptomyces. FEMS Microbiol Rev 2010;34:171-98.
28. Chater KF, Kinashi H. Streptomyces linear plasmids: their discovery, functions, interactions with other replicons, and evolutionary significance. In: Meinhardt F, Klassen R (eds). Microbial Linear Plasmids. Berlin: Springer, 2007, 1-31.
29. Chemler JA, Buchholz TJ, Geders TWet al. Biochemical and structural characterization of germicidin synthase: analysis of a type III polyketide synthase that employs acyl-ACP as a starter unit donor. J Am Chem Soc 2012;134:7359-66.
30. Corre C. In search of the missing ligands for TetR family regulators. Chem Biol 2013;20:140-2.
31. Corre C, Haynes SW, Malet N et al. A butenolide intermediate in methylenomycin furan biosynthesis is implied by incorporation of stereospecifically 13C-labelled glycerols. Chem Commun 2010;46:4079-81.
32. Corre C, Song L, O'Rourke S et al. 2-Alkyl-4-hydroxymethylfuran-3-carboxylic acids, antibiotic production inducers discovered by Streptomyces coelicolor genome mining. P Natl Acad Sci USA 2008;105:17510-5.
33. Craney A, Ozimok C, Pimentel-Elardo SM et al. Chemical perturbation of secondary metabolism demonstrates important links to primary metabolism. Chem Biol 2012;19: 1020-7.
34. Cuthbertson L, Ahn Sang K, Nodwell Justin R. Deglycosylation as a mechanism of inducible antibiotic resistance revealed using a global relational tree for one-component regulators. Chem Biol 2013;20:232-40.
35. Cuthbertson L, Nodwell JR. The TetR family of regulators. Microbiol Mol Biol R 2013;77:440-75.
36. Davies J, Spiegelman GB, Yim G. The world of subinhibitory antibiotic concentrations. Curr Opin Microbiol 2006;9:445-53.
37. Davis JB, Bailey JD, Sello JK. Biomimetic synthesis of a new class of bacterial signaling molecules. Org Lett 2009;11:2984-7.
38. Deng Y, Wu J, Tao F et al. Listening to a new language: DSFbased quorum sensing in Gram-negative bacteria. Chem Rev 2011;111:160-73.
39. Du YL, Shen XL, Yu P et al. Gamma-butyrolactone regulatory system of Streptomyces chattanoogensis links nutrient utilization, metabolism, and development. Appl Environ Microb 2011;77:8415-26.
40. Engel P, Scharfenstein LL, Dyer JM et al. Disruption of a gene encoding a putative γ-butyrolactone-binding protein in Streptomyces tendae affects nikkomycin production. Appl Microbiol Biot 2001;56:414-9.
41. Fajardo A, Martínez JL. Antibiotics as signals that trigger specific bacterial responses. Curr Opin Microbiol 2008;11:161-7.
42. Fang J, Dorrestein PC. Emerging mass spectrometry techniques for the direct analysis of microbial colonies. Curr Opin Microbiol 2014;19:120-9.
43. Fedorova ND, Moktali V, Medema MH. Bioinformatics approaches and software for detection of secondary metabolic gene clusters. Methods Mol Biol 2012;944:23-45.
44. Flardh K, Buttner MJ. Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium. Nat Rev Microbiol 2009;7:36-49.
45. Folcher M, Gaillard H, Nguyen LT et al. Pleiotropic functions of a Streptomyces pristinaespiralis autoregulator receptor in development, antibiotic biosynthesis, and expression of a superoxide dismutase. J Biol Chem 2001;276:44297-306.
46. Goh EB, YimG, Tsui W, et al. Transcriptionalmodulation of bacterial gene expression by subinhibitory concentrations of antibiotics. P Natl Acad Sci USA 2002;99:17025-30.
47. Gomez-Escribano JP, Song L, Fox DJ et al. Structure and biosynthesis of the unusual polyketide alkaloid coelimycin P1, a metabolic product of the cpk gene cluster of Streptomyces coelicolor M145. Chem Sci 2012;3:2716-20.
