Synthesis of the spore envelope in the developmental life cycle of Streptomyces coelicolor

International Journal of Medical Microbiology

Volumn 305, Issue 2, 2015, Pages 183-189

  Sigle, Steffen ^a   Ladwig, Nils ^a   Wohlleben, Wolfgang ^a   Muth, Guenther ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Differentiation; MreB; Peptidoglycan; Serine threonine kinase; Wall teichoic acids

Indexed keywords

BACTERIAL PROTEIN; ENVELOPE PROTEIN; PEPTIDOGLYCAN; SPORE ENVELOPE PROTEIN; UNCLASSIFIED DRUG; MULTIENZYME COMPLEX;

AFFINITY CHROMATOGRAPHY; BACTERIAL SPORE; CELL DIVISION; CELL WALL; GENE CLUSTER; HYDROPHOBICITY; LIFE CYCLE; MORPHOGENESIS; MYCELIUM; NONHUMAN; NUTRIENT LIMITATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SHORT SURVEY; SIGNAL TRANSDUCTION; SPOROGENESIS; STREPTOMYCES COELICOLOR; SYNTHESIS; CHEMISTRY; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

BACTERIAL PROTEINS; CELL WALL; MULTIENZYME COMPLEXES; PEPTIDOGLYCAN; SPORES, BACTERIAL; STREPTOMYCES COELICOLOR;

EID: 84977771279     PISSN: 14384221     EISSN: 16180607     Source Type: Journal    
DOI: 10.1016/j.ijmm.2014.12.014     Document Type: Short Survey

References (51)

