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Chapter 2 : Developmental Decisions during Sporulation in the Aerial Mycelium in Streptomyces
Author:
Keith F. Chater1
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Affiliations:
1: Department of Genetics, John Innes Centre, Norwich Research Park, Colney, Norwich, NR4 7UH, United Kingdom
Content Type: Monograph
Publication Year:
2000
Category: Microbial Genetics and Molecular Biology
Book DOI:
10.1128/9781555818166
Chapter DOI:
10.1128/9781555818166.ch2
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Developmental Decisions during Sporulation in the Aerial Mycelium in Streptomyces, Page 1 of 2
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Abstract:
This chapter deals with an unusual bacterial example involving growth into the air: the formation and metamorphosis of reproductive aerial hyphae in Streptomyces 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 Streptomyces 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
Figures
Developmental Decisions during Sporulation in the Aerial Mycelium in Streptomyces
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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
/content/10.1128/9781555818166.chap2.fig2-1
FIGURE 2
Spore chains and hyphal filaments on the surface of a Streptomyces colony. (Reproduced from Chater, 1998 , with permission.)
10.1128/9781555818166/fig2-1_thmb.gif
10.1128/9781555818166/fig2-1.gif
FIGURE 2
Spore chains and hyphal filaments on the surface of a Streptomyces colony. (Reproduced from Chater, 1998 , 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
/content/10.1128/9781555818166.chap2.fig2-2
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.
10.1128/9781555818166/fig2-2_thmb.gif
10.1128/9781555818166/fig2-2.gif
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
/content/10.1128/9781555818166.chap2.fig2-3
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 Flärdh et al., in press , with permission.)
10.1128/9781555818166/fig2-3_thmb.gif
10.1128/9781555818166/fig2-3.gif
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 Flärdh et al., in press , 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
/content/10.1128/9781555818166.chap2.fig2-4
FIGURE 4
Speculative model implicating Whi proteins in developmental decisions. It is proposed that initially σWhiG is held in an inactive state, but a signal produced while young aerial hyphae are early in growth releases active σWhiG (1). Among the σWhiG 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 Flärdh et al., in press , with permission.)
10.1128/9781555818166/fig2-4_thmb.gif
10.1128/9781555818166/fig2-4.gif
FIGURE 4
Speculative model implicating Whi proteins in developmental decisions. It is proposed that initially σWhiG is held in an inactive state, but a signal produced while young aerial hyphae are early in growth releases active σWhiG (1). Among the σWhiG 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 Flärdh et al., in press , 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
/content/10.1128/9781555818166.chap2.fig2-5
FIGURE 5
The long, often tightly coiled aerial hyphae of a whiB disruption mutant. (Scanning electron micrograph kindly provided by K. Findlay and K. Flärdh.)
10.1128/9781555818166/fig2-5_thmb.gif
10.1128/9781555818166/fig2-5.gif
FIGURE 5
The long, often tightly coiled aerial hyphae of a whiB 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
/content/10.1128/9781555818166.chap2.fig2-6
FIGURE 6
Transcriptional dependencies of whi genes. This scheme combines results from Kelemen et al. ( 1996 , 1998 ), Ryding et al. (1998) , and Ainsa et al. (in press) . (Drawing provided by J. Aínsa.)
10.1128/9781555818166/fig2-6_thmb.gif
10.1128/9781555818166/fig2-6.gif
FIGURE 6
Transcriptional dependencies of whi genes. This scheme combines results from Kelemen et al. ( 1996 , 1998 ), Ryding et al. (1998) , and Ainsa et al. (in press) . (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
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