Expression of the division-controlling gene ftsZ during growth and sporulation of the filamentous bacterium Streptomyces griseus

Dharmatilake, Amitha J.; Kendrick, Kathleen E.

doi:10.1016/0378-1119(94)90034-5

Cited by 25 publications

(23 citation statements)

References 42 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Plasmids from these strains were transformed back into E. coli and analyzed. Plasmids from the small-colony strains had the same restriction digestion pattern as the wild type, while those from the large- (28) from which the central nonconserved domain has been removed (residues 320 to 526); Wol, a Wolbachia species (17); Bsu, B. subtilis (2); Sgr, S. griseus (12); Ana, an Anabaena sp., residues 50 to 428 (13) colony strain were rearranged in their insert portion so that several diagnostic SalI fragments internal to ftsZ were missing (data not shown). This strongly suggests that the large-colony strain carries a plasmid, designated pRW13, with an inactivated ftsZ gene.…”

Section: Resultsmentioning

confidence: 99%

Isolation of an ftsZ homolog from the archaebacterium Halobacterium salinarium: implications for the evolution of FtsZ and tubulin

Margolin¹,

Wang²,

Kumar³

1996

J Bacteriol

108

View full text Add to dashboard Cite

We have isolated a homolog of the cell division gene ftsZ from the extremely halophilic archaebacterium Halobacterium salinarium. The predicted protein of 39 kDa is divergent relative to eubacterial homologs, with 32% identity to Escherichia coli FtsZ. No other eubacterial cell division gene homologs were found adjacent to H. salinarium ftsZ. Expression of the ftsZ gene region in H. salinarium induced significant morphological changes leading to the loss of rod shape. Phylogenetic analysis demonstrated that the H. salinarium FtsZ protein is more related to tubulins than are the FtsZ proteins of eubacteria, supporting the hypothesis that FtsZ may have evolved into eukaryotic tubulin.FtsZ is an essential cell division protein in Escherichia coli and Bacillus subtilis (3, 9) and appears to be conserved among eubacteria (8). It polymerizes to form a circumferential ring at the division site, constricting at the leading edge of the invaginating septum that will eventually separate the two daughter cells (6,26). FtsZ both shares biochemical properties with and has structural similarities to eukaryotic tubulins. Both bind and hydrolyze GTP, polymerize to form tubules in a GTP-dependent manner, and are involved in cytoskeletal processes in the cell during cell division (7,10,31,32,37). All identified FtsZ proteins from eubacteria contain a conserved N terminus that carries the tubulin-like GTP-binding motif and a hydrophilic, variable C terminus.Although the role of FtsZ in cytokinesis differs from the actin-mediated cytokinesis in eukaryotic cells, the biochemical and amino acid sequence data have led to the proposal that FtsZ is a prokaryotic version of tubulin (14). Since the origins of the eukaryotic cytoskeleton are unknown, an intriguing hypothesis is that FtsZ evolved into tubulin. Since it is believed that the archaea and eucarya diverged after the divergence of archaea from bacteria, then identification of an FtsZ protein in an archaebacterial species might shed light on this evolutionary question (18,21). Because archaebacteria in general have a prokaryotic cellular organization similar to that of eubacteria, it is reasonable to propose that their cell division requires an FtsZ homolog derived from the common ancestor of all living cells (44).To gain insight into FtsZ evolution and diversity, we have isolated and determined the nucleotide sequence of an ftsZ gene from the extremely halophilic archaebacterium Halobacterium salinarium, which grows as long, rod-shaped cells. We show that H. salinarium ftsZ is remarkably similar to the eubacterial versions, particularly in the region most similar to tubulins. An alignment of the H. salinarium FtsZ sequence with those of eubacterial FtsZ proteins and tubulins suggests that H. salinarium FtsZ is more related to tubulin than are the eubacterial FtsZs, supporting the idea that tubulin may have evolved from FtsZ. We also show that H. salinarium ftsZ is not flanked by genes normally found adjacent to several known eubacterial ftsZ genes. Finally, we show that expression...

