C-di-GMP signalling and the regulation of developmental transitions in streptomycetes

Nature Reviews Microbiology

Volumn 13, Issue 12, 2015, Pages 749-760

  Bush, Matthew J ^a   Tschowri, Natalia ^b   Schlimpert, Susan ^a   Flärdh, Klas ^c   Buttner, Mark J ^a  

^a JOHN INNES CENTRE   (United Kingdom)

^b HUMBOLDT UNIVERSITY   (Germany)

^c LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC GMP; BIS(3',5')-CYCLIC DIGUANYLIC ACID; TRANSCRIPTION FACTOR;

CELL DIVISION; CHROMOSOME REPLICATION; FUNGUS HYPHAE; FUNGUS SPORE; NONHUMAN; PRIORITY JOURNAL; REPRESSOR GENE; REVIEW; SIGNAL TRANSDUCTION; SPOROGENESIS; STREPTOMYCETACEAE; ANALOGS AND DERIVATIVES; BACTERIAL SPORE; BIOLOGICAL MODEL; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

CYCLIC GMP; GENE EXPRESSION REGULATION, BACTERIAL; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION; SPORES, BACTERIAL; STREPTOMYCETACEAE; TRANSCRIPTION FACTORS;

EID: 84947486837     PISSN: 17401526     EISSN: 17401534     Source Type: Journal    
DOI: 10.1038/nrmicro3546     Document Type: Review

References (110)

