1887

Chapter 2 : Developmental Decisions during Sporulation in the Aerial Mycelium in Streptomyces

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in
Zoomout

Developmental Decisions during Sporulation in the Aerial Mycelium in Streptomyces, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555818166/9781555811587_Chap02-1.gif /docserver/preview/fulltext/10.1128/9781555818166/9781555811587_Chap02-2.gif

Abstract:

This chapter deals with an unusual bacterial example involving growth into the air: the formation and metamorphosis of reproductive aerial hyphae in spp. Sporulation septa differ morphologically from vegetative septa and also show considerable variation among species, particularly in thickness. The role of FtsZ is to form a cytoplasmically located, but membrane-coupled, ring at incipient sites of septation to act as a cytoskeletal element in guiding the ingrowth of the septum by contracting, finally disassembling to leave the (FtsZ-free) completed septum. This mechanism is universal among bacteria, so it is not surprising that an ftsZ gene is present in spp. Indeed, immunofluorescence analysis has shown that both vegetative septum and sporulation septum formation involves FtsZ ring formation. Although very large numbers of genes can be expected to contribute to sporulation, many of them are also important during vegetative growth (for example, genes for macromolecular synthesis and primary metabolism) and others may fulfill very subtle functions that are not readily discernible by investigators. More likely, the physiological role of the stalk is completed when sporulation septation takes place. At this time, the stalk becomes more transparent in phase-contrast microscopy and less fluorescence is seen in stalks after DAPI (4', 6-diamidino- 2-phenylindole) staining for DNA. Thus, our present state of knowledge does not suggest that the conversion of prespore compartments into spores should involve very complex genetic regulation or developmental checkpoints.

Citation: Chater K. 2000. Developmental Decisions during Sporulation in the Aerial Mycelium in Streptomyces, p 33-48. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch2
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of FIGURE 2
FIGURE 2

Spore chains and hyphal filaments on the surface of a colony. (Reproduced from , with permission.)

Citation: Chater K. 2000. Developmental Decisions during Sporulation in the Aerial Mycelium in Streptomyces, p 33-48. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch2
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2
FIGURE 2

Two alternative possible hyphal growth modes. Heavy shading indicates cell wall growth zones. To the left are diagrammed successive stages in rapid growth of a typical segment of vegetative mycelium, in which an exponential increase in total length is maintained by combining linear cell wall growth at the tips with exponentially increasing numbers of branches (and hence, of tips). To the right is diagrammed the situation postulated for a rapidly growing, but unbranched, aerial hypha, in which an exponential increase in total length is achieved by intercalary growth.

Citation: Chater K. 2000. Developmental Decisions during Sporulation in the Aerial Mycelium in Streptomyces, p 33-48. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch2
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3
FIGURE 3

Developing spore chains, (a) External morphologies of two spore chains, the left-hand one being more mature, (b) The regular ladders of sporulation septa (revealed by cell wall staining with fluorescein-linked wheat germ agglutinin after lysozyme treatment) extend to the hyphal tips; note that the lateral cell wall stains strongly in aerial-hyphal stalks, weakly in the least mature part of the long spore chain closest to the stalk, and not at all in the more mature parts, (c) Nuclear segregation (revealed by staining with 7-amino actinomycin D) has not occurred in the absence of septation (arrow in panels b and c). (Modified from , with permission.)

Citation: Chater K. 2000. Developmental Decisions during Sporulation in the Aerial Mycelium in Streptomyces, p 33-48. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch2
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 4
FIGURE 4

Speculative model implicating Whi proteins in developmental decisions. It is proposed that initially σ is held in an inactive state, but a signal produced while young aerial hyphae are early in growth releases active σ (1). Among the σ targets would be genes involved in cell wall biosynthesis, leading to spiral growth. After a moderate number of cell doublings, WhiA and WhiB combine to bring growth to an orderly stop (2), probably in response to one or more further signals. Growth cessation (bold T) would release a further signal, activating WhiH (3). WhiH somehow activates the full initiation of sporulation septation but is less stringently required for certain other late events, such as DNA condensation, changes in the spore wall, and gray-pigment production. The diagrams in the lower part of the figure represent the relevant mutant phenotypes. Bold arrows indicate continuing growth. (Reproduced from , with permission.)

