Recent advances in understanding streptomyces

F1000Research

Volumn 5, Issue , 2016, Pages

  Chater, Keith F ^a  

^a JOHN INNES CENTRE   (United Kingdom)

Author keywords

Genomics; Pathogenic streptomyces; Streptomyces; Streptomyces ecology; Streptomyces evolution

Indexed keywords

GLYCAN; GUANOSINE PHOSPHATE; NITRIC OXIDE;

BACTERIAL CELL WALL; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL STRAIN; BACTERIAL STRUCTURES; BACTERIUM COLONY; BACTERIUM EXAMINATION; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; CYTOPLASM; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC CONSERVATION; GENETIC TRANSCRIPTION; MOLECULAR ECOLOGY; MOLECULAR EVOLUTION; MOLECULAR INTERACTION; NEXT GENERATION SEQUENCING; NONHUMAN; OXIDATION REDUCTION STATE; PATHOGENICITY; PLANT PATHOGEN INTERACTION; PROTEIN DEGRADATION; PROTEIN METABOLISM; REGULATORY MECHANISM; REVIEW; SOIL ORGANISM; SPECIES COMPARISON; SPORE GERMINATION; STREPTOMYCES; STREPTOMYCES COELICOLOR; STREPTOMYCES VENEZUELAE; STRESS;

EID: 85007569560     PISSN: 20461402     EISSN: 1759796X     Source Type: Journal    
DOI: 10.12688/f1000research.9534.1     Document Type: Review

References (139)

1. Charlop-Powers Z Owen JG Reddy BV: Chemical-biogeographic survey of secondary metabolism in soil. Proc Natl Acad Sci U S A. 2014;111(10):3757-62. 24550451 10.1073/pnas.1318021111 3956145
2. Charlop-Powers Z Owen JG Reddy BV: Global biogeographic sampling of bacterial secondary metabolism. eLife. 2015;4:e05048. 25599565 10.7554/eLife.05048 4383359
3. Hopwood DA: Streptomyces in Nature and Medicine: The Antibiotic Makers. Oxford University Press, New York, NY.2007. 10.1093/jhmas/jrn016
4. Chater KF Bir S Lee KJ: The complex extracellular biology of Streptomyces. FEMS Microbiol Rev. 2010;34(2):171-98. 20088961 10.1111/j.1574-6976.2009.00206.x
5. Wibberg D Al-Dilaimi A Busche T: Complete genome sequence of Streptomyces reticuli, an efficient degrader of crystalline cellulose. J Biotechnol. 2016;222:13-4. 26851387 10.1016/j.jbiotec.2016.02.002
6. Lim JH Lee CR Dhakshnamoorthy V: Molecular characterization of Streptomyces coelicolor A(3) SCO6548 as a cellulose 1,4-cellobiosidase. FEMS Microbiol Lett. 2016;363(3): pii: fnv245. 26712534 10.1093/femsle/fnv245
7. Book AJ Lewin GR McDonald BR: Evolution of High Cellulolytic Activity in Symbiotic Streptomyces through Selection of Expanded Gene Content and Coordinated Gene Expression. PLoS Biol. 2016;14(6):e1002475. 27276034 10.1371/journal.pbio.1002475 4898821
8. Barka EA Vatsa P Sanchez L: Taxonomy, Physiology, and Natural Products of Actinobacteria. Microbiol Mol Biol Rev. 2015;80(1):1-43. 26609051 10.1128/MMBR.00019-15 4711186
9. Tenconi E Urem M Witek-Połatynska MA: Multiple allosteric effectors control the affinity of DasR for its target sites. Biochem Biophys Res Commun. 2015;464(1):324-9. 26123391 10.1016/j.bbrc.2015.06.152
10. witek-Połatynska MA Bucca G Laing E: Genome-wide analysis of in vivo binding of the master regulator DasR in Streptomyces coelicolor identifies novel non-canonical targets. PLoS One. 2015;10(4):e0122479. 25875084 10.1371/journal.pone.0122479 4398421
11. Viens P Dubeau MP Kimura A: Uptake of chitosan-derived D-glucosamine oligosaccharides in Streptomyces coelicolor A3(2). FEMS Microbiol Lett. 2015;362(9): pii: fnv048. 25837815 10.1093/femsle/fnv048
12. Seipke RF Kaltenpoth M Hutchings MI: Streptomyces as symbionts: an emerging and widespread theme? FEMS Microbiol Rev. 2012;36(4):862-76. 22091965 10.1111/j.1574-6976.2011.00313.x
13. Viaene T Langendries S Beirinckx S: Streptomyces as a plant's best friend? FEMS Microbiol Ecol. 2016;92(8): pii: fiw119. 27279415 10.1093/femsec/fiw119
14. Liu M Abdel-Mageed WM Ren B: Endophytic Streptomyces sp. Y3111 from traditional Chinese medicine produced antitubercular pluramycins. Appl Microbiol Biotechnol. 2014;98(3):1077-85. 24190497 10.1007/s00253-013-5335-6