show abstract

Section: Resultsmentioning

confidence: 99%

Isolation of an ftsZ homolog from the archaebacterium Halobacterium salinarium: implications for the evolution of FtsZ and tubulin

Margolin¹,

Wang²,

Kumar³

1996

J Bacteriol

108

View full text Add to dashboard Cite

show abstract

“…FtsZ is a tubulin-like protein that polymerizes in a GTP-dependent manner to form a ring at the site of incipient septation (de Boer et al, 1992;RayChaudhuri and Park, 1992;Bramhill and Thompson, 1994;Mukherjee and Lutkenhaus, 1994). It plays a pivotal role in the process of cytokinesis in bacteria, and homologues of FtsZ have been found in all prokaryotes that have been investigated for its presence (Lutkenhaus, 1993;Dharmatilake and Kendrick, 1994;McCormick et al, 1994;Baumann and Jackson, 1996;Bult et al, 1996;Margolin et al, 1996;Quardokus et al, 1996;Wang and Lutkenhaus, 1996).…”

Section: Introductionmentioning

confidence: 99%

Assembly of the cell division protein FtsZ into ladder‐like structures in the aerial hyphae of Streptomyces coelicolor

Schwedock

McCormick

Angert

et al. 1997

Molecular Microbiology

131

134

View full text Add to dashboard Cite

SummaryIn the filamentous bacterium Streptomyces coelicolor, the cell division protein FtsZ is required for the conversion of multinucleoidal aerial hyphae into chains of uninucleoidal spores, although it is not essential for viability. Using immunofluorescence microscopy, we have shown that FtsZ assembles into long, regularly spaced, ladder-like arrays in developing aerial hyphae, with an average spacing of about 1.3 m. Within individual hyphae, ladder formation was relatively synchronous and extended for distances over 100 m. These ladders were present only transiently, decreasing in intensity as chromosomes separated into distinct nucleoids and disappearing upon the completion of septum formation. Evidence from the overall intensity of immunofluorescence staining suggested that ladder formation was regulated in part at the level of the accumulation and degradation of FtsZ within individual aerial hyphae. Finally, FtsZ ladder formation was under developmental control in that long arrays of FtsZ rings could not be detected in certain so-called white mutants (whiG, whiH and whiB ), which are blocked in spore formation. The assembly of FtsZ into ladders represents the earliest known molecular manifestation of the process of spore formation, and its discovery provides insight into the role of whi genes in the conversion of aerial hyphae into chains of spores. We have also described a novel use of a cell wall-staining technique to visualize apical tip growth in vegetatively growing hyphae.

show abstract

“…Moreover, the response regulator YycF of the YycG/YycF two-component system binds directly to the nonessential P1 promoter upstream of ftsAZ and activates transcription of the gene (21, 30). In Streptomyces, among the three ftsZ promoters present in the ftsQ-ftsZ intergenic region, one promoter is constitutively active, the second one is active during vegetative growth, and the third one is active during sporulation (11,19,33,41).A minor sporulation-specific ftsZ transcript was detected from the ftsQ open reading frame (ORF) in Streptomyces griseus (11,33) and in Streptomyces coelicolor (19,39). In Corynebacterium glutamicum ATCC 13869 (Brevibacterium lactofermentum), there is a less abundant short transcript originating from the ftsQ-ftsZ intergenic region and a more abundant transcript starting inside ftsQ (29,42).…”

mentioning

confidence: 99%

mentioning

confidence: 99%

“…A minor sporulation-specific ftsZ transcript was detected from the ftsQ open reading frame (ORF) in Streptomyces griseus (11,33) and in Streptomyces coelicolor (19,39). In Corynebacterium glutamicum ATCC 13869 (Brevibacterium lactofermentum), there is a less abundant short transcript originating from the ftsQ-ftsZ intergenic region and a more abundant transcript starting inside ftsQ (29,42).…”

mentioning

confidence: 99%

See 1 more Smart Citation

Transcriptional Analysis of the Principal Cell Division Gene, ftsZ , of Mycobacterium tuberculosis