1. McCormick, J. R., Su, E. P., Driks, A. & Losick, R. Growth and viability of Streptomyces coelicolor mutant for the cell division gene ftsZ. Mol. Microbiol. 14, 243-254 (1994
2. Flärdh, K. & Buttner, M. J. Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium. Nat. Rev. Microbiol. 7, 36-49 (2009
3. Elliot, M. A. et al. The chaplins: a family of hydrophobic cell-surface proteins involved in aerial mycelium formation in Streptomyces coelicolor. Genes Dev. 17, 1727-1740 (2003
4. Claessen, D. et al. A novel class of secreted hydrophobic proteins is involved in aerial hyphae formation in Streptomyces coelicolor by forming amyloid-like fibrils. Genes Dev. 17, 1714-1726 (2003
5. Claessen, D. et al. Two novel homologous proteins of Streptomyces coelicolor and Streptomyces lividans are involved in the formation of the rodlet layer and mediate attachment to a hydrophobic surface. Mol. Microbiol. 44, 1483-1492 (2002
6. Claessen, D. et al. The formation of the rodlet layer of streptomycetes is the result of the interplay between rodlins and chaplins. Mol. Microbiol. 53, 433-443 (2004
7. Elliot, M. A. & Talbot, N. J. Building filaments in the air: aerial morphogenesis in bacteria and fungi. Curr. Opin. Microbiol. 7, 594-601 (2004
8. DiBerardo, C. et al. Function and redundancy of the chaplin cell surface proteins in aerial hypha formation, rodlet assembly, and viability in Streptomyces coelicolor. J. Bacteriol. 190, 5879-5889 (2008
9. Willey, J. M., Willems, A., Kodani, S. & Nodwell, J. R. Morphogenetic surfactants and their role in the formation of aerial hyphae in Streptomyces coelicolor. Mol. Microbiol. 59, 731-742 (2006
10. Willey, J., Santamaria, R., Guijarro, J., Geistlich, M. & Losick, R. Extracellular complementation of a developmental mutation implicates a small sporulation protein in aerial mycelium formation by S. coelicolor. Cell 65, 641-650 (1991
11. Kodani, S. et al. The SapB morphogen is a lantibiotic-like peptide derived from the product of the developmental gene ramS in Streptomyces coelicolor. Proc. Natl Acad. Sci. USA 101, 11448-11453 (2004
12. Capstick, D. S., Willey, J. M., Buttner, M. J. & Elliot, M. A. SapB and the chaplins: connections between morphogenetic proteins in Streptomyces coelicolor. Mol. Microbiol. 64, 602-613 (2007
13. McCormick, J. R. & Flärdh, K. Signals and regulators that govern Streptomyces development. FEMS Microbiol. Rev. 36, 206-231 (2012
14. Chater, K. F. in Streptomyces: Molecular Biology and Biotechnology (ed. Dyson P.) 43-86 (Caister Academic Press, 2011
15. Ohnishi, Y., Yamazaki, H., Kato, J. Y., Tomono, A. & Horinouchi, S. AdpA, a central transcriptional regulator in the A factor regulatory cascade that leads to morphological development and secondary metabolism in Streptomyces griseus. Biosci. Biotechnol. Biochem. 69, 431-439 (2005
16. Horinouchi, S. Mining and polishing of the treasure trove in the bacterial genus Streptomyces. Biosci. Biotechnol. Biochem. 71, 283-299 (2007
17. Horinouchi, S. in Chemical Communication among Bacteria (eds Winans, S. C. & Bassler, B. L.) 363-377 (ASM Press, 2008
18. Takano, E. γ-Butyrolactones: Streptomyces signalling molecules regulating antibiotic production and differentiation. Curr. Opin. Microbiol. 9, 287-294 (2006
19. Traxler, M. F., Seyedsayamdost, M. R., Clardy, J. & Kolter, R. Interspecies modulation of bacterial development through iron competition and siderophore piracy. Mol. Microbiol. 86, 628-644 (2012
20. Lambert, S. et al. Altered desferrioxamine-mediated iron utilization is a common trait of bald mutants of Streptomyces coelicolor. Metallomics 6, 1390-1399 (2014
21. Jenal, U. & Malone, J. Mechanisms of cyclic-di GMP signaling in bacteria. Annu. Rev. Genet. 40, 385-407 (2006
22. Hengge, R. Principles of c di GMP signalling in bacteria. Nat. Rev. Microbiol. 7, 263-273 (2009
23. Römling, U., Galperin, M. Y. & Gomelsky, M. Cyclic di GMP: the first 25 years of a universal bacterial second messenger. Microbiol. Mol. Biol. Rev. 77, 1-52 (2013