15. Yang X Yang Y Peng T: A new cyclopeptide from endophytic Streptomyces sp. YIM 64018. Nat Prod Commun. 2013;8(12):1753-4. 24555291
16. Conti R Chagas FO Caraballo-Rodriguez AM: Endophytic Actinobacteria from the Brazilian Medicinal Plant Lychnophora ericoides Mart. and the Biological Potential of Their Secondary Metabolites. Chem Biodivers. 2016;13(6):727-36. 27128202 10.1002/cbdv.201500225
17. Chen X Pizzatti C Bonaldi M: Biological Control of Lettuce Drop and Host Plant Colonization by Rhizospheric and Endophytic Streptomycetes. Front Microbiol. 2016;7:714. 27242735 10.3389/fmicb.2016.00714 4874062
18. Zloch M Thiem D Gadzala-Kopciuch R: Synthesis of siderophores by plant-associated metallotolerant bacteria under exposure to Cd 2+. Chemosphere. 2016;156:312-25. 27183333 10.1016/j.chemosphere.2016.04.130
19. Miao GP Zhu CS Feng JT: Effects of plant stress signal molecules on the production of wilforgine in an endophytic actinomycete isolated from Tripterygium wilfordii Hook.f. Curr Microbiol. 2015;70(4):571-9. 25523369 10.1007/s00284-014-0758-6
20. Shi Y Zhang X Lou K: Isolation, characterization, and insecticidal activity of an endophyte of drunken horse grass, Achnatherum inebrians. J Insect Sci. 2013;13(1):151. 24784492 10.1673/031.013.15101 4018183
21. Singh SP Gaur R: Evaluation of antagonistic and plant growth promoting activities of chitinolytic endophytic actinomycetes associated with medicinal plants against Sclerotium rolfsii in chickpea. J Appl Microbiol. 2016;121(2):506-18. 27170067 10.1111/jam.13176
22. Wang W Zhai Y Cao L: Illumina-based analysis of core actinobacteriome in roots, stems, and grains of rice. Microbiol Res. 2016;190:12-8. 27393994 10.1016/j.micres.2016.05.003
23. Passari AK Chandra P Zothanpuia: Detection of biosynthetic gene and phytohormone production by endophytic actinobacteria associated with Solanum lycopersicum and their plant-growth-promoting effect. Res Microbiol. 2016;167(8):692-705. 27421813 10.1016/j.resmic.2016.07.001
24. Mukasheva T Berzhanova R Ignatova L: Bacterial endophytes of Trans-Ili Alatau region's plants as promising components of a microbial preparation for agricultural use. Acta Biochim Pol. 2016;63(2):321-8. 27028415 10.18388/abp.2015_1157
25. Tchinda RA Boudjeko T Simao-Beaunoir AM: Morphological, Physiological, and Taxonomic Characterization of Actinobacterial Isolates Living as Endophytes of Cacao Pods and Cacao Seeds. Microbes Environ. 2016;31(1):56-62. 26947442 10.1264/jsme2.ME15146 4791117
26. Peng SM Wang BL Xu JZ: [Effect of different treatment on endophytic bacterial communities in continuous cropping of Chrysanthemum morifoliu]. Zhongguo Zhong Yao Za Zhi. 2014;39(24):4763-8. 25898574
27. Andam CP Doroghazi JR Campbell AN: A Latitudinal Diversity Gradient in Terrestrial Bacteria of the Genus Streptomyces. MBio. 2016;7(2):e02200-15. 27073097 10.1128/mBio.02200-15 4817263
28. Martiny JB: History Leaves Its Mark on Soil Bacterial Diversity. MBio. 2016;7(3): pii: e00784-16. 27273826 10.1128/mBio.00784-16 4959671
29. Kurth F Mailnder S Bnn M: Streptomyces-induced resistance against oak powdery mildew involves host plant responses in defense, photosynthesis, and secondary metabolism pathways. Mol Plant Microbe Interact. 2014;27(9):891-900. 24779643 10.1094/MPMI-10-13-0296-R
30. Hanshew AS McDonald BR Daz Daz C: Characterization of actinobacteria associated with three ant-plant mutualisms. Microb Ecol. 2015;69(1):192-203. 25096989 10.1007/s00248-014-0469-3
31. Kaltenpoth M Roeser-Mueller K Koehler S: Partner choice and fidelity stabilize coevolution in a Cretaceous-age defensive symbiosis. Proc Natl Acad Sci U S A. 2014;111(17):6359-64. 24733936 10.1073/pnas.1400457111 4035988
