SlmA, a Nucleoid-Associated, FtsZ Binding Protein Required for Blocking Septal Ring Assembly over Chromosomes in E. coli

Abstract

Cell division in Escherichia coli begins with assembly of the tubulin-like FtsZ protein into a ring structure just underneath the cell membrane. Spatial control over Z ring assembly is achieved by two partially redundant negative regulatory systems, the Min system and nucleoid occlusion (NO), which cooperate to position the division site at midcell. In contrast to the well-studied Min system, almost nothing is known about how Z ring assembly is blocked in the vicinity of nucleoids to effect NO. Reasoning that Min function might become essential in cells impaired for NO, we screened for mutations synthetically lethal with a defective Min system (slm mutants). By using this approach, we identified SlmA (Ttk) as the first NO factor in E. coli. Our combined genetic, cytological, and biochemical results suggest that SlmA is a DNA-associated division inhibitor that is directly involved in preventing Z ring assembly on portions of the membrane surrounding the nucleoid.

In the Beginning, Escherichia coli Assembled the Proto-ring: An Initial Phase of Division

“…Nucleoid occlusion blocks septation across the nucleoid, therefore excluding a potentially harmful guillotine effect on the chromosome. In E. coli, it is accomplished by SlmA, a DNA-associated division inhibitor directly involved in preventing FtsZ polymerization in the vicinity of the nucleoid (12). A dimer of SlmA binds simultaneously to two molecules of FtsZ and to specific DNA sequences distributed all over the chromosome except at the Ter region.…”

Evidence That Bacteriophage λ Kil Peptide Inhibits Bacterial Cell Division by Disrupting FtsZ Protofilaments and Sequestering Protein Subunits

“…All published studies agree that MinC does not modify FtsZ GTPase activity (17,21). Nucleoid occlusion is mediated by SlmA, a sequence-specific DNA-binding protein that interferes with FtsZ assembly preventing Z-ring formation in the vicinity of the nucleoid (22). This protein forms an active dimer of dimers complex with the DNA (23) that blocks FtsZ assembly (24,25).…”

Modeling Three-Dimensional Spatial Regulation of Bacterial Cell Division (Dissertation)

“…Although the protein can diffuse over the entire membrane, nucleoid occlusion prevents the polymerization from taking place over the nucleoid mass, leaving only the midcell and the two cell poles as viable locations for polymerization (Woldringh et al, 1990(Woldringh et al, , 1991Bernhardt and de Boer, 2005).…”

“…The rod-shaped bacterium begins to divide when the tubulin-homolog FtsZ, polymerizes into a constricting annular structure (Z-ring) on the inner membrane (Adams and Errington, 2009;Lutkenhaus, 2007). To ensure equal distribution of cell contents to the two progeny cells, the constriction site is restricted to the middle of the cell long axis by two mechanisms: (i) nucleoid occlusion, which allows the Z-ring to assemble only at the midcell and the cell poles, locations that are devoid of the nucleoid mass (Woldringh et al, 1990(Woldringh et al, , 1991Bernhardt and de Boer, 2005), and (ii) carefully orchestrated RD of the minB operon encoded proteins, MinC, MinD, and MinE, in the cytoplasm and inner membrane, which suppresses polar Z-rings to avoid the minicelling phenotype (Lutkenhaus, 2007;Vats et al, 2009). The phenotype is characterized by the formation of chromosomeless minicells by polar septation and elongated cells with multiple chromosomes.…”