Transient DNA Occupancy of the SMC Interarm Space in Prokaryotic Condensin

• Published in: Molecular cell Vol. 75; no. 2; pp. 209 - 223.e6
• Main Authors: Vazquez Nunez, Roberto, Ruiz Avila, Laura B., Gruber, Stephan
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 25.07.2019
• Subjects: Adenosine Triphosphatases - genetics; Adenosine Triphosphate - genetics; Bacillus subtilis - genetics; Bacterial Proteins - chemistry; Bacterial Proteins - genetics; Cell Cycle Proteins - chemistry; Cell Cycle Proteins - genetics; chromosome condensation; Chromosomes, Bacterial - genetics; cohesin; condensin; DNA - chemistry; DNA - genetics; DNA loop extrusion; DNA-Binding Proteins - chemistry; DNA-Binding Proteins - genetics; Hydrolysis; kleisin; MukB; Multiprotein Complexes - genetics; Nucleic Acid Conformation; Prokaryotic Cells - chemistry; Rad50; SMC; Smc5; SmcScpAB; SmcScpAB; Rad50; condensin; cohesin; kleisin; SMC; MukB; Smc5; chromosome condensation; DNA loop extrusion
• ISSN: 1097-2765; 1097-4164; 1097-4164
• DOI: 10.1016/j.molcel.2019.05.001

Multi-subunit SMC ATPases control chromosome superstructure and DNA topology, presumably by DNA translocation and loop extrusion. Chromosomal DNA is entrapped within the tripartite SMCkleisin ring. Juxtaposed SMC heads (“J heads”) or engaged SMC heads (“E heads”) split the SMCkleisin ring into “S” and “K” sub-compartments. Here, we map a DNA-binding interface to the S compartment of E heads SmcScpAB and show that head-DNA association is essential for efficient DNA translocation and for traversing highly transcribed genes in Bacillus subtilis. We demonstrate that in J heads, SmcScpAB chromosomal DNA resides in the K compartment but is absent from the S compartment. Our results imply that the DNA occupancy of the S compartment changes during the ATP hydrolysis cycle. We propose that DNA translocation involves DNA entry into and exit out of the S compartment, possibly by DNA transfer between compartments and DNA segment capture. [Display omitted] •Hinge-DNA association is dispensable for Smc function and DNA translocation•DNA association by engaged Smc heads is essential and supports translocation•DNA is excluded from the interarm space in J heads SmcScpAB•DNA transfer into and out of the interarm space may promote DNA translocation By mapping the location of chromosomal DNA in the bacterial SMC complex, Vazquez Nunez et al. reveal that juxtaposed heads exclude DNA from the interarm space. Transient DNA occupancy in the interarm space occurs through essential head-DNA association. DNA transfer into and out of the interarm space is proposed to promote DNA translocation.