32. Kumbhar C Mudliar P Bhatia L: Widespread predatory abilities in the genus Streptomyces. Arch Microbiol. 2014;196(4):235-48. 24535490 10.1007/s00203-014-0961-7
33. Ian E Malko DB Sekurova ON: Genomics of sponge-associated Streptomyces spp. closely related to Streptomyces albus J1074: insights into marine adaptation and secondary metabolite biosynthesis potential. PLoS One. 2014;9(5):e96719. 24819608 10.1371/journal.pone.0096719 4018334
34. Huguet-Tapia JC Bignell DR Loria R: Characterization of the integration and modular excision of the integrative conjugative element PAISt in Streptomyces turgidiscabies Car8. PLoS One. 2014;9(6):e99345. 24927117 10.1371/journal.pone.0099345 4057263
35. Chapleau M Guertin JF Farrokhi A: Identification of genetic and environmental factors stimulating excision from Streptomyces scabiei chromosome of the toxicogenic region responsible for pathogenicity. Mol Plant Pathol. 2016;17(4):501-9. 26177341 10.1111/mpp.12296
36. Francis IM Jourdan S Fanara S: The cellobiose sensor CebR is the gatekeeper of Streptomyces scabies pathogenicity. MBio. 2015;6(2):e02018. 25714708 10.1128/mBio.02018-14 4358012
37. Cheng Z Bown L Tahlan K: Regulation of coronafacoyl phytotoxin production by the PAS-LuxR family regulator CfaR in the common scab pathogen Streptomyces scabies. PLoS One. 2015;10(3):e0122450. 25826255 10.1371/journal.pone.0122450 4380410
38. Bignell DR Francis IM Fyans JK: Thaxtomin A production and virulence are controlled by several bld gene global regulators in Streptomyces scabies. Mol Plant Microbe Interact. 2014;27(8):875-85. 24678834 10.1094/MPMI-02-14-0037-R
39. Padilla-Reynaud R Simao-Beaunoir AM Lerat S: Suberin Regulates the Production of Cellulolytic Enzymes in Streptomyces scabiei, the Causal Agent of Potato Common Scab. Microbes Environ. 2015;30(3):245-53. 26330095 10.1264/jsme2.ME15034 4567563
40. Huguet-Tapia JC Lefebure T Badger JH: Genome Content and Phylogenomics Reveal both Ancestral and Lateral Evolutionary Pathways in Plant-Pathogenic Streptomyces Species. Appl Environ Microbiol. 2016;82(7):2146-55. 26826232 10.1128/AEM.03504-15 4807529
41. Studholme DJ: Genome Update. Let the consumer beware: Streptomyces genome sequence quality. Microb Biotechnol. 2016;9(1):3-7. 26986204 10.1111/1751-7915.12344 4720414
42. Kim J Kim Y Jeong Y: Comparative Genomics Reveals the Core and Accessory Genomes of Streptomyces Species. J Microbiol Biotechnol. 2015;25(10):1599-605. 26032364 10.4014/jmb.1504.04008
43. Doroghazi JR Buckley DH: Widespread homologous recombination within and between Streptomyces species. ISME J. 2010;4(9):1136-43. 20393569 10.1038/ismej.2010.45
44. Cheng K Rong X Huang Y: Widespread interspecies homologous recombination reveals reticulate evolution within the genus Streptomyces. Mol Phylogenet Evol. 2016;102:246-54. 27329941 10.1016/j.ympev.2016.06.004
45. Thoma L Muth G: The conjugative DNA-transfer apparatus of Streptomyces. Int J Med Microbiol. 2015;305(2):224-9. 25592263 10.1016/j.ijmm.2014.12.020
46. Thoma L Vollmer B Muth G: Fluorescence microscopy of Streptomyces conjugation suggests DNA-transfer at the lateral walls and reveals the spreading of the plasmid in the recipient mycelium. Environ Microbiol. 2016;18(2):598-608. 26286483 10.1111/1462-2920.13027
47. Seipke RF: Strain-level diversity of secondary metabolism in Streptomyces albus. PLoS One. 2015;10(1):e0116457. 25635820 10.1371/journal.pone.0116457 4312078
48. Sexton DL St-Onge RJ Haiser HJ: Resuscitation-promoting factors are cell wall-lytic enzymes with important roles in the germination and growth of Streptomyces coelicolor. J Bacteriol. 2015;197(5):848-60. 25512314 10.1128/JB.02464-14 4325095
49. St-Onge RJ Haiser HJ Yousef MR: Nucleotide second messenger-mediated regulation of a muralytic enzyme in Streptomyces. Mol Microbiol. 2015;96(4):779-95. 25682701 10.1111/mmi.12971