Citation: Chater K. 2000. Developmental Decisions during Sporulation in the Aerial Mycelium in Streptomyces, p 33-48. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch2
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 5
FIGURE 5

The long, often tightly coiled aerial hyphae of a disruption mutant. (Scanning electron micrograph kindly provided by K. Findlay and K. Flärdh.)

Citation: Chater K. 2000. Developmental Decisions during Sporulation in the Aerial Mycelium in Streptomyces, p 33-48. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch2
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 6
FIGURE 6

Transcriptional dependencies of genes. This scheme combines results from Kelemen et al. ( ), , and . (Drawing provided by J. Aínsa.)

Citation: Chater K. 2000. Developmental Decisions during Sporulation in the Aerial Mycelium in Streptomyces, p 33-48. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch2
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555818166.chap2
1. Aínsa, J. A.,, H. D. Parry,, and K. F. Chater. A response regulator-like protein that functions at an intermediate stage of sporulation in Streptomyces coelicolor A3(2). Mol. Microbiol., in press.
2. Blanco, G.,, A. Pereda,, P. Brian,, C. Méndez,, K. F. Chater,, and J. A. Salas. 1993. A hydroxylase-like gene product contributes to synthesis of a polyketide spore pigment in Streptomyces halstedii. J. Bacteriol. 175: 80438048.
3. Braña, A. F.,, C. Méndez,, L. A. Díaz,, M. B. Manzanal,, and C. Hardisson. 1986. Glycogen and trehalose accumulation during colony development in Streptomyces antibioticus. J. Gen. Microbiol. 132: 13191326.
4. Brown, D. W.,, and J. J. Salvo. 1994. Isolation and characterisation of sexual spore pigments from Aspergillus nidulans. Appl. Environ. Microbiol. 60: 979983.
5. Brown, D. W.,, F. M. Hauser,, and J. J. Salvo. 1993. Structural elucidation of a putative conidial pigment intermediate in Aspergillus parasiticus. Tetrahedron Lett. 34:419422.
6. Bruton, C. J.,, K. A. Plaskitt,, and K. F. Chater. 1995. Tissue-specific glycogen branching isoenzymes in a multicellular prokaryote, Streptomyces coelicolor A3(2). Mol. Microbiol. 18:8999.
7. Chater, K. F. 1972. A morphological and generic mapping study of white colony mutants of Streptomyces coelicolor. J. Cen. Microbiol. 72:928.
8. Chater, K. F. 1989. Multilevel regulation of Streptomyces differentiation. Trends Genet. 5:372376.
9. Chater, K. F. 1991. Saps, hydrophobins, and aerial growth. Curr. Biol. 1:318320.
10. Chater, K. F. 1998. Taking a genetic scalpel to the Streptomyces colony. Microbiology 144:14651478.
11. Chater, K. F.,, and R. Losick,. 1997. The mycelial life-style of Streptomyces coelicolor A3(2) and its relatives, p. 149182. In J. H. Shapiro, and M. Dworkin (ed.). Bacteria as Multicellular Organisms. Oxford University Press, New York, N.Y.
12. Chater, K. F.,, C.J. Bruton,, K. A. Plaskitt,, M. J. Buttner,, C. Méndez,, and J. Helmann. 1989. The developmental fate of S. coelicolor hyphae depends crucially on a gene product homologous with the motility sigma factor of B. subtilis. Cell 59: 133143.
13. Cole, S. T.,, R. Brosch,, J. Parkhill,, T. Gamier,, C. Churcher,, D. Harris,, S. V. Gordon,, K. Eiglmeier,, S. Gas,, C. E. Barry,, F. Tekaia,, K. Badcock,, D. Basham,, D. Brown,, T. Chil-lingworth,, R. Conner,, R. Davies,, K. Devlin,, T. Feltwell,, S. Gentles,, N. Hamlin,, S. Holroyd,, T. Hornsby,, K. Jaels,, A. Krogh,, J. McLean,, S. Moule,, L. Murphy,, K. Oliver,, J. Osborne,, M. A. Quail,, A. Rajandream,, J. Rogers,, S. Rutter,, K. Segger,, J. Skelton,, R. Squares,, S. Squares,, J. E. Sulston,, K. Taylor,, S. Whitehead,, and B. G. Barrel]. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393: 537544.
