Chromosome segregation in Archaea: SegA– and SegB–DNA complex structures provide insights into segrosome assembly

• Published in: Nucleic acids research 2021-12, Vol.49 (22), p.13150-13164
• Main Authors: Yen, Cheng-Yi, Lin, Min-Guan, Chen, Bo-Wei, Ng, Irene W, Read, Nicholas, Kabli, Azhar F, Wu, Che-Ting, Shen, Yo-You, Chen, Chen-Hao, Barillà, Daniela, Sun, Yuh-Ju, Hsiao, Chwan-Deng
• Format: Article
• Language: English
• Subjects: Adenosine Diphosphate - metabolism; Adenosine Triphosphatases - chemistry; Adenosine Triphosphatases - genetics; Adenosine Triphosphatases - metabolism; Adenosine Triphosphate - metabolism; Archaeal Proteins - chemistry; Archaeal Proteins - genetics; Archaeal Proteins - metabolism; Chromatin - genetics; Chromatin - metabolism; Chromatin - ultrastructure; Chromosome Segregation; Chromosomes, Archaeal - genetics; Crystallography, X-Ray; DNA, Archaeal - chemistry; DNA, Archaeal - genetics; DNA, Archaeal - metabolism; DNA-Binding Proteins - chemistry; DNA-Binding Proteins - genetics; DNA-Binding Proteins - metabolism; Microscopy, Electron; Models, Molecular; Multiprotein Complexes - chemistry; Multiprotein Complexes - metabolism; Multiprotein Complexes - ultrastructure; Mutation; Nucleic Acid Conformation; Protein Binding; Protein Conformation; Structural Biology; Sulfolobus solfataricus - genetics; Sulfolobus solfataricus - metabolism
• ISSN: 0305-1048; 1362-4962
• DOI: 10.1093/nar/gkab1155

Abstract Genome segregation is a vital process in all organisms. Chromosome partitioning remains obscure in Archaea, the third domain of life. Here, we investigated the SegAB system from Sulfolobus solfataricus. SegA is a ParA Walker-type ATPase and SegB is a site-specific DNA-binding protein. We determined the structures of both proteins and those of SegA–DNA and SegB–DNA complexes. The SegA structure revealed an atypical, novel non-sandwich dimer that binds DNA either in the presence or in the absence of ATP. The SegB structure disclosed a ribbon–helix–helix motif through which the protein binds DNA site specifically. The association of multiple interacting SegB dimers with the DNA results in a higher order chromatin-like structure. The unstructured SegB N-terminus plays an essential catalytic role in stimulating SegA ATPase activity and an architectural regulatory role in segrosome (SegA–SegB–DNA) formation. Electron microscopy results also provide a compact ring-like segrosome structure related to chromosome organization. These findings contribute a novel mechanistic perspective on archaeal chromosome segregation.