Evidence for a DNA-relay mechanism in ParABS-mediated chromosome segregation
Hoong Chuin Lim,
Ivan Vladimirovich Surovtsev,
Bruno Gabriel Beltran,
Fang Huang,
Jörg Bewersdorf,
Christine Jacobs-Wagner
Affiliations
Hoong Chuin Lim
Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, United States; Microbial Diversity Institute, Yale University, West Haven, United States
Ivan Vladimirovich Surovtsev
Microbial Diversity Institute, Yale University, West Haven, United States; Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, United States; Howard Hughes Medical Institute, Yale University, New Haven, United States
Bruno Gabriel Beltran
Department of Mathematics, Louisiana State University, Baton Rouge, United States; Howard Hughes Medical Institute, Yale University, New Haven, United States
Fang Huang
Department of Cell Biology, Yale School of Medicine, New Haven, United States
Jörg Bewersdorf
Department of Cell Biology, Yale School of Medicine, New Haven, United States; Department of Biomedical Engineering, Yale University, New Haven, United States
Christine Jacobs-Wagner
Microbial Diversity Institute, Yale University, West Haven, United States; Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, United States; Howard Hughes Medical Institute, Yale University, New Haven, United States; Department of Microbial Pathogenesis, Yale School of Medicine, New Haven, United States
The widely conserved ParABS system plays a major role in bacterial chromosome segregation. How the components of this system work together to generate translocation force and directional motion remains uncertain. Here, we combine biochemical approaches, quantitative imaging and mathematical modeling to examine the mechanism by which ParA drives the translocation of the ParB/parS partition complex in Caulobacter crescentus. Our experiments, together with simulations grounded on experimentally-determined biochemical and cellular parameters, suggest a novel 'DNA-relay' mechanism in which the chromosome plays a mechanical function. In this model, DNA-bound ParA-ATP dimers serve as transient tethers that harness the elastic dynamics of the chromosome to relay the partition complex from one DNA region to another across a ParA-ATP dimer gradient. Since ParA-like proteins are implicated in the partitioning of various cytoplasmic cargos, the conservation of their DNA-binding activity suggests that the DNA-relay mechanism may be a general form of intracellular transport in bacteria.