14. Davis, N. K.,, and K. F. Chater. 1992. The Streptomyces coelicolor whiB gene encodes a small transcription factor-like protein dispensable for growth but essential for sporulation. Mol. Gen. Genet. 232: 351358.
15. DiRusso, C. C.,, and T. Nyström. 1998. The fats of Escherichia coli during infancy and old age: regulation by global regulators, alarmones and lipid intermediates. Mol. Microbiol. 27:18.
16. Donachie, W. D. 1993. The cell cycle of Escherichia coli. Annu. Rev. Microbiol. 47:199230.
17. Dukan, S.,, and T. Nyström. 1998. Bacterial senescence: stasis results in increased and differential oxidation of cytoplasmic proteins leading to developmental induction of the heat shock regulon. Genes Dev. 12:34313441.
18. Flärdh, K. Personal communication.
19. Flärdh, K.,, P. Palacios,, and M. Vicente. 1998. Cell division genes fisQAS in Escherichia coli require distant cis-acting signals upstream of ddlB for full expression. Mol. Microbiol. 30:305315.
20. Flärdh, K.,, K. C. Findlay,, and K. F. Chater. Association of early sporulation genes with suggested developmental decision points in Streptomyces coelicolor A3(2). Microbiology, in press.
21. Gerber, N. N. 1979. Volatile substances from actinomycetes: their role in the odor pollution of water. Crit. Rev. Microbiol. 7:191214.
22. Hao, J.,, and K. E. Kendrick. 1998. Visualization of penicillin-binding proteins during sporulation of Streptomyces griseus. J. Bacteriol. 180:21252132.
23. Hardisson, C.,, and M. B. Manzanal. 1976. Ultra-structural studies of sporulation in Streptomyces. J. Bacteriol. 127:14431454.
24. Homerová, D.,, O. Benada,, O. Kofronova,, B. Rezuchová,, and J. Kormanec. 1996. Disruption of a glycogen branching enzyme gene, glgB, specifically affects the sporulation-associated phase of glycogen accumulation in Streptomyces aureofaciens. Microbiology 142:12011208.
25. Hopwood, D. A.,, H. Wildermuth,, and H. M. Palmer. 1970. Mutants of Streptomyces coelicolor defective in sporulation. J. Cen. Microbiol. 61: 397408.
26. Kelemen, G. H.,, and M.J. Buttner. 1998. Initiation of aerial mycelium formation in Streptomyces. Curr. Opin. Microbiol. 1:656662.
27. Kelemen, G. H.,, M. S. B. Paget,, and M.J. Buttner. Personal communication.
28. Kelemen, G. H.,, G. L. Brown,, J. Kormanec,, L. Potúčková,, K. F. Chater,, and M. J. Buttner. 1996. 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. 21:593603.
29. Kelemen, G. H.,, P. Brian,, K. Flardh,, L. Chamberlin,, K. F. Chater,, and M.J. Buttner. 1998. Developmental regulation of transcription of whiE, a locus specifying the polyketide spore pigment in Streptomyces coelicolor A3(2). J. Bacteriol. 180: 25152521.
30. Kendrick, K. E. Personal communication.
31. Kim, H.-J.,, M. J. Calcutt,, F. J. Schmidt,, and K. F. Chater. Chromosome partitioning during sporulation of Streptomyces coelicolor A3(2) involves an oriC-linked parAB locus. Manuscript in preparation.
32. Kormanec, J.,, L. Potüčková,, and B. Rezuchová. 1994. The Streptomyces aureofaciens homologue of the whiG gene encoding a putative sigma factor essential for sporulation. Gene 143:101103.
33. Kormanec, J.,, D. Homerová,, L. Potüčková,, R. Novâkovâ,, and B. Rezuchová. 1996. Differential expression of two sporulation specific σ factors of Streptomyces aureofaciens correlates with the developmental stage. Gene 181:1927.