50. Flardh K Richards DM Hempel AM: Regulation of apical growth and hyphal branching in Streptomyces. Curr Opin Microbiol. 2012;15(6):737-43. 23153774 10.1016/j.mib.2012.10.012
51. Chandra G Chater KF: Developmental biology of Streptomyces from the perspective of 100 actinobacterial genome sequences. FEMS Microbiol Rev. 2014;38(3):345-79. 24164321 10.1111/1574-6976.12047 4255298
52. Chaplin AK Petrus ML Mangiameli G: GlxA is a new structural member of the radical copper oxidase family and is required for glycan deposition at hyphal tips and morphogenesis of Streptomyces lividans. Biochem J. 2015;469(3):433-44. 26205496 10.1042/BJ20150190
53. Liman R Facey PD van Keulen G: A laterally acquired galactose oxidase-like gene is required for aerial development during osmotic stress in Streptomyces coelicolor. PLoS One. 2013;8(1):e54112. 23326581 10.1371/journal.pone.0054112 3543389
54. van Dissel D Claessen D Roth M: A novel locus for mycelial aggregation forms a gateway to improved Streptomyces cell factories. Microb Cell Fact. 2015;14:44. 25889360 10.1186/s12934-015-0224-6 4391728
55. Zacchetti B Willemse J Recter B: Aggregation of germlings is a major contributing factor towards mycelial heterogeneity of Streptomyces. Sci Rep. 2016;6: 27045. 27244565 10.1038/srep27045 4886682
56. Yage P Lopez-Garcia MT Rioseras B: New insights on the development of Streptomyces and their relationships with secondary metabolite production. Curr Trends Microbiol. 2012;8:65-73. 24707121 3972883
57. Celler K Koning RI Willemse J: Cross-membranes orchestrate compartmentalization and morphogenesis in Streptomyces. Nat Commun. 2016;7: ncomms11836. 27291257 10.1038/ncomms11836 4909990
58. Yage P Willemse J Koning RI: Subcompartmentalization by cross-membranes during early growth of Streptomyces hyphae. Nat Commun. 2016;7: 12467. 27514833 10.1038/ncomms12467 4990651
59. Mingyar E Sevcikova B Rezuchova B: The F-specific anti-sigma factor RsfA is one of the protein kinases that phosphorylates the pleiotropic anti-anti-sigma factor BldG in Streptomyces coelicolor A3(2). Gene. 2014;538(2):280-7. 24462756 10.1016/j.gene.2014.01.041
60. Hindra Moody MJ Jones SE: Complex intra-operonic dynamics mediated by a small RNA in Streptomyces coelicolor. PLoS One. 2014;9(1):e85856. 24465751 10.1371/journal.pone.0085856 3896431
61. Maupin-Furlow JA: Prokaryotic ubiquitin-like protein modification. Annu Rev Microbiol. 2014;68:155-75. 24995873 10.1146/annurev-micro-091313-103447 4757901
62. Boubakri H Seghezzi N Duchateau M: The Absence of Pupylation (Prokaryotic Ubiquitin-Like Protein Modification) Affects Morphological and Physiological Differentiation in Streptomyces coelicolor. J Bacteriol. 2015;197(21):3388-99. 26283768 10.1128/JB.00591-15 4621069
63. Compton CL Fernandopulle MS Nagari RT: Genetic and Proteomic Analyses of Pupylation in Streptomyces coelicolor. J Bacteriol. 2015;197(17):2747-53. 26031910 10.1128/JB.00302-15 4524032
64. Mao XM Ren NN Sun N: Proteasome involvement in a complex cascade mediating SigT degradation during differentiation of Streptomyces coelicolor. FEBS Lett. 2014;588(4):608-13. 24440356 10.1016/j.febslet.2013.12.029
65. Niu G Chater KF Tian Y: Specialised metabolites regulating antibiotic biosynthesis in Streptomyces spp. FEMS Microbiol Rev. 2016;40(4):554-73. 27288284 10.1093/femsre/fuw012
66. Zou Z Du D Zhang Y: A butyrolactone-sensing activator/repressor, JadR3, controls a regulatory mini-network for jadomycin biosynthesis. Mol Microbiol. 2014;94(3):490-505. 25116816 10.1111/mmi.12752
67. Nodwell JR: Are you talking to me? A possible role for butyrolactones in interspecies signalling. Mol Microbiol. 2014;94(3):483-5. 25200025 10.1111/mmi.12787
68. Schlimpert S Flrdh K Buttner M: Fluorescence Time-lapse Imaging of the Complete S. venezuelae Life Cycle Using a Microfluidic Device. J Vis Exp. 2016; (108):53863. 26967231 10.3791/53863 4828195