48. Gräfe U, Reinhardt G, Schade W et al. Interspecific inducers of cytodifferentiation and anthracycline biosynthesis from Streptomyces bikinensis and S. cyaneofuscatus. Biotechnol Lett 1983;5:591-6.
49. Gräfe U, Schade W, Eritt I et al. A new inducer of anthracycline biosynthesis from Streptomyces viridochromogenes. J Antibiot 1982;35:1722-3.
50. Grkovic S, Brown MH, Roberts NJ et al. QacR is a repressor protein that regulates expression of the Staphylococcus aureus multidrug efflux pump QacA. J Biol Chem 1998; 273:18665-73.
51. Grkovic S, Hardie KM, Brown MH et al. Interactions of the QacR multidrug-binding protein with structurally diverse ligands: implications for the evolution of the binding pocket. Biochemistry 2003;42:15226-36.
52. Guyet A, Benaroudj N, Proux C et al. Identified members of the Streptomyces lividans AdpA regulon involved in differentiation and secondary metabolism. BMC Microbiol 2014;14:81.
53. Hara H, Ohnishi Y, Horinouchi S. DNA microarray analysis of global gene regulation by A-factor in Streptomyces griseus. Microbiology 2009;155:2197-210.
54. Hara O, Horinouchi S, Uozumi T et al. Genetic analysis of Afactor synthesis in Streptomyces coelicolor A3(2) and Streptomyces griseus. J Gen Microbiol 1983;129:2939-44.
55. Hesketh A, Chen WJ, Ryding J et al. The global role of ppGpp synthesis in morphological differentiation and antibiotic production in Streptomyces coelicolor A3(2). Genome Biol 2007;8:R161.
56. Higashi T, Iwasaki Y, Ohnishi Y et al. A-factor and phosphate depletion signals are transmitted to the grixazone biosynthesis genes via the pathway-specific transcriptional activator GriR. J Bacteriol 2007;189:3515-24.
57. Higo A, Hara H, Horinouchi S et al. Genome-wide distribution of AdpA, a global regulator for secondary metabolism andmorphological differentiation in Streptomyces, revealed the extent and complexity of the AdpA regulatory network. DNA Res 2012;19:259-73.
58. Hillen W, Berens C. Mechanisms underlying expression of Tn10 encoded tetracycline resistance. Annu Rev Microbiol 1994;48:345-69.
59. Hoffman LR, D'Argenio DA, MacCoss MJ et al. Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 2005;436:1171-5.
60. Hopwood DA. Streptomyces in Nature and Medicine: The Antibiotic Makers. New York, USA: Oxford University Press, 2007. Horinouchi S. Mining and polishing of the treasure trove in the bacterial genus Streptomyces. Biosci Biotech Bioch 2007;71:283-99.
61. Horinouchi S, Kumada Y, Beppu T. Unstable genetic determinant of A-factor biosynthesis in streptomycin-producing organisms: cloning and characterization. J Bacteriol 1984;158:481-7.
62. Hsiao NH, Gottelt M, Takano E. Regulation of antibiotic production by bacterial hormones. Methods Enzymol 2009a;458:143-57.
63. Hsiao NH, Nakayama S, MerloME et al. Analysis of two additional signaling molecules in Streptomyces coelicolor and the development of a butyrolactone-specific reporter system. Chem Biol 2009b;16:951-60.
64. Hsiao N-H, Söding J, Linke D et al. ScbA from Streptomyces coelicolor A3(2) has homology to fatty acid synthases and is able to synthesize γ-butyrolactones. Microbiology 2007;153:1394-404.
65. Huang J, Shi J, Molle V et al. Cross-regulation among disparate antibiotic biosynthetic pathways of Streptomyces coelicolor. Mol Microbiol 2005;58:1276-87.
66. Igarashi Y, Kan Y, Fujii K et al. Goadsporin, a chemical substance which promotes secondary metabolism and morphogenesis in streptomycetes. II. Structure determination. J Antibiot 2001;54:1045-53.
67. Imai Y, Sato S, Tanaka Y et al. Lincomycin at subinhibitory concentrations potentiates secondary metabolite production by Streptomyces spp. Appl Environ Microb 2015; 81:3869-79.
