FtsW Is a Dispensable Cell Division Protein Required for Z-Ring Stabilization during Sporulation Septation in Streptomyces coelicolor

Abstract

The conserved rodA and ftsW genes encode polytopic membrane proteins that are essential for bacterial cell elongation and division, respectively, and each gene is invariably linked with a cognate class B high-molecularweight penicillin-binding protein (HMW PBP) gene. Filamentous differentiating Streptomyces coelicolor possesses four such gene pairs. Whereas rodA, although not its cognate HMW PBP gene, is essential in these bacteria, mutation of SCO5302 or SCO2607 (sfr) caused no gross changes to growth and septation. In contrast, disruption of either ftsW or the cognate ftsI gene blocked the formation of sporulation septa in aerial hyphae. The inability of spiral polymers of FtsZ to reorganize into rings in aerial hyphae of these mutants indicates an early pivotal role of an FtsW-FtsI complex in cell division. Concerted assembly of the complete divisome was unnecessary for Z-ring stabilization in aerial hyphae as ftsQ mutants were found to be blocked at a later stage in cell division, during septum closure. Complete cross wall formation occurred in vegetative hyphae in all three fts mutants, indicating that the typical bacterial divisome functions specifically during nonessential sporulation septation, providing a unique opportunity to interrogate the function and dependencies of individual components of the divisome in vivo.Gram-positive Streptomyces spp. are actinomycetes that typically inhabit terrestrial soils and marine sediments as freeliving saprophytes. In a manner similar to that of a filamentous fungus, a streptomycete colonizes its particulate environment by growing branching multigenomic hyphae that form a ramifying network, enabling the organism to exploit a localized nutrient source. Being nonmotile, they achieve dispersal by means of unigenomic spores borne on specialized nonfeeding aerial hyphae. The latter grow out of the semiaqueous environment inhabited by the feeding vegetative hyphae of terrestrial streptomycetes and ultimately undergo multiple coordinated cell divisions, generating chains of spores. The spores can then be dispersed by physical agents or the activities of motile animals inhabiting the same niche.Streptomyces spp. grow by hyphal tip extension and subapical branching. Most de novo cell wall synthesis is at the tips, rather than by insertion of new murein into the lateral walls (19). Cross wall formation in the feeding substrate hyphae is relatively infrequent and a subapical cell separated from the tip compartment by such a cross wall can only grow once it has created a new tip by lateral branching. Tip growth contrasts markedly to the paradigm in rod-shaped bacteria such as Escherichia coli and Bacillus subtilis, which grow by intercalation of new murein into lateral walls, not into the cell wall surrounding the poles: the cell wall material of polar caps is inert after its initial synthesis during cell division (10). The mechanism for apical extension of Streptomyces hyphae is unclear. One important component of an apical protein complex has been identified: DivIVA. This pro...

Taxonomy, Physiology, and Natural Products of Actinobacteria

“…While the ftsZ mutant also fails to make cross-walls, most of the other cell division mutants are only defective in sporulation-specific cell division (278,(290)(291)(292)(293)). This illustrates a major difference between vegetative and aerial cell division.…”

Medium-Dependent Phenotypes of Streptomyces coelicolor with Mutations in ftsI or ftsW

“…Thus, assignments for ftsW Sc and ftsI Sc are based on sequence similarity and synteny in the dcw cluster, as well as on mutant phenotypes like those of S. coelicolor ftsL and divIC mutants (2). A similar analysis of the same genes was concurrently reported (14).…”

“…3D, E, and G). Complete cross-walls were reported in a concurrent study of ftsI and ftsW mutants (14). However, those observations were done with cells grown on a very unusual choice of medium for Streptomyces (2ϫ yeast-tryptone [YT] medium), and perhaps the salt concentration may have affected the observed phenotypes.…”

Plant growth promotion by streptomycetes: ecophysiology, mechanisms and applications

“…The growth of Streptomyces involves hyphal tip extension and sub-apical branching [39]. Unlike the process in rod-shaped bacteria where cytokinesis is based on building a cross wall by depositing murein into lateral walls, Streptomyces growth occurs by hyphae production at the cell pole [37].…”