69. Donczew M Mackiewicz P Wrbel A: ParA and ParB coordinate chromosome segregation with cell elongation and division during Streptomyces sporulation. Open Biol. 2016;6(4):150263. 27248800 10.1098/rsob.150263 4852455
70. Al-Bassam MM Bibb MJ Bush MJ: Response regulator heterodimer formation controls a key stage in Streptomyces development. PLoS Genet. 2014;10(8):e1004554. 25101778 10.1371/journal.pgen.1004554 4125116
71. Bush MJ Chandra G Bibb MJ: Genome-Wide Chromatin Immunoprecipitation Sequencing Analysis Shows that WhiB Is a Transcription Factor That Cocontrols Its Regulon with WhiA To Initiate Developmental Cell Division in Streptomyces. MBio. 2016;7(2):e00523-16. 27094333 10.1128/mBio.00523-16 4850268
72. Bush MJ Tschowri N Schlimpert S: c-di-GMP signalling and the regulation of developmental transitions in streptomycetes. Nat Rev Microbiol. 2015;13(12):749-60. 26499894 10.1038/nrmicro3546
73. Tschowri N Schumacher MA Schlimpert S: Tetrameric c-di-GMP mediates effective transcription factor dimerization to control Streptomyces development. Cell. 2014;158(5):1136-47. 25171413 10.1016/j.cell.2014.07.022 4151990
74. Tran NT Den Hengst CD Gomez-Escribano JP: Identification and characterization of CdgB, a diguanylate cyclase involved in developmental processes in Streptomyces coelicolor. J Bacteriol. 2011;193(12):3100-8. 21515767 10.1128/JB.01460-10 3133206
75. Tschowri N: Cyclic Dinucleotide-Controlled Regulatory Pathways in Streptomyces Species. J Bacteriol. 2016;198(1):47-54. 26216850 10.1128/JB.00423-15 4686203
76. Kelemen GH Brown GL Kormanec J: The positions of the sigma-factor genes, whiG and sigF, in the hierarchy controlling the development of spore chains in the aerial hyphae of Streptomyces coelicolor A3(2). Mol Microbiol. 1996;21(3):593-603. 8866481 10.1111/j.1365-2958.1996.tb02567.x
77. Zhang G Tian Y Hu K: Importance and regulation of inositol biosynthesis during growth and differentiation of Streptomyces. Mol Microbiol. 2012;83(6):1178-94. 22329904 10.1111/j.1365-2958.2012.08000.x
78. Chater KF Horinouchi S: Signalling early developmental events in two highly diverged Streptomyces species. Mol Microbiol. 2003;48(1):9-15. 12657041 10.1046/j.1365-2958.2003.03476.x
79. Liu S Yu P Yuan P: Sigma factor WhiG ch positively regulates natamycin production in Streptomyces chattanoogensis L10. Appl Microbiol Biotechnol. 2015;99(6):2715-26. 25724582 10.1007/s00253-014-6307-1
80. Green J Rolfe MD Smith LJ: Transcriptional regulation of bacterial virulence gene expression by molecular oxygen and nitric oxide. Virulence. 2014;5(8):794-809. 25603427 10.4161/viru.27794 4601167
81. Crack JC Green J Thomson AJ: Iron-sulfur clusters as biological sensors: the chemistry of reactions with molecular oxygen and nitric oxide. Acc Chem Res. 2014;47(10):3196-205. 25262769 10.1021/ar5002507
82. Chen Z Hu Y Cumming BM: Mycobacterial WhiB6 Differentially Regulates ESX-1 and the Dos Regulon to Modulate Granuloma Formation and Virulence in Zebrafish. Cell Rep. 2016;16(9):2512-24. 27545883 10.1016/j.celrep.2016.07.080
83. Serrano PN Wang H Crack JC: Nitrosylation of Nitric-Oxide-Sensing Regulatory Proteins Containing [4Fe-4S] Clusters Gives Rise to Multiple Iron-Nitrosyl Complexes. Angew Chem Int Ed Engl. 2016;55(47):14575-14579. 27778474 10.1002/anie.201607033
84. Sasaki Y Oguchi H Kobayashi T: Nitrogen oxide cycle regulates nitric oxide levels and bacterial cell signaling. Sci Rep. 2016;6: 22038. 26912114 10.1038/srep22038 4766573
85. Cunningham-Bussel A Zhang T Nathan CF: Nitrite produced by Mycobacterium tuberculosis in human macrophages in physiologic oxygen impacts bacterial ATP consumption and gene expression. Proc Natl Acad Sci U S A. 2013;110(45):E4256-65. 24145454 10.1073/pnas.1316894110 3831502