34. Kormanec, J.,, B. Ševčíková,, O. Sprusansky,, O. Benada,, O. Kofronova,, R. Nováková,, B. Rezuchovâ,, L. Potúčková,, and D. Homerová. 1998. The Streptomyces aureofaciens homologue of the whiB gene is essential for sporulation; its expression correlates with the developmental stage. Folia Microbiol. 43:605612.
35. Kormanec, J.,, R. Novakova,, D. Homerova,, and B. Ševčíková. 1999. The Streptomyces aureofaciens homologue of the sporulation gene whiH is dependent on rpoZ-encoded σ factor. Biochim. Biophys. Acta 1444:8084.
36. Losick, R.,, and L. Shapiro. 1993. Checkpoints that couple gene expression to morphogenesis. Science 262:12271228.
37. Martin, M. C.,, D. Schneider,, C. J. Bruton,, K. F. Chater,, and C. Hardisson. 1997. A glgC gene essential only for the first of two spatially distinct phases of glycogen synthesis in Streptomyces coelicolor A3(2). J. Bacteriol. 179:77847789.
38. McCormick, J.,, E. P. Su,, A. Driks,, and R. Losick. 1994. Growth and viability of Streptomyces coelicolor mutant for the cell division gene ftsZ. Mol. Microbiol. 14:243254.
39. McCormick, J. R.,, and R. Losick. 1996. Cell division gene ftsQ is required for efficient sporulation but not growth and viability in Streptomyces coelicolor A3(2). J. Bacteriol. 178:52955301.
40. McVittie, A. M. 1974. Ultrastructural studies on sporulation in wild-type and white colony mutants of Streptomyces coelicolor. J. Gen. Microbiol. 81: 291302.
41. Miguélez, E. M.,, C. Martín,, M. B. Manzanal,, and C. Hardisson. 1992. Growth and morphogenesis in Streptomyces. FEMS Microbiol. Lett. 100: 351360.
42. Miguélez, E. M.,, M. García,, C. Hardisson,, and M. B. Manzanal. 1994. Autoradiographic study of hyphal growth during aerial mycelium development in Streptomyces antibioticus. J. Bacteriol. 176: 21052107.
43. Miwa, Y.,, and Y. Fujita. 1988. Purification and characterization of a repressor for the Bacillus subtilis gnt operon. J. Biol. Chem. 263:1325213257.
44. Nodwell, J.,, and R. Losick. Personal communication.
45. Nodwell, J. R.,, K. McGovern,, and R. Losick. 1996. An oligopeptide permease responsible for the import of an extracellular signal governing aerial mycelium formation in Streptomyces coelicolor. Mol. Microbiol. 22:881893.
46. Palacios, P.,, M. Vicente,, and M. Sanchez. 1996. Dependency of Escherichia coli cell-division size, and independency of nucleoid segregation on the mode and level of ftsZ expression. Mol. Microbiol. 20: 10931098.
47. Perego, M. 1998. Kinase-phosphatase competition regulates Bacillus subtilis development. Trends Microbiol. 6:366370.
48. Plaskitt, K. A.,, and K. F. Chater. 1995. Influences of developmental genes on localised glycogen deposition in colonics of a mycelial prokaryote, Streplomyces coelicolor A(3)2: a possible interface between metabolism and morphogenesis. Phil. Trans. R. Soc. B. 347:105121.
49. Potúčková, L.,, G. H. Kelemen,, K. C. Findlay,, M. A. Lonetto,, M.J. Buttner,, and J. Kormanec. 1995. A new RNA polymerase sigma factor, σF, is required for the late stages of morphological differentiation in Streptomyces spp. Mol. Microbiol. 17:3748.
50. Rezuchová, B.,, I. Barak,, and J. Kormanec. 1997. Disruption of a sigma factor gene, sigF, affects an intermediate stage of spore pigment production in Streptomyces aureofaciens. FEMS Microbiol. Lett. 153: 371377.
51. Rothfield, L. I.,, and S. S. Justice. 1997. Bacterial cell division: the cycle of the ring. Cell 88:581584.
52. Ryding, N. J.,, J. Ainsa,, and K. F. Chater. Unpublished data.