68. Kaltenpoth M, Strupat K, Svatos A. Linking metabolite production to taxonomic identity in environmental samples by (MA)LDI-FISH. ISME J 2016;10:527-31.
69. Kato JY, Funa N, Watanabe H et al. Biosynthesis of γ-butyrolactone autoregulators that switch on secondary metabolism andmorphological development in Streptomyces. P Natl Acad Sci USA 2007;104:2378-83.
70. Kawachi R, Akashi T, Kamitani Y et al. Identification of an AfsA homologue (BarX) from Streptomyces virginiae as a pleiotropic regulator controlling autoregulator biosynthesis, virginiamycin biosynthesis and virginiamycin M1 resistance. Mol Microbiol 2000;36:302-13.
71. Keymer JE, Galajda P, Muldoon C et al. Bacterial metapopulations in nanofabricated landscapes. P Natl Acad Sci USA 2006;103:17290-5.
72. Khokhlov AS, Tovarova II, Borisova LN et al. The A-factor, responsible for streptomycin biosynthesis bymutant strains of Actinomyces streptomycini. Dokl Akad Nauk SSSR 1967;177:232-5.
73. Kim HJ, Boedicker JQ, Choi JWet al. Defined spatial structure stabilizes a synthetic multispecies bacterial community. P Natl Acad Sci USA 2008;105:18188-93.
74. Kindaichi T, Ito T, Okabe S. Ecophysiological interaction between nitrifying bacteria and heterotrophic bacteria in autotrophic nitrifying biofilms as determined by microautoradiographyfluorescence in situ hybridization. Appl Environ Microb 2004;70:1641-50.
75. Kinoshita H, Ipposhi H, Okamoto S et al. Butyrolactone autoregulator receptor protein (BarA) as a transcriptional regulator in Streptomyces virginiae. J Bacteriol 1997;179:6986-93.
76. Kitani S, Doi M, Shimizu T et al. Control of secondary metabolism by farX,which is involved in the γ-butyrolactone biosynthesis of Streptomyces lavendulae FRI-5. Arch Microbiol 2010;192:211-20.
77. Kitani S, Iida A, Izumi TA et al. Identification of genes involved in the butyrolactone autoregulator cascade that modulates secondary metabolism in Streptomyces lavendulae FRI-5. Gene 2008;425:9-16.
78. Kitani S, Kinoshita H, Nihira T et al. In vitro analysis of the butyrolactone autoregulator receptor protein (FarA) of Streptomyces lavendulae FRI-5 reveals that FarA acts as a DNA-binding transcriptional regulator that controls its own synthesis. J Bacteriol 1999;181:5081-4.
79. Kitani S, Miyamoto KT, Takamatsu S et al. Avenolide, a Streptomyces hormone controlling antibiotic production in Streptomyces avermitilis. P Natl Acad Sci USA 2011; 108:16410-5.
80. Kitani S, Yamada Y, Nihira T. Gene replacement analysis of the butyrolactone autoregulator receptor (FarA) reveals that FarA acts as a novel regulator in secondary metabolism of Streptomyces lavendulae FRI-5. J Bacteriol 2001;183:4357-63.
81. Kondo K, Higuchi Y, Sakuda S et al. New virginiae butanolides from Streptomyces virginiae. J Antibiot 1989;42:1873-6.
82. Konig CC, Scherlach K, Schroeckh V et al. Bacterium induces cryptic meroterpenoid pathway in the pathogenic fungus Aspergillus fumigatus. Chembiochem 2013;14:938-42.
83. Kroiss J, Kaltenpoth M, Schneider B et al. Symbiotic streptomycetes provide antibiotic combination prophylaxis for wasp offspring. Nat Chem Biol 2010;6:261-3.
84. Kurniawan YN, Kitani S, Maeda A et al. Differential contributions of two SARP family regulatory genes to indigoidine biosynthesis in Streptomyces lavendulae FRI-5. Appl Microbiol Biot 2014;98:9713-21.
85. Kurosawa K, Ghiviriga I, Sambandan TG et al. Rhodostreptomycins, antibiotics biosynthesized following horizontal gene transfer from Streptomyces padanus to Rhodococcus fascians. J Am Chem Soc 2008;130:1126-7.
