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Membrane fission during bacterial spore development requires DNA-driven cellular inflation

Ane Landajuela, Martha Braun, Alejandro Martínez-Calvo, Christopher D. A. Rodrigues, Thierry Doan, David Z. Rudner, View ORCID ProfileNed S. Wingreen, View ORCID ProfileErdem Karatekin
doi: https://doi.org/10.1101/2021.10.08.463650
Ane Landajuela
1Cellular and Molecular Physiology, Yale University, New Haven, CT, USA
2Nanobiology Institute, Yale University, West Haven, CT, USA
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  • For correspondence: ane.landajuela@yale.edu matha.braun@yale.edu erdem.karatekin@yale.edu
Martha Braun
2Nanobiology Institute, Yale University, West Haven, CT, USA
3Molecular Biophysics and Biochemistry, Yale University, New Haven, CT, USA
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  • For correspondence: ane.landajuela@yale.edu matha.braun@yale.edu erdem.karatekin@yale.edu
Alejandro Martínez-Calvo
4Grupo de Mecánica de Fluidos, Universidad Carlos III de Madrid, Spain
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Christopher D. A. Rodrigues
5iThree Institute, University of Technology Sydney (UTS), Australia
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Thierry Doan
6Laboratoire d’Ingénierie des Systèmes Macromoléculaires, Aix-Marseille Université - CNRS UMR7255, Marseilles, France
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David Z. Rudner
7Department of Microbiology, Harvard Medical School, Boston, Massachusetts,USA
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Ned S. Wingreen
8Department of Molecular Biology, Princeton University, Princeton, NJ 08544, USA
9Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, NJ 08544, USA
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  • ORCID record for Ned S. Wingreen
Erdem Karatekin
1Cellular and Molecular Physiology, Yale University, New Haven, CT, USA
2Nanobiology Institute, Yale University, West Haven, CT, USA
3Molecular Biophysics and Biochemistry, Yale University, New Haven, CT, USA
10Université de Paris, SPPIN - Saints-Pères Paris Institute for the Neurosciences, Centre National de la Recherche Scientifique (CNRS), F-75006 Paris, France
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  • ORCID record for Erdem Karatekin
  • For correspondence: ane.landajuela@yale.edu matha.braun@yale.edu erdem.karatekin@yale.edu
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SUMMARY

Bacteria require membrane fission for cell division and endospore formation. FisB catalyzes membrane fission during sporulation, but the molecular basis is unclear as it cannot remodel membranes by itself. Sporulation initiates with an asymmetric division that generates a large mother cell and a smaller forespore that contains only 1/4 of its complete genome. As the mother cell membranes engulf the forespore, a DNA translocase pumps the rest of the chromosome into the small forespore compartment, inflating it due to increased turgor. When the engulfing membranes undergo fission, the forespore is released into the mother cell cytoplasm. Here we show that forespore inflation and FisB accumulation are both required for efficient membrane fission. We suggest that high membrane tension in the engulfment membrane caused by forespore inflation drives FisB-catalyzed membrane fission. Collectively our data indicate that DNA-translocation has a previously unappreciated second function in energizing FisB-mediated membrane fission under energy-limited conditions.

HIGHLIGHTS

  • - Membrane fission during endospore formation requires rapid forespore inflation by ATP-driven DNA translocation.

  • - Forespore inflation increases the tension of the engulfment and forespore membranes to near lysis tensions.

  • - FisB catalyzes membrane fission, but only if the membrane tension is high.

  • - Membrane fission utilizes chemical energy transduced to mechanical energy during DNA-packing into the forespore.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted October 08, 2021.
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Membrane fission during bacterial spore development requires DNA-driven cellular inflation
Ane Landajuela, Martha Braun, Alejandro Martínez-Calvo, Christopher D. A. Rodrigues, Thierry Doan, David Z. Rudner, Ned S. Wingreen, Erdem Karatekin
bioRxiv 2021.10.08.463650; doi: https://doi.org/10.1101/2021.10.08.463650
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Membrane fission during bacterial spore development requires DNA-driven cellular inflation
Ane Landajuela, Martha Braun, Alejandro Martínez-Calvo, Christopher D. A. Rodrigues, Thierry Doan, David Z. Rudner, Ned S. Wingreen, Erdem Karatekin
bioRxiv 2021.10.08.463650; doi: https://doi.org/10.1101/2021.10.08.463650

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