53. Ryding, N. J.,, G. H. Kelemen,, C. A. Whatling,, K. Flardh,, M. J. Buttner,, and K. F. Chater. 1998. A developmentally regulated gene encoding a repressor-like protein is essential for sporulation in Streptomyces coelicolor A3(2). Microbiology 29: 343357.
54. Ryding, N.J.,, M.J. Bibb,, V. Molle,, K. C. Findlay,, K. F. Chater,, and M.J. Buttner. 1999. New sporulation loci in Streptomyces coelicolor A3(2). J. Bacteriol. 181, in press.
55. Ryding, N.J.,, J. A. Aínsa,, N. Hartley,, C.J. Braton,, and K. F. Chater. Unpublished data.
56. Schneider, D.,, C. J. Bruton,, and K. F. Chater. Unpublished data.
57. Schwedock, J.,, J. R. McCormick,, E. R. Angert,, J. R. Nodwell,, and R. Losick. 1997. Assembly of the cell division protein FtsZ into ladder-like structures in the aerial hyphae of Streptomyces coelicolor. Mol. Microbiol. 25:847858.
58. Shahab, N.,, F. Flett,, S. G. Oliver,, and P. R. Butler. 1996. Growth rate control of protein and nucleic acid content in Streptomyces coelicolor A3(2) and Escherichia coli B/r. Microbiology 142:19271935.
59. Soliveri, J.,, K. L. Brown,, M. J. Buttner,, and K. F. Chater. Two promoters for the whiB sporulation gene of Streptomyces coelicolor A3(2), and their activities in relation to development. J. Bacteriol. 174:62156220.
60. Soliveri, J.,, C. Granozzi,, K. A. Plaskitt,, and K. F. Chater. 1993. Functional and evolutionary implications of a survey of various actinomycctes for homologues of two Streptomyces coelicolor sporulation genes. J. Gen. Microbiol. 139:25692578.
61. Soliveri, J. A.,, J. Gomez,, W. R. Bishai,, and K. F. Chater. Unpublished data.
62. Storz, G.,, and J. A. Imlay. 1999. Oxidative stress. Curr. Opin. Microbiol. 2:188194.
63. Tan, H.,, H. Yang,, Y. Tian,, W. Wu,, C. A. Whatling,, L. C. Chamberlin,, M.J. Buttner,, J. Nodwell,, and K. F. Chater. 1998. The Streptomyces coelicolor sporulation-specific σWhiG form of RNA polymerase transcribes a gene encoding a ProX-like protein that is dispensable for sporulation. Gene 212:137146.
64. Tillotson, R. D.,, H. A. B. Wösten,, M. Richter,, and J. M. Willey. 1998. A surface active protein involved in aerial mycelium formation in the filamentous fungus Schizophillum commune restores the capacity of a bald mutant of the filamentous bacterium Streptomyces coelicolor to erect aerial structures. Mol Microbiol. 30:595602.
65. Ward, J. E.Jr.,, and J. Lutkenhaus. 1985. Overproduction of FtsZ induces minicell formation in E. coli. Cell 42:941949.
66. Wheeler, R. T.,, and L. Shapiro. 1997. Bacterial chromosome segregation: is there a mitotic apparatus? Cell 88:577579.
67. Wildermuth, H.,, and D. A. Hopwood. 1970. Septation during sporulation in Streptomyces coelicolor. J. Gen. Microbiol. 60:5159.
68. Willey, J.,, R. Santamaría,, J. Guijarro,, M. Geistlich,, and R. Losick. 1991. Extracellular complementation of a developmental mutation implicates a small sporulation protein in aerial mycelium formation by Streptomyces coelicolor. Cell 65:641650.
69. Willey, J.,, J. Schwedock,, and R. Losick. 1993. Multiple extracellular signals govern the production of a morphogenetic protein involved in aerial mycelium formation by Streptomyces coelicolor. Genes Dev. 7:895903.
70. Yu, T.-W.,, Y. Shen,, R. McDaniel,, H. G. Floss,, C. Khosla,, D. A. Hopwood,, and B. S. Moore. 1998. Engineered biosynthesis of novel polyketides from Streptomyces spore pigment polyketide synthases, J. Am. Chem. Soc. 120:77497759.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error