24. Tran, N. T., den Hengst, C. D., Gomez-Escribano, J. P. & Buttner, M. J. Identification and characterization of CdgB, a diguanylate cyclase involved in developmental processes in Streptomyces coelicolor. J. Bacteriol. 193, 3100-3108 (2011
25. Hull, T. D. et al. Cyclic di GMP phosphodiesterases RmdA and RmdB are involved in regulating colony morphology and development in Streptomyces coelicolor. J. Bacteriol. 194, 4642-4651 (2012
26. Tschowri, N. et al. Tetrameric c di GMP mediates effective transcription factor dimerization to control Streptomyces development. Cell 158, 1136-1147 (2014
27. Chater, K. F. & Horinouchi, S. Signalling early developmental events in two highly diverged Streptomyces species. Mol. Microbiol. 48, 9-15 (2003
28. Schirmer, T. & Jenal, U. Structural and mechanistic determinants of c di GMP signalling. Nat. Rev. Microbiol. 7, 724-735 (2009
29. Bush, M. J., Bibb, M. J., Chandra, G., Findlay, K. C. & Buttner, M. J. Genes required for aerial growth, cell division and chromosome segregation are targets of WhiA before sporulation in Streptomyces venezuelae. mBio 4, e00684-e00613 (2013
30. den Hengst, C. D. et al. Genes essential for morphological development and antibiotic production in Streptomyces coelicolor are targets of BldD during vegetative growth. Mol. Microbiol. 78, 361-379 (2010
31. Elliot, M. A., Bibb, M. J., Buttner, M. J. & Leskiw, B. K. BldD is a direct regulator of key developmental genes in Streptomyces coelicolor A3(2). Mol. Microbiol. 40, 257-269 (2001
32. Flärdh, K., Leibovitz, E., Buttner, M. J. & Chater, K. F. Generation of a non-sporulating strain of Streptomyces coelicolor A3(2) by the manipulation of a developmentally controlled ftsZ promoter. Mol. Microbiol. 38, 737-749 (2000
33. McCormick, J. R. Cell division is dispensable but not irrelevant in Streptomyces. Curr. Opin. Microbiol. 12, 689-698 (2009
34. Willemse, J., Borst, J. W., De Waal, E., Bisseling, T. & van Wezel, G. P. Positive control of cell division: FtsZ is recruited by SsgB during sporulation of Streptomyces. Genes Dev. 25, 89-99 (2011
35. Ausmees, N. et al. SmeA, a small membrane protein with multiple functions in Streptomyces sporulation including targeting of a SpoIIIE/FtsK-like protein to cell division septa. Mol. Microbiol. 65, 1458-1473 (2007
36. Tzanis, A. et al. A sporulation specific, sigF-dependent protein, SspA, affects septum positioning in Streptomyces coelicolor. Mol. Microbiol. 91, 363-380 (2014
37. Kim, I. K. et al. Crystal structure of the DNA-binding domain of BldD, a central regulator of aerial mycelium formation in Streptomyces coelicolor A3(2). Mol. Microbiol. 60, 1179-1193 (2006
38. Kim, J. M., Won, H. S. & Kang, S. O. The C terminal domain of the transcriptional regulator BldD from Streptomyces coelicolor A3(2) constitutes a novel fold of winged-helix domains. Proteins: Structure, function and bioinformatics. Proteins 82, 1093-1098 (2014
39. Abel, S. et al. Regulatory cohesion of cell cycle and cell differentiation through interlinked phosphorylation and second messenger networks. Mol. Cell 43, 550-560 (2011
40. Abel, S. et al. Bi modal distribution of the second messenger c di GMP controls cell fate and asymmetry during the Caulobacter cell cycle. PLoS Genet. 9, e1003744 (2013
41. Massie, J. P. et al. Quantification of high-specificity cyclic diguanylate signaling. Proc. Natl Acad. Sci. USA 109, 12746-12751 (2012
42. Ryan, R. P. et al. Cell-cell signal-dependent dynamic interactions between HD GYP and GGDEF domain proteins mediate virulence in Xanthomonas campestris. Proc. Natl Acad. Sci. USA 107, 5989-5994 (2010
43. Lindenberg, S., Klauck, G., Pesavento, C., Klauck, E. & Hengge, R. The EAL domain protein YciR acts as a trigger enzyme in a c di GMP signalling cascade in E. coli biofilm control. EMBO J. 32, 2001-2014 (2013
44. Jenal, U. Think globally, act locally: how bacteria integrate local decisions with their global cellular programme. EMBO J. 32, 1972-1974 (2013