1. Ausmees N., Wahlstedt H., Bagchi S., Elliot M.A., Buttner M.J., Flardh K. 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. 2007, 65:1458-1473.
2. Bagchi S., Tomenius H., Belova L.M., Ausmees N. Intermediate filament-like proteins in bacteria and a cytoskeletal function in Streptomyces. Mol. Microbiol. 2008, 70:1037-1050.
3. Bibb M.J., Domonkos A., Chandra G., Buttner M.J. Expression of the chaplin and rodlin hydrophobic sheath proteins in Streptomyces venezuelae is controlled by sigma (BldN) and a cognate anti-sigma factor, RsbN. Mol. Microbiol. 2012, 84:1033-1049.
4. Brown S., Santa Maria J.P., Walker S. Wall teichoic acids of gram-positive bacteria. Annu. Rev. Microbiol. 2013, 67:313-336.
5. Burger A., Sichler K., Kelemen G., Buttner M., Wohlleben W. Identification and characterization of the mre gene region of Streptomyces coelicolor A3(2). Mol. Gen. Genet. 2000, 263:1053-1060.
6. 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. 2007, 64:602-613.
7. Carballido-Lopez R., Errington J. A dynamic bacterial cytoskeleton. Trends Cell Biol. 2003, 13:577-583.
8. Chandra G., Chater K.F. Developmental biology of Streptomyces from the perspective of 100 actinobacterial genome sequences. FEMS Microbiol. Rev. 2014, 38:345-379.
9. Chater K.F. Genetics of differentiation in Streptomyces. Annu. Rev. Microbiol. 1993, 47:685-713.
10. Claessen D., de Jong W., Dijkhuizen L., Wosten H.A. Regulation of Streptomyces development: reach for the sky!. Trends Microbiol. 2006, 14:313-319.
11. Claessen D., Rink R., de Jong W., Siebring J., de Vreugd P., Boersma F.G., Dijkhuizen L., Wosten H.A. A novel class of secreted hydrophobic proteins is involved in aerial hyphae formation in Streptomyces coelicolor by forming amyloid-like fibrils. Genes Dev. 2003, 17:1714-1726.
12. Claessen D., Stokroos I., Deelstra H.J., Penninga N.A., Bormann C., Salas J.A., Dijkhuizen L., Wosten H.A. The formation of the rodlet layer of streptomycetes is the result of the interplay between rodlins and chaplins. Mol. Microbiol. 2004, 53:433-443.
13. Daniel R.A., Errington J. Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell. Cell 2003, 113:767-776.
14. Defeu Soufo H.J., Graumann P.L. Dynamic movement of actin-like proteins within bacterial cells. EMBO Rep. 2004, 5:789-794.
15. Ditkowski B., Holmes N., Rydzak J., Donczew M., Bezulska M., Ginda K., Kedzierski P., Zakrzewska-Czerwinska J., Kelemen G.H., Jakimowicz D. Dynamic interplay of ParA with the polarity protein, Scy, coordinates the growth with chromosome segregation in Streptomyces coelicolor. Open Biol. 2013, 3:130006.
16. Divakaruni A.V., Baida C., White C.L., Gober J.W. The cell shape proteins MreB and MreC control cell morphogenesis by positioning cell wall synthetic complexes. Mol. Microbiol. 2007, 66:174-188.
17. Divakaruni A.V., Loo R.R., Xie Y., Loo J.A., Gober J.W. The cell-shape protein MreC interacts with extracytoplasmic proteins including cell wall assembly complexes in Caulobacter crescentus. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:18602-18607.
18. Dominguez-Escobar J., Chastanet A., Crevenna A.H., Fromion V., Wedlich-Soldner R., Carballido-Lopez R. Processive movement of MreB-associated cell wall biosynthetic complexes in bacteria. Science 2011, 333:225-228.
19. Elliot M.A., Karoonuthaisiri N., Huang J., Bibb M.J., Cohen S.N., Kao C.M., Buttner M.J. The chaplins: a family of hydrophobic cell-surface proteins involved in aerial mycelium formation in Streptomyces coelicolor. Genes Dev. 2003, 17:1727-1740.
20. Flardh K., Buttner M.J. Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium. Nat. Rev. Microbiol. 2009, 7:36-49.
21. Flardh K., Richards D.M., Hempel A.M., Howard M., Buttner M.J. Regulation of apical growth and hyphal branching in Streptomyces. Curr. Opin. Microbiol. 2012, 15:737-743.
22. Formstone A., Carballido-Lopez R., Noirot P., Errington J., Scheffers D.J. Localization and interactions of teichoic acid synthetic enzymes in Bacillus subtilis. J. Bacteriol. 2008, 190:1812-1821.
23. Fuchino K., Bagchi S., Cantlay S., Sandblad L., Wu D., Bergman J., Kamali-Moghaddam M., Flardh K., Ausmees N. Dynamic gradients of an intermediate filament-like cytoskeleton are recruited by a polarity landmark during apical growth. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:1889-1897.
24. Gebbink M.F., Claessen D., Bouma B., Dijkhuizen L., Wosten H.A. Amyloids - a functional coat for microorganisms. Nat. Rev. Microbiol. 2005, 3:333-341.
25. Haiser H.J., Yousef M.R., Elliot M.A. Cell wall hydrolases affect germination, vegetative growth, and sporulation in Streptomyces coelicolor. J. Bacteriol. 2009, 191:6501-6512.
26. Heichlinger A., Ammelburg M., Kleinschnitz E.M., Latus A., Maldener I., Flardh K., Wohlleben W., Muth G. The MreB-like protein Mbl of Streptomyces coelicolor A3(2) depends on MreB for proper localization and contributes to spore wall synthesis. J. Bacteriol. 2011, 193:1533-1542.
27. Hempel A.M., Cantlay S., Molle V., Wang S.B., Naldrett M.J., Parker J.L., Richards D.M., Jung Y.G., Buttner M.J., Flardh K. The Ser/Thr protein kinase AfsK regulates polar growth and hyphal branching in the filamentous bacteria Streptomyces. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:2371-2379.