86. Le TB, Fiedler HP, den Hengst CD et al. Coupling of the biosynthesis and export of the DNA gyrase inhibitor simocyclinone in Streptomyces antibioticus. Mol Microbiol 2009;72:1462-74.
87. Le TB, Schumacher MA, Lawson DM et al. The crystal structure of the TetR family transcriptional repressor SimR bound to DNA and the role of a flexible N-terminal extension inminor groove binding. Nucleic Acids Res 2011a;39:9433-47.
88. Le TB, Stevenson CE, Fiedler HP et al. Structures of the TetRlike simocyclinone efflux pump repressor, SimR, and the mechanism of ligand-mediated derepression. J Mol Biol 2011b;408:40-56.
89. Lee JH, Lee J. Indole as an intercellular signal in microbial communities. FEMS Microbiol Rev 2010;34:426-44.
90. Lee YJ, Kitani S, Kinoshita H et al. Identification by gene deletion analysis of barS2, a gene involved in the biosynthesis of γ-butyrolactone autoregulator in Streptomyces virginiae. Arch Microbiol 2008;189:367-74.
91. Lee YJ, Kitani S, Nihira T. Null mutation analysis of an afsAfamily gene, barX, that is involved in biosynthesis of the γ-butyrolactone autoregulator in Streptomyces virginiae. Microbiology 2010;156:206-10.
92. Leung K, Zahn H, Leaver T et al. A programmable droplet-based microfluidic device applied to multiparameter analysis of single microbes and microbial communities. P Natl Acad Sci USA 2012;109:7665-70.
93. Li Q,Wang L, Xie Y et al. SsaA, a member of a novel class of transcriptional regulators, controls sansanmycin production in Streptomyces sp. strain SS through a feedback mechanism. J Bacteriol 2013;195:2232-43.
94. Li W, Liu G, Tan H. Disruption of sabR affects nikkomycin biosynthesis and morphogenesis in Streptomyces ansochromogenes. Biotechnol Lett 2003;25:1491-7.
95. Li X, Yu T, He Q et al. Binding of a biosynthetic intermediate to AtrA modulates the production of lidamycin by Streptomyces globisporus. Mol Microbiol 2015;96:1257-71.
96. Linares JF, Gustafsson I, Baquero F et al. Antibiotics as intermicrobial signaling agents instead of weapons. P Natl Acad Sci USA 2006;103:19484-9.
97. Liu G, Chater KF, Chandra G et al. Molecular regulation of antibiotic biosynthesis in Streptomyces. Microbiol Mol Biol R 2013;77:112-43.
98. Liu W, Zhang Q, Guo J et al. Increasing avermectin production in Streptomyces avermitilis by manipulating the expression of a novel TetR-family regulator and its target gene product. Appl Environ Microb 2015;81:5157-73.
99. McCormick JR, Fl Ärdh K. Signals and regulators that govern Streptomyces development. FEMS Microbiol Rev 2012;36:206-31.
100. McHardy AC, Rigoutsos I. What's in the mix: phylogenetic classification of metagenome sequence samples. Curr Opin Microbiol 2007;10:499-503.
101. Mao XM, Luo S, Zhou RC et al. Transcriptional regulation of the daptomycin gene cluster in Streptomyces roseosporus by an autoregulator, AtrA. J Biol Chem 2015;290:7992-8001.
102. Martín J, Liras P. Cascades and networks of regulatory genes that control antibiotic biosynthesis. In: Wang X, Chen J, Quinn P (eds). Reprogramming Microbial Metabolic Pathways. Berlin: Springer, 2012, 115-38.
103. Martin JF, Liras P. Engineering of regulatory cascades and networks controlling antibiotic biosynthesis in Streptomyces. Curr Opin Microbiol 2010;13:263-73.
104. Mast Y, Guezguez J, Handel F et al. A complex signaling cascade governs pristinamycin biosynthesis in Streptomyces pristinaespiralis. Appl Environ Microb 2015;81:6621-36.