45. Kelemen, G. H. et al. A connection between stress and development in the multicellular prokaryote Streptomyces coelicolor A3(2). Mol. Microbiol. 40, 804-814 (2001
46. Elliot, M. A. & Leskiw, B. K. The BldD protein from Streptomyces coelicolor is a DNA-binding protein. J. Bacteriol. 181, 6832-6835 (1999
47. Allenby, N. E., Laing, E., Bucca, G., Kierzek, A. M. & Smith, C. P. Diverse control of metabolism and other cellular processes in Streptomyces coelicolor by the PhoP transcription factor: genome-wide identification of in vivo targets. Nucleic Acids Res. 40, 9543-9556 (2012
48. Chandra, G. & Chater, K. F. Developmental biology of Streptomyces from the perspective of 100 actinobacterial genome sequences. FEMS Microbiol. Rev. 38, 345-379 (2014
49. Chng, C., Lum, A. M., Vroom, J. A. & Kao, C. M. A key developmental regulator controls the synthesis of the antibiotic erythromycin in Saccharopolyspora erythraea. Proc. Natl Acad. Sci. USA 105, 11346-11351 (2008
50. Bibb, M. J., Domonkos, Á, Chandra, G. & Buttner, M. J. Expression of the chaplin and rodlin hydrophobic sheath proteins in Streptomyces venezuelae is controlled by sBldN and a cognate anti-sigma factor, RsbN. Mol. Microbiol. 84, 1033-1049 (2012
51. Helmann, J. D. in Bacterial stress responses, 2nd Edition (eds Storz, G. & Hengge, R.) 31-41 (ASM press, 2011
52. Staron, A. et al. The third pillar of bacterial signal transduction: classification of the extracytoplasmic function (ECF) s factor protein family. Mol. Microbiol. 74, 557-581 (2009
53. Ruban-Osmialowska, B., Jakimowicz, D., Smulczyk-Krawczyszyn, A., Chater, K. F. & Zakrzewska-Czerwinska, J. Replisome localization in vegetative and aerial hyphae of Streptomyces coelicolor. J. Bacteriol. 188, 7311-7316 (2006
54. Higo, A., Hara, H., Horinouchi, S. & Ohnishi, Y. Genome-wide distribution of AdpA, a global regulator for secondary metabolism and morphological differentiation in Streptomyces, revealed the extent and complexity of the AdpA regulatory network. DNA Res. 19, 259-273 (2012
55. Wolanski, M., Jakimowicz, D. & Zakrzewska-Czerwinska, J. AdpA, key regulator for morphological differentiation regulates bacterial chromosome replication. Open Biol. 2, 120097 (2012
56. Chater, K. F. & 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. 46, 1-11 (2008
57. Higo, A., Horinouchi, S. & Ohnishi, Y. Strict regulation of morphological differentiation and secondary metabolism by a positive feedback loop between two global regulators AdpA and BldA in Streptomyces griseus. Mol. Microbiol. 81, 1607-1622 (2011
58. Takano, E. et al. A rare leucine codon in adpA is implicated in the morphological defect of bldA mutants of Streptomyces coelicolor. Mol. Microbiol. 50, 475-486 (2003
59. Flärdh, K., Findlay, K. C. & Chater, K. F. Association of early sporulation genes with suggested developmental decision points in Streptomyces coelicolor A3(2). Microbiology 145, 2229-2243 (1999
60. Aínsa, J. A. et al. WhiA, a protein of unknown function conserved among Gram-positive bacteria, is essential for sporulation in Streptomyces coelicolor A3(2). J. Bacteriol. 182, 5470-5478 (2000
61. Bagchi, S., Tomenius, H., Belova, L. M. & Ausmees, N. Intermediate filament-like proteins in bacteria and a cytoskeletal function in Streptomyces. Mol. Microbiol. 70, 1037-1050 (2008
62. Fuchino, K. et al. Dynamic gradients of an intermediate filament-like cytoskeleton are recruited by a polarity landmark during apical growth. Proc. Natl Acad. Sci. USA 110, E1889-E1897 (2013
63. Hempel, A. M. et al. The Ser/Thr protein kinase AfsK regulates polar growth and hyphal branching in the filamentous bacteria Streptomyces. Proc. Natl Acad. Sci. USA 109, E2371-E2379 (2012
64. Holmes, N. A. et al. Coiled-coil protein Scy is a key component of a multiprotein assembly controlling polarized growth in Streptomyces. Proc. Natl Acad. Sci. USA 110, E397-E406 (2013