86. Cunningham-Bussel A Bange FC Nathan CF: Nitrite impacts the survival of Mycobacterium tuberculosis in response to isoniazid and hydrogen peroxide. Microbiologyopen. 2013;2(6):901-11. 24019302 10.1002/mbo3.126 3892337
87. Fischer M Falke D Pawlik T: Oxygen-dependent control of respiratory nitrate reduction in mycelium of Streptomyces coelicolor A3(2). J Bacteriol. 2014;196(23):4152-62. 25225271 10.1128/JB.02202-14 4248870
88. Lundberg JO Weitzberg E Gladwin MT: The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics. Nat Rev Drug Discov. 2008;7(2):156-67. 18167491 10.1038/nrd2466
89. Vasudevan D Bovee RC Thomas DD: Nitric oxide, the new architect of epigenetic landscapes. Nitric Oxide. 2016;59:54-62. 27553128 10.1016/j.niox.2016.08.002
90. Crack JC Munnoch J Dodd EL: NsrR from Streptomyces coelicolor is a nitric oxide-sensing [4Fe-4S] cluster protein with a specialized regulatory function. J Biol Chem. 2015;290(20):12689-704. 25771538 10.1074/jbc.M115.643072 4432287
91. Crack JC Svistunenko DA Munnoch J: Differentiated, Promoter-specific Response of [4Fe-4S] NsrR DNA Binding to Reaction with Nitric Oxide. J Biol Chem. 2016;291(16):8663-72. 26887943 10.1074/jbc.M115.693192 4861436
92. Wang W Shu D Chen L: Cross-talk between an orphan response regulator and a noncognate histidine kinase in Streptomyces coelicolor. FEMS Microbiol Lett. 2009;294(2):150-6. 19341396 10.1111/j.1574-6968.2009.01563.x
93. Zhang L Willemse J Claessen D: SepG coordinates sporulation-specific cell division and nucleoid organization in Streptomyces coelicolor. Open Biol. 2016;6(4):150164. 27053678 10.1098/rsob.150164 4852450
94. Ladwig N Franz-Wachtel M Hezel F: Control of Morphological Differentiation of Streptomyces coelicolor A3(2) by Phosphorylation of MreC and PBP2. PLoS One. 2015;10(4):e0125425. 25927987 10.1371/journal.pone.0125425 4416010
95. Molle V Palframan WJ Findlay KC: WhiD and WhiB, homologous proteins required for different stages of sporulation in Streptomyces coelicolor A3(2). J Bacteriol. 2000;182(5):1286-95. 10671449 10.1128/JB.182.5.1286-1295.2000 94414
96. Sandoval-Caldern M Nguyen DD Kapono CA: Plasticity of Streptomyces coelicolor Membrane Composition Under Different Growth Conditions and During Development. Front Microbiol. 2015;6:1465. 26733994 10.3389/fmicb.2015.01465 4686642
97. Chandra G Chater KF Bornemann S: Unexpected and widespread connections between bacterial glycogen and trehalose metabolism. Microbiology. 2011;157(Pt 6):1565-72. 21474533 10.1099/mic.0.044263-0
98. Miah F Bibb MJ Barclay JE: Developmental delay in a Streptomyces venezuelae glgE null mutant is associated with the accumulation of maltose 1-phosphate. Microbiology. 2016;162(7):1208-19. 27121970 10.1099/mic.0.000296 5042117
99. Kim JN Jeong Y Yoo JS: Genome-scale analysis reveals a role for NdgR in the thiol oxidative stress response in Streptomyces coelicolor. BMC Genomics. 2015;16(1):116. 25766138 10.1186/s12864-015-1311-0 4340878
100. Liu G Chater KF Chandra G: Molecular regulation of antibiotic biosynthesis in Streptomyces. Microbiol Mol Biol Rev. 2013;77(1):112-43. 23471619 10.1128/MMBR.00054-12 3591988
101. Xu D Waack P Zhang Q: Structure and regulatory targets of SCO3201, a highly promiscuous TetR-like regulator of Streptomyces coelicolor M145. Biochem Biophys Res Commun. 2014;450(1):513-8. 24928397 10.1016/j.bbrc.2014.06.003
102. Rodrguez H Rico S Yepes A: The two kinases, AbrC1 and AbrC2, of the atypical two-component system AbrC are needed to regulate antibiotic production and differentiation in Streptomyces coelicolor. Front Microbiol. 2015;6:450. 26029189 10.3389/fmicb.2015.00450 4428217
103. Rico S Santamara RI Yepes A: Deciphering the regulon of Streptomyces coelicolor AbrC3, a positive response regulator of antibiotic production. Appl Environ Microbiol. 2014;80(8):2417-28. 24509929 10.1128/AEM.03378-13 3993177