28. Holmes N.A., Walshaw J., Leggett R.M., Thibessard A., Dalton K.A., Gillespie M.D., Hemmings A.M., Gust B., Kelemen G.H. Coiled-coil protein Scy is a key component of a multiprotein assembly controlling polarized growth in Streptomyces. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:397-406.
29. Jakimowicz D., van Wezel G.P. Cell division and DNA segregation in Streptomyces: how to build a septum in the middle of nowhere?. Mol. Microbiol. 2012, 85:393-404.
30. Kawai Y., Marles-Wright J., Cleverley R.M., Emmins R., Ishikawa S., Kuwano M., Heinz N., Bui N.K., Hoyland C.N., Ogasawara N., Lewis R.J., Vollmer W., Daniel R.A., Errington J. A widespread family of bacterial cell wall assembly proteins. EMBO J. 2011, 30:4931-4941.
31. Kim S.Y., Gitai Z., Kinkhabwala A., Shapiro L., Moerner W.E. Single molecules of the bacterial actin MreB undergo directed treadmilling motion in Caulobacter crescentus. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:10929-10934.
32. Kleinschnitz E.M., Heichlinger A., Schirner K., Winkler J., Latus A., Maldener I., Wohlleben W., Muth G. Proteins encoded by the mre gene cluster in Streptomyces coelicolor A3(2) cooperate in spore wall synthesis. Mol. Microbiol. 2011, 79:1367-1379.
33. Kleinschnitz E.M., Latus A., Sigle S., Maldener I., Wohlleben W., Muth G. Genetic analysis of SCO2997, encoding a TagF homologue, indicates a role for wall teichoic acids in sporulation of Streptomyces coelicolor A3(2). J. Bacteriol. 2011, 193:6080-6085.
34. Kodani S., Hudson M.E., Durrant M.C., Buttner M.J., Nodwell J.R., Willey J.M. The SapB morphogen is a lantibiotic-like peptide derived from the product of the developmental gene ramS in Streptomyces coelicolor. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:11448-11453.
35. Letek M., Ordonez E., Vaquera J., Margolin W., Flardh K., Mateos L.M., Gil J.A. DivIVA is required for polar growth in the MreB-lacking rod-shaped actinomycete Corynebacterium glutamicum. J. Bacteriol. 2008, 190:3283-3292.
36. Mauel C., Young M., Karamata D. Genes concerned with synthesis of poly(glycerol phosphate), the essential teichoic acid in Bacillus subtilis strain 168, are organized in two divergent transcription units. J. Gen. Microbiol. 1991, 137:929-941.
37. Mazza P., Noens E.E., Schirner K., Grantcharova N., Mommaas A.M., Koerten H.K., Muth G., Flardh K., van Wezel G.P., Wohlleben W. MreB of Streptomyces coelicolor is not essential for vegetative growth but is required for the integrity of aerial hyphae and spores. Mol. Microbiol. 2006, 60:838-852.
38. McCormick J.R., Flardh K. Signals and regulators that govern Streptomyces development. FEMS Microbiol. Rev. 2012, 36:206-231.
39. Molle V., Kremer L. Division and cell envelope regulation by Ser/Thr phosphorylation: Mycobacterium shows the way. Mol. Microbiol. 2010, 75:1064-1077.
40. Ostash B., Shashkov A., Streshinskaya G., Tul'skaya E., Baryshnikova L., Dmitrenok A., Dacyuk Y., Fedorenko V. Identification of Streptomyces coelicolor M145 genomic region involved in biosynthesis of teichulosonic acid-cell wall glycopolymer. Folia Microbiol. 2014, 59:355-360.
41. Petrickova K., Petricek M. Eukaryotic-type protein kinases in Streptomyces coelicolor: variations on a common theme. Microbiology 2003, 149:1609-1621.
42. Poralla K., Muth G., Hartner T. Hopanoids are formed during transition from substrate to aerial hyphae in Streptomyces coelicolor A3(2). FEMS Microbiol. Lett. 2000, 189:93-95.
43. Shashkov A.S., Ostash B.E., Fedorenko V.A., Streshinskaya G.M., Tul'skaya E.M., Senchenkova S.N., Baryshnikova L.M., Evtushenko L.I. Novel teichulosonic acid from cell wall of Streptomyces coelicolor M145. Carbohydr. Res. 2012, 359:70-75.
44. van den Ent F., Amos L.A., Lowe J. Prokaryotic origin of the actin cytoskeleton. Nature 2001, 413:39-44.
45. Wang L., Yu Y., He X., Zhou X., Deng Z., Chater K.F., Tao M. Role of an FtsK-like protein in genetic stability in Streptomyces coelicolor A3(2). J. Bacteriol. 2007, 189:2310-2318.
46. White C.L., Kitich A., Gober J.W. Positioning cell wall synthetic complexes by the bacterial morphogenetic proteins MreB and MreD. Mol. Microbiol. 2010, 76:616-633.
47. 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. 2011, 25:89-99.
48. Wolanski M., Wali R., Tilley E., Jakimowicz D., Zakrzewska-Czerwinska J., Herron P. Replisome trafficking in growing vegetative hyphae of Streptomyces coelicolor A3(2). J. Bacteriol. 2011, 193:1273-1275.
49. Xie P., Zeng A., Lv X., Cheng Q., Qin Z. A putative transglycosylase encoded by SCO4132 influences morphological differentiation and actinorhodin production in Streptomyces coelicolor. Acta Biochim. Biophys. Sin. 2013, 45:296-302.
50. Xie P., Zeng A., Qin Z. cmdABCDEF, a cluster of genes encoding membrane proteins for differentiation and antibiotic production in Streptomyces coelicolor A3(2). BMC Microbiol. 2009, 9:157.
51. Yang D.C., Peters N.T., Parzych K.R., Uehara T., Markovski M., Bernhardt T.G. An ATP-binding cassette transporter-like complex governs cell-wall hydrolysis at the bacterial cytokinetic ring. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:1052-1060.