65. Flärdh, K., Richards, D. M., Hempel, A. M., Howard, M. & Buttner, M. J. Regulation of apical growth and hyphal branching in Streptomyces. Curr. Opin. Microbiol. 15, 737-743 (2012
66. Ditkowski, B. et al. Dynamic interplay of ParA with the polarity protein, Scy, coordinates the growth with chromosome segregation in Streptomyces coelicolor. Open Biol. 3, 130006 (2013
67. Surdova, K. et al. The conserved DNA-binding protein WhiA is involved in cell division in Bacillus subtilis. J. Bacteriol. 195, 5450-5460 (2013
68. Knizewski, L. & Ginalski, K. Bacterial DUF199/ COG1481 proteins including sporulation regulator WhiA are distant homologs of LAGLIDADG homing endonucleases that retained only DNA binding. Cell Cycle 6, 1666-1670 (2007
69. Kaiser, B. K., Clifton, M. C., Shen, B. W. & Stoddard, B. L. The structure of a bacterial DUF199/ WhiA protein: domestication of an invasive endonuclease. Structure 17, 1368-1376 (2009
70. Taylor, G. K. & Stoddard, B. L. Structural, functional and evolutionary relationships between homing endonucleases and proteins from their host organisms. Nucleic Acids Res. 40, 5189-5200 (2012
71. Kaiser, B. K. & Stoddard, B. L. DNA recognition and transcriptional regulation by the WhiA sporulation factor. Sci. Rep. 1, 156 (2011
72. Al Bassam, M. M., Bibb, M. J., Bush, M. J., Chandra, G. & Buttner, M. J. Response regulator heterodimer formation controls a key stage in Streptomyces development. PLoS Genetics 10, e1004554 (2014
73. Jakimowicz, P. et al. Evidence that the Streptomyces developmental protein WhiD, a member of the WhiB family, binds a [4Fe 4S] cluster. J. Biol. Chem. 280, 8309-8315 (2005
74. Singh, A. et al. Mycobacterium tuberculosis WhiB3 responds to O2 and nitric oxide via its [4Fe 4S] cluster and is essential for nutrient starvation survival. Proc. Natl Acad. Sci. USA 104, 11562-11567 (2007
75. Singh, A. et al. Mycobacterium tuberculosis WhiB3 maintains redox homeostasis by regulating virulence lipid anabolism to modulate macrophage response. PLoS Pathog. 5, e1000545 (2009
76. Crack, J. C. et al. Characterization of [4Fe 4S]-containing and cluster-free forms of Streptomyces WhiD. Biochemistry 48, 12252-12264 (2009
77. Crack, J. C. et al. Mechanistic insight into the nitrosylation of the [4Fe 4S] cluster of WhiB-like proteins. J. Am. Chem. Soc. 133, 1112-1121 (2011
78. den Hengst, C. D. & Buttner, M. J. Redox control in actinobacteria. Biochem. Biophys. Acta. 1780, 1201-1216 (2008
79. Burian, J. et al. The mycobacterial antibiotic resistance determinant WhiB7 acts as a transcriptional activator by binding the primary sigma factor SigA (RpoV). Nucleic Acids Res. 41, 10062-10076 (2013
80. Burian, J., Ramón-García, S., Howes, C. G. & Thompson, C. J. WhiB7, a transcriptional activator that coordinates physiology with intrinsic drug resistance in Mycobacterium tuberculosis. Expert Rev. Anti. Infect. Ther. 10, 1037-1047 (2012
81. Rybniker, J. et al. Insights into the function of the WhiB-like protein of mycobacteriophage TM4 - a transcriptional inhibitor of WhiB2. Mol. Microbiol. 77, 642-657 (2010
82. Smith, L. et al. Mycobacterium tuberculosis WhiB1 is an essential DNA-binding protein with a nitric oxide-sensitive iron-sulfur cluster. Biochem. J. 432, 417-427 (2010
83. Aínsa, J. A., Parry, H. D. & Chater, K. F. A response regulator-like protein that functions at an intermediate stage of sporulation in Streptomyces coelicolor A3(2). Mol. Microbiol. 34, 607-619 (1999
84. Ryding, N. J. et al. A developmentally regulated gene encoding a repressor-like protein is essential for sporulation in Streptomyces coelicolor A3(2). Mol. Microbiol. 29, 343-357 (1998
85. Persson, J., Chater, K. F. & Flärdh, K. Molecular and cytological analysis of the expression of Streptomyces sporulation regulatory gene whiH. FEMS Microbiol. Lett. 341, 96-105 (2013
86. Rigali, S., Derouaux, A., Giannotta, F. & Dusart, J. Subdivision of the helix-turn-helix GntR family of bacterial regulators in the FadR, HutC, MocR, and YtrA subfamilies. J. Biol. Chem. 277, 12507-12515 (2002