104. Bekiesch P Franz-Wachtel M Kulik A: DNA affinity capturing identifies new regulators of the heterologously expressed novobiocin gene cluster in Streptomyces coelicolor M512. Appl Microbiol Biotechnol. 2016;100(10):4495-509. 26795961 10.1007/s00253-016-7306-1
105. Huang J Shi J Molle V: Cross-regulation among disparate antibiotic biosynthetic pathways of Streptomyces coelicolor. Mol Microbiol. 2005;58(5):1276-87. 16313616 10.1111/j.1365-2958.2005.04879.x
106. Vicente CM Payero TD Santos-Aberturas J: Pathway-specific regulation revisited: cross-regulation of multiple disparate gene clusters by PAS-LuxR transcriptional regulators. Appl Microbiol Biotechnol. 2015;99(12):5123-35. 25715784 10.1007/s00253-015-6472-x
107. Li X Wang J Li S: ScbR- and ScbR2-mediated signal transduction networks coordinate complex physiological responses in Streptomyces coelicolor. Sci Rep. 2015;5: 14831. 26442964 10.1038/srep14831 4595836
108. Li X Yu T He Q: Binding of a biosynthetic intermediate to AtrA modulates the production of lidamycin by Streptomyces globisporus. Mol Microbiol. 2015;96(6):1257-71. 25786547 10.1111/mmi.13004
109. Li Y Li J Tian Z: Coordinative Modulation of Chlorothricin Biosynthesis by Binding of the Glycosylated Intermediates and End Product to a Responsive Regulator ChlF1. J Biol Chem. 2016;291(10):5406-17. 26750095 10.1074/jbc.M115.695874 4777870
110. Wolański M Łebkowski T Kois-Ostrowska A: Two transcription factors, CabA and CabR, are independently involved in multilevel regulation of the biosynthetic gene cluster encoding the novel aminocoumarin, cacibiocin. Appl Microbiol Biotechnol. 2016;100(7):3147-64. 26637421 10.1007/s00253-015-7196-7
111. Xu G Wang J Wang L: "Pseudo" gamma-butyrolactone receptors respond to antibiotic signals to coordinate antibiotic biosynthesis. J Biol Chem. 2010;285(35):27440-8. 20562102 10.1074/jbc.M110.143081 2930742
112. Sekurova ON Zhang J Kristiansen KA: Activation of chloramphenicol biosynthesis in Streptomyces venezuelae ATCC 10712 by ethanol shock: insights from the promoter fusion studies. Microb Cell Fact. 2016;15:85. 27206520 10.1186/s12934-016-0484-9 4875748
113. Robertson AW Forget SM Martinez-Farina CF: JadX is a Disparate Natural Product Binding Protein. J Am Chem Soc. 2016;138(7):2200-8. 26814718 10.1021/jacs.5b11286
114. Wang W Ji J Li X: Angucyclines as signals modulate the behaviors of Streptomyces coelicolor. Proc Natl Acad Sci U S A. 2014;111(15):5688-93. 24706927 10.1073/pnas.1324253111 3992645
115. Abrudan MI Smakman F Grimbergen AJ: Socially mediated induction and suppression of antibiosis during bacterial coexistence. Proc Natl Acad Sci U S A. 2015;112(35):11054-9. 26216986 10.1073/pnas.1504076112 4568218
116. Cornforth DM Foster KR: Antibiotics and the art of bacterial war. Proc Natl Acad Sci U S A. 2015;112(35):10827-8. 26305963 10.1073/pnas.1513608112 4568221
117. Imai Y Sato S Tanaka Y: Lincomycin at Subinhibitory Concentrations Potentiates Secondary Metabolite Production by Streptomyces spp. Appl Environ Microbiol. 2015;81(11):3869-79. 25819962 10.1128/AEM.04214-14 4421039
118. Bertrand S Bohni N Schnee S: Metabolite induction via microorganism co-culture: a potential way to enhance chemical diversity for drug discovery. Biotechnol Adv. 2014;32(6):1180-204. 24651031 10.1016/j.biotechadv.2014.03.001
119. Schberle TF Orland A Knig GM: Enhanced production of undecylprodigiosin in Streptomyces coelicolor by co-cultivation with the corallopyronin A-producing myxobacterium, Corallococcus coralloides. Biotechnol Lett. 2014;36(3):641-8. 24249103 10.1007/s10529-013-1406-0
120. Vargas-Bautista C Rahlwes K Straight P: Bacterial competition reveals differential regulation of the pks genes by Bacillus subtilis. J Bacteriol. 2014;196(4):717-28. 24187085 10.1128/JB.01022-13 3911183
