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Polyploidy, regular patterning of genome copies, and unusual control of DNA partitioning in the Lyme disease spirochete

Author

Listed:
  • Constantin N. Takacs

    (Stanford University
    Stanford University
    The Howard Hughes Medical Institute)

  • Jenny Wachter

    (National Institutes of Health
    University of Saskatchewan)

  • Yingjie Xiang

    (Yale University
    Microbial Sciences Institute, Yale West Campus)

  • Zhongqing Ren

    (Indiana University)

  • Xheni Karaboja

    (Indiana University)

  • Molly Scott

    (Microbial Sciences Institute, Yale West Campus
    Yale University)

  • Matthew R. Stoner

    (The Howard Hughes Medical Institute
    Microbial Sciences Institute, Yale West Campus
    Yale University)

  • Irnov Irnov

    (Stanford University
    Stanford University
    The Howard Hughes Medical Institute)

  • Nicholas Jannetty

    (The Howard Hughes Medical Institute
    Microbial Sciences Institute, Yale West Campus
    Yale University)

  • Patricia A. Rosa

    (National Institutes of Health)

  • Xindan Wang

    (Indiana University)

  • Christine Jacobs-Wagner

    (Stanford University
    Stanford University
    The Howard Hughes Medical Institute)

Abstract

Borrelia burgdorferi, the tick-transmitted spirochete agent of Lyme disease, has a highly segmented genome with a linear chromosome and various linear or circular plasmids. Here, by imaging several chromosomal loci and 16 distinct plasmids, we show that B. burgdorferi is polyploid during growth in culture and that the number of genome copies decreases during stationary phase. B. burgdorferi is also polyploid inside fed ticks and chromosome copies are regularly spaced along the spirochete’s length in both growing cultures and ticks. This patterning involves the conserved DNA partitioning protein ParA whose localization is controlled by a potentially phage-derived protein, ParZ, instead of its usual partner ParB. ParZ binds its own coding region and acts as a centromere-binding protein. While ParA works with ParZ, ParB controls the localization of the condensin, SMC. Together, the ParA/ParZ and ParB/SMC pairs ensure faithful chromosome inheritance. Our findings underscore the plasticity of cellular functions, even those as fundamental as chromosome segregation.

Suggested Citation

  • Constantin N. Takacs & Jenny Wachter & Yingjie Xiang & Zhongqing Ren & Xheni Karaboja & Molly Scott & Matthew R. Stoner & Irnov Irnov & Nicholas Jannetty & Patricia A. Rosa & Xindan Wang & Christine J, 2022. "Polyploidy, regular patterning of genome copies, and unusual control of DNA partitioning in the Lyme disease spirochete," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34876-4
    DOI: 10.1038/s41467-022-34876-4
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    References listed on IDEAS

    as
    1. Kati Böhm & Giacomo Giacomelli & Andreas Schmidt & Axel Imhof & Romain Koszul & Martial Marbouty & Marc Bramkamp, 2020. "Chromosome organization by a conserved condensin-ParB system in the actinobacterium Corynebacterium glutamicum," Nature Communications, Nature, vol. 11(1), pages 1-17, December.
    2. Claire M. Fraser & Sherwood Casjens & Wai Mun Huang & Granger G. Sutton & Rebecca Clayton & Raju Lathigra & Owen White & Karen A. Ketchum & Robert Dodson & Erin K. Hickey & Michelle Gwinn & Brian Doug, 1997. "Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi," Nature, Nature, vol. 390(6660), pages 580-586, December.
    3. Antoine Le Gall & Diego I. Cattoni & Baptiste Guilhas & Céline Mathieu-Demazière & Laura Oudjedi & Jean-Bernard Fiche & Jérôme Rech & Sara Abrahamsson & Heath Murray & Jean-Yves Bouet & Marcelo Nollma, 2016. "Bacterial partition complexes segregate within the volume of the nucleoid," Nature Communications, Nature, vol. 7(1), pages 1-10, November.
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