Differential Regulation of ftsZ Transcription during Septation of Streptomyces griseus

Abstract

Streptomyces has been known to form two types of septa. The data in this research demonstrated that Streptomyces griseus forms another type of septum near the base of sporogenic hyphae (basal septum). To understand the regulation of the septation machinery in S. griseus, we investigated the expression of the ftsZ gene. S1 nuclease protection assays revealed that four ftsZ transcripts were differentially expressed during morphological differentiation. The vegetative transcript (emanating from P veg ) is present at a moderate level during vegetative growth, but is switched off within the first 2 h of sporulation. Two sporulation-specific transcripts predominantly accumulated, and the levels increased by approximately fivefold together shortly before sporulation septa begin to form. Consistently, the sporulation-specific transcripts were expressed much earlier and more abundantly in a group of nonsporulating mutants that form their sporulation septa prematurely. Promoter-probe studies with two different reporter systems confirmed the activities of the putative promoters identified from the 5 end point of the transcripts. The levels and expression timing of promoter activities were consistent with the results of nuclease protection assays. The aseptate phenotype of the P spo mutant indicated that the increased transcription from P spo is required for sporulation septation, but not for vegetative or basal septum formation.The early discernible event in bacterial cell division is the involvement of FtsZ, which governs the localization of septum formation. ftsZ is present in all bacteria so far examined, including wall-less bacteria (55), as well as in archaea (34, 56) and plastids of Arabidopsis (42). FtsZ forms the leading edge of the cell division septum by migrating from random cytoplasmic locations to the internal face of the cell membrane at the division plane, where FtsZ polymerizes into a ring structure (7). In Escherichia coli, the Min proteins appear to permit this ring structure to form at the center of the cell rather than at either pole (12). In Bacillus subtilis, ftsZ is required for both binary fission and asymmetric septation (6). Sharing some structural and biochemical properties with the eucaryotic cytoskeletal protein tubulin, FtsZ possesses GTPase activity (11,40,46). Interaction of FtsZ with GTP appears to be necessary for polymerization in vitro (9, 41). The inward growth of the division septum is presumably accompanied by the controlled depolymerization of the FtsZ ring, the appositional sliding of polymeric subunits (9), or a profound change in the ring architecture.Although the role of FtsZ appears to be similar in procaryotes, the pattern of synthesis of FtsZ differs, apparently in compliance with the physiological demands of each species. The level of FtsZ from Caulobacter crescentus varies in concert with the division cycle; FtsZ reaches a maximal level in predivisional cells and is absent from swarmer cells, in which FtsZ appears to be specifically degraded (45). In E. coli, FtsZ is present...

Dynamics of FtsZ Assembly during Sporulation in Streptomyces coelicolor A3(2)

“…We suggest that such a septum demarcates the compartment in which sporulation septation later commences with a significantly increased expression of FtsZ, as judged by the increase in the fluorescent signal from FtsZ-EGFP. The latter observation is in agreement with the developmentally controlled induction of ftsZ transcription in sporogenic hyphae (15,30). The rise in the cytoplasmic concentration of FtsZ leads to the initiation of assembly into spiral-shaped filaments (Fig.…”

“…The process may start with the placement of a Z ring and a basal septum in the distal part of the sporogenic hypha (stage A). For S. griseus, it has been suggested that the sporogenic cells are delimited at the base by a specialized septum, different from both vegetative cross walls and sporulation septa (30). No direct equivalent has been observed in S. coelicolor.…”

“…The developmental control of this synchronous cell division involves a sporulation-specific up-regulation of ftsZ expression in sporogenic hyphae in both S. coelicolor and Streptomyces griseus (15,30). This occurred at one specific promoter and depended on a set of regulators of early stages of sporulationthe whiA, whiB, whiG, whiH, whiI, and whiJ genes (15).…”

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

“…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).…”

“…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).…”