105. Matselyukh B, Mohammadipanah F, Laatsch H et al. Nmethylphenylalanyl-dehydrobutyrine diketopiperazine, an A-factor mimic that restores antibiotic biosynthesis and morphogenesis in Streptomyces globisporus 1912-B2 and Streptomyces griseus 1439. J Antibiot 2015;68:9-14.
106. Medema MH, Fischbach MA. Computational approaches to natural product discovery. Nat Chem Biol 2015;11:639-48.
107. Mehra S, Charaniya S, Takano E et al. A bistable gene switch for antibiotic biosynthesis: the butyrolactone regulon in Streptomyces coelicolor. PLoS One 2008;3:e2724.
108. Miller MB, Bassler BL. Quorum sensing in bacteria. Annu Rev Microbiol 2001;55:165-99.
109. Musat N, Halm H, Winterholler B et al. A single-cell view on the ecophysiology of anaerobic phototrophic bacteria. P Natl Acad Sci USA 2008;105:17861-6.
110. Namwat W, Lee CK, Kinoshita H et al. Identification of the varR gene as a transcriptional regulator of virginiamycin S resistance in Streptomyces virginiae. J Bacteriol 2001;183:2025-31.
111. Natsume R, Ohnishi Y, Senda T et al. Crystal structure of a γ-butyrolactone autoregulator receptor protein in Streptomyces coelicolor A3(2). J Mol Biol 2004;336:409-19.
112. Nett M, Ikeda H, Moore BS. Genomic basis for natural product biosynthetic diversity in the actinomycetes. Nat Prod Rep 2009;26:1362-84.
113. Ng WL, Bassler BL. Bacterial quorum-sensing network architectures. Annu Rev Genet 2009;43:197-222.
114. Nutzmann HW, Reyes-Dominguez Y, Scherlach K et al. Bacteriainduced natural product formation in the fungus Aspergillus nidulans requires Saga/Ada-mediated histone acetylation. P Natl Acad Sci USA 2011;108:14282-7.
115. O'Brien J, Wright GD. An ecological perspective ofmicrobial secondary metabolism. Curr Opin Biotechnol 2011;22:552-8.
116. Onaka H, Horinouchi S. DNA-binding activity of the A-factor receptor protein and its recognition DNA sequences. MolMicrobiol 1997;24:991-1000.
117. Onaka H, Mori Y, Igarashi Y et al. Mycolic acid-containing bacteria induce natural-product biosynthesis in Streptomyces species. Appl Environ Microb 2011;77:400-6.
118. Onaka H, Nakagawa T, Horinouchi S. Involvement of two Afactor receptor homologues in Streptomyces coelicolor A3(2) in the regulation of secondary metabolism andmorphogenesis. Mol Microbiol 1998;28:743-53.
119. Onaka H, Sugiyama M, Horinouchi S. A mutation at proline-115 in the A-factor receptor protein of Streptomyces griseus abolishes DNA-binding ability but not ligand-binding ability. J Bacteriol 1997;179:2748-52.
120. Onaka H, Tabata H, Igarashi Y et al. Goadsporin, a chemical substance which promotes secondary metabolism andmorphogenesis in streptomycetes. I. Purification and characterization. J Antibiot 2001;54:1036-44.
121. O'Rourke S,Wietzorrek A, Fowler K et al. Extracellular signalling, translational control, two repressors and an activator all contribute to the regulation of methylenomycin production in Streptomyces coelicolor. Mol Microbiol 2009;71:763-78.
122. Orphan VJ, House CH, Hinrichs KU et al. Methane-consuming archaea revealed by directly coupled isotopic and phylogenetic analysis. Science 2001;293:484-7.
123. Perez J, Munoz-Dorado J, Brana AF et al. Myxococcus xanthus induces actinorhodin overproduction and aerialmycelium formation by Streptomyces coelicolor. Microb Biotechnol 2011;4:175-83.
124. Ramos JL, Martinez-Bueno M, Molina-Henares AJ et al. The TetR family of transcriptional repressors. Microbiol Mol Biol R 2005;69:326-56.
125. Recio E, Aparicio JF, Rumbero A et al. Glycerol, ethylene glycol and propanediol elicit pimaricin biosynthesis in the PI-factor-defective strain Streptomyces natalensis npi287 and increase polyene production in several wild-type actinomycetes. Microbiology 2006;152:3147-56.