Roy

Ajitkumar

2005

J Bacteriol

View full text Add to dashboard Cite

Bacterial cell division is a tightly regulated process that involves spatial and temporal control of the replication and segregation of the chromosome (karyokinesis) and cytoplasmic division of the cell (cytokinesis) (12,27,37). The principal cell division protein FtsZ initiates septation through polymerization to form a ring-like structure at the leading edge of the invaginating septum to guide cytokinesis (1,5,27,37). Although the function of FtsZ seems to be similar in all bacterial cells, transcriptional regulation of the gene differs remarkably, apparently in compliance with the physiological demands and growth conditions of different bacterial genera and species. In Escherichia coli, six promoters distributed in the upstream ftsQ, ftsA, and ddlB coding sequences drive one-third of the total ftsQAZ transcripts. The remaining two-thirds of ftsZ transcription is driven by promoters that are placed beyond 6 kb upstream of ddlB gene (10,18,40). Some of these promoters are upregulated by protein factors, such as SdiA, which regulates the ftsQ2p promoter (46), and the response regulator RcsB, which regulates the ftsA1p promoter (8, 22). Like for E. coli, the presence of multiple promoters for ftsZ has been reported for Bartonella bacilliformis and Bartonella henselae (17), Shewanella violacea (31), Neisseria gonorrhoeae (20), and Thermoplasma acidophilum (48). However, in the differentiating bacterium Caulobacter crescentus, monocistronic ftsZ is driven by a single promoter under the control of the global cell cycle regulator CtrA (32). In Bacillus subtilis, where the organization of the genes in the dcw cluster is similar to that in E. coli, among the three promoters that drive ftsA-ftsZ cotranscription, two are active during vegetative growth (SigA dependent) and one is active during sporulation (SigH dependent) (24). Moreover, the response regulator YycF of the YycG/YycF two-component system binds directly to the nonessential P1 promoter upstream of ftsAZ and activates transcription of the gene (21, 30). In Streptomyces, among the three ftsZ promoters present in the ftsQ-ftsZ intergenic region, one promoter is constitutively active, the second one is active during vegetative growth, and the third one is active during sporulation (11,19,33,41).A minor sporulation-specific ftsZ transcript was detected from the ftsQ open reading frame (ORF) in Streptomyces griseus (11,33) and in Streptomyces coelicolor (19,39). In Corynebacterium glutamicum ATCC 13869 (Brevibacterium lactofermentum), there is a less abundant short transcript originating from the ftsQ-ftsZ intergenic region and a more abundant transcript starting inside ftsQ (29,42).Mycobacterium tuberculosis, which is a member of the lower Actinomycetes group and is similar to Corynebacterium and Streptomyces, is known to shut down its proliferation inside activated macrophages (34,35). Similarly, proliferation of the pathogen is arrested at a uniform stage of the cell cycle when the cell enters the state of dormancy and is resumed when the cell comes out of dorm...

show abstract

Expression of the division-controlling gene ftsZ during growth and sporulation of the filamentous bacterium Streptomyces griseus

Cited by 25 publications

References 42 publications

Isolation of an ftsZ homolog from the archaebacterium Halobacterium salinarium: implications for the evolution of FtsZ and tubulin

Isolation of an ftsZ homolog from the archaebacterium Halobacterium salinarium: implications for the evolution of FtsZ and tubulin

Assembly of the cell division protein FtsZ into ladder‐like structures in the aerial hyphae of Streptomyces coelicolor

Transcriptional Analysis of the Principal Cell Division Gene, ftsZ , of Mycobacterium tuberculosis

Contact Info

Product

Resources

About