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Research Article

Bacillus subtilis chromosome organization oscillates between two distinct patterns

Xindan Wang, Paula Montero Llopis, and David Z. Rudner
PNAS September 2, 2014 111 (35) 12877-12882; first published July 28, 2014; https://doi.org/10.1073/pnas.1407461111
Xindan Wang
Department of Microbiology and Immunobiology, Harvard Medical School, Boston, MA 02115
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Paula Montero Llopis
Department of Microbiology and Immunobiology, Harvard Medical School, Boston, MA 02115
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David Z. Rudner
Department of Microbiology and Immunobiology, Harvard Medical School, Boston, MA 02115
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  • For correspondence: rudner@hms.harvard.edu
  1. Edited by Sharon R. Long, Stanford University, Stanford, CA, and approved July 2, 2014 (received for review April 23, 2014)

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Significance

In bacteria, faithful and efficient DNA segregation is intimately linked to the spatial organization of the chromosome. Two distinct organization patterns have been described for bacterial chromosomes (ori-ter and left-ori-right) that appear to arise from distinct segregation mechanisms. Here, we show that the Bacillus subtilis chromosome oscillates between them during a replication–segregation cycle. Our data further suggest that the highly conserved condensin complex and the parABS partitioning system function as the core components that underlie these alternating patterns. We propose that this oscillatory cycle enhances the efficiency of DNA replication and sister chromosome segregation and provides a unifying model for the diverse patterns of chromosome organization observed in bacteria.

Abstract

Bacterial chromosomes have been found to possess one of two distinct patterns of spatial organization. In the first, called “ori-ter” and exemplified by Caulobacter crescentus, the chromosome arms lie side-by-side, with the replication origin and terminus at opposite cell poles. In the second, observed in slow-growing Escherichia coli (“left-ori-right”), the two chromosome arms reside in separate cell halves, on either side of a centrally located origin. These two patterns, rotated 90° relative to each other, appear to result from different segregation mechanisms. Here, we show that the Bacillus subtilis chromosome alternates between them. For most of the cell cycle, newly replicated origins are maintained at opposite poles with chromosome arms adjacent to each other, in an ori-ter configuration. Shortly after replication initiation, the duplicated origins move as a unit to midcell and the two unreplicated arms resolve into opposite cell halves, generating a left-ori-right pattern. The origins are then actively segregated toward opposite poles, resetting the cycle. Our data suggest that the condensin complex and the parABS partitioning system are the principal driving forces underlying this oscillatory cycle. We propose that the distinct organization patterns observed for bacterial chromosomes reflect a common organization–segregation mechanism, and that simple modifications to it underlie the unique patterns observed in different species.

  • DNA replication
  • ParA
  • chromosome segregation
  • SMC condensin

Footnotes

  • ↵1To whom correspondence should be addressed. Email: rudner{at}hms.harvard.edu.
  • Author contributions: X.W. and D.Z.R. designed research; X.W. performed research; X.W. and P.M.L. contributed new reagents/analytic tools; X.W. and D.Z.R. analyzed data; and X.W. and D.Z.R. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • See Commentary on page 12580.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1407461111/-/DCSupplemental.

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Oscillating chromosome organization patterns
Xindan Wang, Paula Montero Llopis, David Z. Rudner
Proceedings of the National Academy of Sciences Sep 2014, 111 (35) 12877-12882; DOI: 10.1073/pnas.1407461111

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Oscillating chromosome organization patterns
Xindan Wang, Paula Montero Llopis, David Z. Rudner
Proceedings of the National Academy of Sciences Sep 2014, 111 (35) 12877-12882; DOI: 10.1073/pnas.1407461111
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