126. Recio E, Colinas A, Rumbero A et al. PI factor, a novel type quorum-sensing inducer elicits pimaricin production in Streptomyces natalensis. J Biol Chem 2004;279:41586-93.
127. Robertson AW, Forget SM, Martinez-Farina CF et al. JadX is a disparate natural product binding protein. J Am Chem Soc 2016;138:2200-8.
128. Romero D, Traxler MF, López D et al. Antibiotics as signal molecules. Chem Rev 2011;111:5492-505.
129. Rutledge PJ, Challis GL. Discovery of microbial natural products by activation of silent biosynthetic gene clusters. Nat Rev Microbiol 2015;13:509-23.
130. Salehi-Najafabadi Z, Barreiro C, Martinez-Castro M et al. Characterisation of a γ-butyrolactone receptor of Streptomyces tacrolimicus: effect on sporulation and tacrolimus biosynthesis. Appl Microbiol Biot 2011;92:971-84.
131. Sato K, Nihira T, Sakuda S et al. Isolation and structure of a new butyrolactone autoregulator from Streptomyces sp. FRI-5. J Biosci Bioeng 1989;68:170-3.
132. Schaberle TF, Orland A, Konig GM. Enhanced production of undecylprodigiosin in Streptomyces coelicolor by co-cultivation with the corallopyronin A-producing myxobacterium, Corallococcus coralloides. Biotechnol Lett 2014;36:641-8.
133. Schlimpert S, Fl Ärdh K, Buttner M. Fluorescence time-lapse imaging of the complete S. venezuelae life cycle using a microfluidic device. J Vis Exp 2016;108:e53863.
134. Schroeckh V, Scherlach K, Nutzmann HW et al. Intimate bacterial-fungal interaction triggers biosynthesis of archetypal polyketides in Aspergillus nidulans. P Natl Acad Sci USA 2009;106:14558-63.
135. Schumacher MA, Miller MC, Grkovic S et al. Structural basis for cooperative DNA binding by two dimers of the multidrugbinding protein QacR. EMBO J 2002;21:1210-8.
136. Seipke RF, Kaltenpoth M, Hutchings MI. Streptomyces as symbionts: an emerging and widespread theme? FEMS Microbiol Rev 2012;36:862-76.
137. Sengupta S, Chattopadhyay MK, Grossart HP. The multifaceted roles of antibiotics and antibiotic resistance in nature. Front Microbiol 2013;4:47.
138. Seyedsayamdost MR. High-throughput platform for the discovery of elicitors of silent bacterial gene clusters. P Natl Acad Sci USA 2014;111:7266-71.
139. Sherwood EJ, Bibb MJ. The antibiotic planosporicin coordinates its own production in the actinomycete Planomonospora alba. P Natl Acad Sci USA 2013;110:E2500-9.
140. Shikura N, Yamamura J, Nihira T. barS1, a gene for biosynthesis of a gamma-butyrolactone autoregulator, a microbial signaling molecule eliciting antibiotic production in Streptomyces species. J Bacteriol 2002;184:5151-7.
141. Sidda JD, Corre C. Gamma-butyrolactone and furan signaling systems in Streptomyces. Methods Enzymol 2012;517:71-87.
142. Sidda JD, Song LJ, Poon V et al. Discovery of a family of ? -aminobutyrate ureas via rational derepression of a silent bacterial gene cluster. Chem Sci 2014;5:86-89.
143. Straight PD, Fischbach MA, Walsh CT et al. A singular enzymatic megacomplex fromBacillus subtilis. P Natl Acad Sci USA 2007;104:305-10.
144. Straight PD, Willey JM, Kolter R. Interactions between Streptomyces coelicolor and Bacillus subtilis: Role of surfactants in raising aerial structures. J Bacteriol 2006;188:4918-25.
145. Sugiyama M, Onaka H, Nakagawa T et al. Site-directed mutagenesis of the A-factor receptor protein: Val-41 important for DNA-binding and Trp-119 important for ligand-binding. Gene 1998;222:133-44.