87. Hoskisson, P. A. & Rigali, S. Variation in form and function the helix-turn-helix regulators of the GntR superfamily. Adv. Appl. Microbiol. 69, 1-22 (2009
88. DiRusso, C. C. & Nyström, T. The fats of Escherichia coli during infancy and old age: regulation by global regulators, alarmones and lipid intermediates. Mol. Microbiol. 27, 1-8 (1998
89. Tian, Y., Fowler, K., Findlay, K., Tan, H. & Chater, K. F. An unusual response regulator influences sporulation at early and late stages in Streptomyces coelicolor. J. Bacteriol. 189, 2873-2885 (2007
90. Molle, V. & Buttner, M. J. Different alleles of the response regulator gene bldM arrest Streptomyces coelicolor development at distinct stages. Mol. Microbiol. 36, 1265-1278 (2000
91. Reményi, A., Schöler, H. R. & Wilmanns, M. Combinatorial control of gene expression. Nat. Struct. Mol. Biol. 11, 812-815 (2004
92. Majdalani, N. & Gottesman, S. The Rcs phosphorelay: a complex signal transduction system. Annu. Rev. Microbiol. 59, 379-405 (2005
93. Majdalani, N. & Gottesman, S. Genetic dissection of signaling through the Rcs phosphorelay. Methods Enzymol. 423, 349-362 (2007
94. Richet, E., Vidal-Ingigliardi, D. & Raibaud, O. A new mechanism for coactivation of transcription initiation: repositioning of an activator triggered by the binding of a second activator. Cell 66, 1185-1195 (1991
95. Wade, J. T., Belyaeva, T. A., Hyde, E. I. & Busby, S. J. A simple mechanism for co dependence on two activators at an Escherichia coli promoter. EMBO J. 20, 7160-7167 (2001
96. Browning, D. F. & Busby, S. J. The regulation of bacterial transcription initiation. Nat. Rev. Microbiol. 2, 57-65 (2004
97. Lee, D. J., Minchin, S. D. & Busby, S. J. Activating transcription in bacteria. Annu. Rev. Microbiol. 66, 125-152 (2012
98. Traag, B. A., Kelemen, G. H. & van Wezel, G. P. Transcription of the sporulation gene ssgA is activated by the IclR-type regulator SsgR in a whi-independent manner in Streptomyces coelicolor A3(2). Mol. Microbiol. 53, 985-1000 (2004
99. Kelemen, G. H. et al. Developmental regulation of transcription of whiE, a locus specifying the polyketide spore pigment in Streptomyces coelicolor A3(2). J. Bacteriol. 180, 2515-2521 (1998
100. Schlimpert, S., Flärdh, K. & Buttner, M. J. Fluorescence time-lapse imaging of the complete Streptomyces life cycle using a microfluidic device. J. Vis. Exp. (in the press)
101. Domínguez-Escobar, J. et al. Processive movement of MreB-associated cell wall biosynthetic complexes in bacteria. Science 333, 225-228 (2011
102. Garner, E. C. et al. Coupled, circumferential motions of the cell wall synthesis machinery and MreB filaments in B. subtilis. Science 333, 222-225 (2011
103. Margolin, W. Sculpting the bacterial cell. Curr. Biol. 19, R812-R822 (2009
104. Cabeen, M. T. & Jacobs-Wagner, C. The bacterial cytoskeleton. Annu. Rev. Genet. 44, 365-392 (2010
105. Kysela, D. T., Brown, P. J., Huang, K. C. & Brun, Y. V. Biological consequences and advantages of asymmetric bacterial growth. Annu. Rev. Microbiol. 67, 417-435 (2013
106. Brown, P. J., Kysela, D. T. & Brun, Y. V. Polarity and the diversity of growth mechanisms in bacteria. Semin. Cell. Dev. Biol. 22, 790-798 (2011
107. Errington, J. Bacterial morphogenesis and the enigmatic MreB helix. Nat. Rev. Microbiol. 13, 241-248 (2015
108. Hempel, A. M., Wang, S., Letek, M., Gil, J. A. & Flärdh, K. Assemblies of DivIVA mark sites for hyphal branching and can establish new zones of cell wall growth in Streptomyces coelicolor. J. Bacteriol. 90, 7579-7583 (2008
109. Richards, D., Hempel, A. M., Flärdh, K., Buttner, M. J. & Howard, M. Mechanistic basis of branch-site selection in filamentous bacteria. PLoS Comput. Biol. 8, e1002423 (2012
110. Glazebrook, M. A., Doull, J. L., Stuttard, C. & Vining, L. C. Sporulation of Streptomyces venezuelae in submerged cultures. J. Gen. Microbiol. 136, 581-588 (1990