DNA-Membrane Anchor Facilitates Efficient Chromosome Translocation at a Distance in <named-content content-type="genus-species">Bacillus subtilis</named-content>

ABSTRACT Chromosome segregation in sporulating Bacillus subtilis involves the tethering of sister chromosomes at opposite cell poles. RacA is known to mediate chromosome tethering by interacting with both centromere-like elements in the DNA and with DivIVA, a membrane protein which localizes to the...

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Autores principales:	Nikolai P. Radzinski, Marina Besprozvannaya, Eric L. McLean, Anusha Talwalkar, Briana M. Burton
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Bacillus chromosome organization chromosome segregation sporulation Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/918d4c68ebd84533ab9880b6c67b4ede
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spelling	oai:doaj.org-article:918d4c68ebd84533ab9880b6c67b4ede2021-11-15T15:55:25ZDNA-Membrane Anchor Facilitates Efficient Chromosome Translocation at a Distance in <named-content content-type="genus-species">Bacillus subtilis</named-content>10.1128/mBio.01117-192150-7511https://doaj.org/article/918d4c68ebd84533ab9880b6c67b4ede2019-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01117-19https://doaj.org/toc/2150-7511ABSTRACT Chromosome segregation in sporulating Bacillus subtilis involves the tethering of sister chromosomes at opposite cell poles. RacA is known to mediate chromosome tethering by interacting with both centromere-like elements in the DNA and with DivIVA, a membrane protein which localizes to the cell poles. RacA has a secondary function in which it assists in nucleoid condensation. Here we demonstrate that, in addition to positioning and condensing the chromosome, RacA contributes to efficient transport of DNA by the chromosome segregation motor SpoIIIE. When RacA is deleted, one-quarter of cells fail to capture DNA in the nascent spore, yet 70% of cells fail to form viable spores without RacA. This discrepancy indicates that RacA possesses a role in sporulation beyond DNA capture and condensation. We observed that the mutant cells had reduced chromosome translocation into the forespore across the entire length of the chromosome, requiring nearly twice as much time to move a given DNA locus. Additionally, functional abolition of the RacA-DivIVA interaction reduced translocation to a similar degree as in a racA deletion strain, demonstrating the importance of the RacA-mediated tether in translocation and chromosome packaging during sporulation. We propose that the DNA-membrane anchor facilitates efficient translocation by SpoIIIE, not through direct protein-protein contacts but by virtue of physical effects on the chromosome that arise from anchoring DNA at a distance. IMPORTANCE To properly segregate their chromosomes, organisms tightly regulate the organization and dynamics of their DNA. Aspects of the process by which DNA is translocated during sporulation are not yet fully understood, such as what factors indirectly influence the activity of the motor protein SpoIIIE. In this work, we have shown that a DNA-membrane tether mediated by RacA contributes to the activity of SpoIIIE. Loss of RacA nearly doubles the time of translocation, despite the physically distinct locations these proteins and their activities occupy within the cell. This is a rare example of an explicit effect that DNA-membrane connections can have on cell physiology and demonstrates that distant changes to the state of the chromosome can influence motor proteins which act upon it.Nikolai P. RadzinskiMarina BesprozvannayaEric L. McLeanAnusha TalwalkarBriana M. BurtonAmerican Society for MicrobiologyarticleBacilluschromosome organizationchromosome segregationsporulationMicrobiologyQR1-502ENmBio, Vol 10, Iss 3 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Bacillus chromosome organization chromosome segregation sporulation Microbiology QR1-502
spellingShingle	Bacillus chromosome organization chromosome segregation sporulation Microbiology QR1-502 Nikolai P. Radzinski Marina Besprozvannaya Eric L. McLean Anusha Talwalkar Briana M. Burton DNA-Membrane Anchor Facilitates Efficient Chromosome Translocation at a Distance in <named-content content-type="genus-species">Bacillus subtilis</named-content>
description	ABSTRACT Chromosome segregation in sporulating Bacillus subtilis involves the tethering of sister chromosomes at opposite cell poles. RacA is known to mediate chromosome tethering by interacting with both centromere-like elements in the DNA and with DivIVA, a membrane protein which localizes to the cell poles. RacA has a secondary function in which it assists in nucleoid condensation. Here we demonstrate that, in addition to positioning and condensing the chromosome, RacA contributes to efficient transport of DNA by the chromosome segregation motor SpoIIIE. When RacA is deleted, one-quarter of cells fail to capture DNA in the nascent spore, yet 70% of cells fail to form viable spores without RacA. This discrepancy indicates that RacA possesses a role in sporulation beyond DNA capture and condensation. We observed that the mutant cells had reduced chromosome translocation into the forespore across the entire length of the chromosome, requiring nearly twice as much time to move a given DNA locus. Additionally, functional abolition of the RacA-DivIVA interaction reduced translocation to a similar degree as in a racA deletion strain, demonstrating the importance of the RacA-mediated tether in translocation and chromosome packaging during sporulation. We propose that the DNA-membrane anchor facilitates efficient translocation by SpoIIIE, not through direct protein-protein contacts but by virtue of physical effects on the chromosome that arise from anchoring DNA at a distance. IMPORTANCE To properly segregate their chromosomes, organisms tightly regulate the organization and dynamics of their DNA. Aspects of the process by which DNA is translocated during sporulation are not yet fully understood, such as what factors indirectly influence the activity of the motor protein SpoIIIE. In this work, we have shown that a DNA-membrane tether mediated by RacA contributes to the activity of SpoIIIE. Loss of RacA nearly doubles the time of translocation, despite the physically distinct locations these proteins and their activities occupy within the cell. This is a rare example of an explicit effect that DNA-membrane connections can have on cell physiology and demonstrates that distant changes to the state of the chromosome can influence motor proteins which act upon it.
format	article
author	Nikolai P. Radzinski Marina Besprozvannaya Eric L. McLean Anusha Talwalkar Briana M. Burton
author_facet	Nikolai P. Radzinski Marina Besprozvannaya Eric L. McLean Anusha Talwalkar Briana M. Burton
author_sort	Nikolai P. Radzinski
title	DNA-Membrane Anchor Facilitates Efficient Chromosome Translocation at a Distance in <named-content content-type="genus-species">Bacillus subtilis</named-content>
title_short	DNA-Membrane Anchor Facilitates Efficient Chromosome Translocation at a Distance in <named-content content-type="genus-species">Bacillus subtilis</named-content>
title_full	DNA-Membrane Anchor Facilitates Efficient Chromosome Translocation at a Distance in <named-content content-type="genus-species">Bacillus subtilis</named-content>
title_fullStr	DNA-Membrane Anchor Facilitates Efficient Chromosome Translocation at a Distance in <named-content content-type="genus-species">Bacillus subtilis</named-content>
title_full_unstemmed	DNA-Membrane Anchor Facilitates Efficient Chromosome Translocation at a Distance in <named-content content-type="genus-species">Bacillus subtilis</named-content>
title_sort	dna-membrane anchor facilitates efficient chromosome translocation at a distance in <named-content content-type="genus-species">bacillus subtilis</named-content>
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/918d4c68ebd84533ab9880b6c67b4ede
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DNA-Membrane Anchor Facilitates Efficient Chromosome Translocation at a Distance in <named-content content-type="genus-species">Bacillus subtilis</named-content>

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