146. Tahlan K, Ahn SK, Sing A et al. Initiation of actinorhodin export in Streptomyces coelicolor. Mol Microbiol 2007;63:951-61.
147. Tahlan K, Yu Z, Xu Y et al. Ligand recognition by ActR, a TetR-like regulator of actinorhodin export. J Mol Biol 2008;383:753-61.
148. Takano E. γ-butyrolactones: Streptomyces signalling molecules regulating antibiotic production and differentiation. Curr Opin Microbiol 2006;9:287-94.
149. Takano E, Chakraburtty R, Nihira T et al. A complex role for the γ-butyrolactone SCB1 in regulating antibiotic production in Streptomyces coelicolor A3(2). Mol Microbiol 2001;41:1015-28.
150. Takano E, Kinoshita H, Mersinias V et al. A bacterial hormone (the SCB1) directly controls the expression of a pathwayspecific regulatory gene in the cryptic type I polyketide biosynthetic gene cluster of Streptomyces coelicolor. Mol Microbiol 2005;56:465-79.
151. Takano E, Nihira T, Hara Y et al. Purification and structural determination of SCB1, a γ-butyrolactone that elicits antibiotic production in Streptomyces coelicolor A3(2). J Biol Chem 2000;275:11010-6.
152. Tan GY, Bai L, Zhong JJ. Exogenous 1,4-butyrolactone stimulates A-factor-like cascade and validamycin biosynthesis in Streptomyces hygroscopicus 5008. Biotechnol Bioeng 2013;110:2984-93.
153. Tan GY, Peng Y, Lu C et al. Engineering validamycin production by tandem deletion of γ-butyrolactone receptor genes in Streptomyces hygroscopicus 5008. Metab Eng 2015;28:74-81.
154. Tomono A, Tsai Y, Yamazaki H et al. Transcriptional control by Afactor of strR, the pathway-specific transcriptional activator for streptomycin biosynthesis in Streptomyces griseus. J Bacteriol 2005;187:5595-604.
155. Traxler MF, Kolter R. Natural products in soil microbe interactions and evolution. Nat Prod Rep 2015;32:956-70.
156. TraxlerMF, Seyedsayamdost MR, Clardy J et al. Interspecies modulation of bacterial development through iron competition and siderophore piracy. Mol Microbiol 2012;86:628-44.
157. Traxler MF, Watrous JD, Alexandrov T et al. Interspecies interactions stimulate diversification of the Streptomyces coelicolor secreted metabolome. MBio 2013;4:e00459-13.
158. Tschowri N, Schumacher MA, Schlimpert S et al. Tetrameric cdi-GMP mediates effective transcription factor dimerization to control Streptomyces development. Cell 2014;158:1136-47.
159. Tsui WH, Yim G, Wang HH et al. Dual effects of MLS antibiotics: transcriptional modulation and interactions on the ribosome. Chem Biol 2004;11:1307-16.
160. van Wezel GP, McDowall KJ. The regulation of the secondary metabolism of Streptomyces: new links and experimental advances. Nat Prod Rep 2011;28:1311-33.
161. Vanwonterghem I, Jensen PD, Ho DP et al. Linkingmicrobial community structure, interactions and function in anaerobic digesters using new molecular techniques. Curr Opin Biotechnol 2014;27:55-64.
162. Vargas-Bautista C, Rahlwes K, Straight P. Bacterial competition reveals differential regulation of the pks genes by Bacillus subtilis. J Bacteriol 2014;196:717-28.
163. Vetsigian K, Jajoo R, Kishony R. Structure and evolution of Streptomyces interaction networks in soil and in silico. PLoS Biol 2011;9:e1001184.
164. Wang J, Wang W, Wang L et al. A novel role of 'pseudo'γ-butyrolactone receptors in controlling γ-butyrolactone biosynthesis in Streptomyces. Mol Microbiol 2011;82:236-50.
165. Wang L, Tian X,Wang J et al. Autoregulation of antibiotic biosynthesis by binding of the end product to an atypical response regulator. P Natl Acad Sci USA 2009;106:8617-22.
166. Wang W, Ji J, Li X et al. Angucyclines as signals modulate the behaviors of Streptomyces coelicolor. P Natl Acad Sci USA 2014;111:5688-93.