121. Traxler MF Kolter R: Natural products in soil microbe interactions and evolution. Nat Prod Rep. 2015;32(7):956-70. 26000872 10.1039/c5np00013k
122. Jeong Y Kim JN Kim MW: The dynamic transcriptional and translational landscape of the model antibiotic producer Streptomyces coelicolor A3(2). Nat Commun. 2016;7: 11605. 27251447 10.1038/ncomms11605 4895711
123. Chater KF Chandra G: The use of the rare UUA codon to define "expression space" for genes involved in secondary metabolism, development and environmental adaptation in streptomyces. J Microbiol. 2008;46(1):1-11. 18337685 10.1007/s12275-007-0233-1
124. Chandra G Chater KF: Evolutionary flux of potentially bldA-dependent Streptomyces genes containing the rare leucine codon TTA. Antonie Van Leeuwenhoek. 2008;94(1):111-26. 18320344 10.1007/s10482-008-9231-5
125. Jensen SE: Biosynthesis of clavam metabolites. J Ind Microbiol Biotechnol. 2012;39(10):1407-19. 22948564 10.1007/s10295-012-1191-0
126. Ferguson NL Pea-Castillo L Moore MA: Proteomics analysis of global regulatory cascades involved in clavulanic acid production and morphological development in Streptomyces clavuligerus. J Ind Microbiol Biotechnol. 2016;43(4):537-55. 26790415 10.1007/s10295-016-1733-y
127. Zeng H Wen S Xu W: Highly efficient editing of the actinorhodin polyketide chain length factor gene in Streptomyces coelicolor M145 using CRISPR/Cas9-CodA(sm) combined system. Appl Microbiol Biotechnol. 2015;99(24):10575-85. 26318449 10.1007/s00253-015-6931-4
128. Liu Y Tao W Wen S: In Vitro CRISPR/Cas9 System for Efficient Targeted DNA Editing. MBio. 2015;6(6):e01714-15. 26556277 10.1128/mBio.01714-15 4659471
129. Tong Y Charusanti P Zhang L: CRISPR-Cas9 Based Engineering of Actinomycetal Genomes. ACS Synth Biol. 2015;4(9):1020-9. 25806970 10.1021/acssynbio.5b00038
130. Huang H Zheng G Jiang W: One-step high-efficiency CRISPR/Cas9-mediated genome editing in Streptomyces. Acta Biochim Biophys Sin (Shanghai). 2015;47(4):231-43. 25739462 10.1093/abbs/gmv007
131. Qiu Y Wang S Chen Z: An Active Type I-E CRISPR-Cas System Identified in Streptomyces avermitilis. PLoS One. 2016;11(2):e0149533. 26901661 10.1371/journal.pone.0149533 4762764
132. Du D Wang L Tian Y: Genome engineering and direct cloning of antibiotic gene clusters via phage BT1 integrase-mediated site-specific recombination in Streptomyces. Sci Rep. 2015;5: 8740. 25737113 10.1038/srep08740 4349145
133. Antoraz S Santamaria RI Daz M: Toward a new focus in antibiotic and drug discovery from the Streptomyces arsenal. Front Microbiol. 2015;6:461. 26029195 10.3389/fmicb.2015.00461 4429630
134. Baltz RH: Genetic manipulation of secondary metabolite biosynthesis for improved production in Streptomyces and other actinomycetes. J Ind Microbiol Biotechnol. 2016;43(2-3):343-70. 26364200 10.1007/s10295-015-1682-x
135. Breitling R Takano E: Synthetic Biology of Natural Products. Cold Spring Harb Perspect Biol. 2016;8(10): pii: a023994. 27503995 10.1101/cshperspect.a023994
136. Weber T Blin K Duddela S: antiSMASH 3.0-a comprehensive resource for the genome mining of biosynthetic gene clusters. Nucleic Acids Res. 2015;43(W1):W237-43. 25948579 10.1093/nar/gkv437 4489286
137. Luo Y Zhang L Barton KW: Systematic Identification of a Panel of Strong Constitutive Promoters from Streptomyces albus. ACS Synth Biol. 2015;4(9):1001-10. 25924180 10.1021/acssynbio.5b00016
138. Li S Wang W Li X: Genome-wide identification and characterization of reference genes with different transcript abundances for Streptomyces coelicolor. Sci Rep. 2015;5: 15840. 26527303 10.1038/srep15840 4630627
139. Willemse J Borst JW de Waal E: Positive control of cell division: FtsZ is recruited by SsgB during sporulation of Streptomyces. Genes Dev. 2011;25(1):89-99. 21205868 10.1101/gad.600211 3012939