167. Waters CM, Bassler BL. Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Bi 2005;21:319-46.
168. Watrous J, Roach P, Heath B et al. Metabolic profiling directly from the petri dish using nanospray desorption electrospray ionization imaging mass spectrometry. Anal Chem 2013;85:10385-91.
169. Watrous JD, Dorrestein PC. Imaging mass spectrometry in microbiology. Nat Rev Microbiol 2011;9:683-94.
170. Wietzorrek A, Bibb M. A novel family of proteins that regulates antibiotic production in streptomycetes appears to contain an OmpR-like DNA-binding fold. Mol Microbiol 1997;25:1181-4.
171. Willems AR, Tahlan K, Taguchi T et al. Crystal structures of the Streptomyces coelicolor TetR-like protein ActR alone and in complex with actinorhodin or the actinorhodin biosynthetic precursor (S)-DNPA. J Mol Biol 2008;376:1377-87.
172. Willey JM, Gaskell AA. Morphogenetic signalingmolecules of the streptomycetes. Chem Rev 2011;111:174-87.
173. Wu C, Zacchetti B, Ram AF et al. Expanding the chemical space for natural products by Aspergillus-Streptomyces cocultivation and biotransformation. Sci Rep 2015;5:10868.
174. Xu G, Wang J, Wang L et al. 'Pseudo' γ-butyrolactone receptors respond to antibiotic signals to coordinate antibiotic biosynthesis. J Biol Chem 2010;285:27440-8.
175. Xu Y, Willems A, Au-Yeung C et al. A two-step mechanism for the activation of actinorhodin export and resistance in Streptomyces coelicolor. MBio 2012;3:e00191-12.
176. Yamada Y, Sugamura K, Kondo K et al. The structure of inducing factors for virginiamycin production in Streptomyces virginiae. J Antibiot 1987;40:496-504.
177. Yamazaki H, Tomono A, Ohnishi Y et al. DNA-binding specificity of AdpA, a transcriptional activator in the A-factor regulatory cascade in Streptomyces griseus. Mol Microbiol 2004;53:555-72.
178. Yang YH, Song E, Kim JN et al. Characterization of a new ScbRlike γ-butyrolactone binding regulator (SlbR) in Streptomyces coelicolor. Appl Microbiol Biot 2012;96:113-21.
179. Yang YL, Xu Y, Straight P et al. Translating metabolic exchange with imaging mass spectrometry. Nat Chem Biol 2009;5:885-7.
180. YimG,McClure J, Surette MG et al. Modulation of Salmonella gene expression by subinhibitory concentrations of quinolones. J Antibiot 2011;64:73-8.
181. Yim G, Wang HH, Davies J. Antibiotics as signalling molecules. Philos T Roy Soc B 2007;362:1195-200.
182. Zhang J, Jiang Y, Cao Y et al. Violapyrones A-G, alpha-pyrone derivatives from Streptomyces violascens isolated from Hylobates hoolock feces. J Nat Prod 2013a;76:2126-30.
183. Zhang Y, Pan G, Zou Z et al. JadR*-mediated feed-forward regulation of cofactor supply in jadomycin biosynthesis. Mol Microbiol 2013b;90:884-97.
184. Zhou ZX, Xu QQ, Bu QT et al. Transcriptome-guided identification of SprA as a pleiotropic regulator in Streptomyces chattanoogensis. Appl Microbiol Biotechnol 2015;99:1287-98.
185. Zhu D, Wang Y, Zhang M et al. Product-mediated regulation of pentalenolactone biosynthesis in Streptomyces species by the MarR/SlyA family activators PenR and PntR. J Bacteriol 2013;195:1255-66.
186. Zhu H, Sandiford SK, van Wezel GP. Triggers and cues that activate antibiotic production by actinomycetes. J Ind Microbiol Biot 2014;41:371-86.
187. Zou Z, Du D, Zhang Y et al. A γ-butyrolactone-sensing activator/ repressor, JadR3, controls a regulatory mini-network for jadomycin biosynthesis. Mol Microbiol 2014;94:490-505.