Novel Chromosome Organization Pattern in <italic toggle="yes">Actinomycetales</italic>—Overlapping Replication Cycles Combined with Diploidy

ABSTRACT Bacteria regulate chromosome replication and segregation tightly with cell division to ensure faithful segregation of DNA to daughter generations. The underlying mechanisms have been addressed in several model species. It became apparent that bacteria have evolved quite different strategies...

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Autores principales: Kati Böhm, Fabian Meyer, Agata Rhomberg, Jörn Kalinowski, Catriona Donovan, Marc Bramkamp
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Publicado: American Society for Microbiology 2017
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spelling oai:doaj.org-article:c20b8e55caab4c56875c2245e35e28462021-11-15T15:51:30ZNovel Chromosome Organization Pattern in <italic toggle="yes">Actinomycetales</italic>—Overlapping Replication Cycles Combined with Diploidy10.1128/mBio.00511-172150-7511https://doaj.org/article/c20b8e55caab4c56875c2245e35e28462017-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00511-17https://doaj.org/toc/2150-7511ABSTRACT Bacteria regulate chromosome replication and segregation tightly with cell division to ensure faithful segregation of DNA to daughter generations. The underlying mechanisms have been addressed in several model species. It became apparent that bacteria have evolved quite different strategies to regulate DNA segregation and chromosomal organization. We have investigated here how the actinobacterium Corynebacterium glutamicum organizes chromosome segregation and DNA replication. Unexpectedly, we found that C. glutamicum cells are at least diploid under all of the conditions tested and that these organisms have overlapping C periods during replication, with both origins initiating replication simultaneously. On the basis of experimental data, we propose growth rate-dependent cell cycle models for C. glutamicum. IMPORTANCE Bacterial cell cycles are known for few model organisms and can vary significantly between species. Here, we studied the cell cycle of Corynebacterium glutamicum, an emerging cell biological model organism for mycolic acid-containing bacteria, including mycobacteria. Our data suggest that C. glutamicum carries two pole-attached chromosomes that replicate with overlapping C periods, thus initiating a new round of DNA replication before the previous one is terminated. The newly replicated origins segregate to midcell positions, where cell division occurs between the two new origins. Even after long starvation or under extremely slow-growth conditions, C. glutamicum cells are at least diploid, likely as an adaptation to environmental stress that may cause DNA damage. The cell cycle of C. glutamicum combines features of slow-growing organisms, such as polar origin localization, and fast-growing organisms, such as overlapping C periods.Kati BöhmFabian MeyerAgata RhombergJörn KalinowskiCatriona DonovanMarc BramkampAmerican Society for MicrobiologyarticleCorynebacteriumParAParBcell cyclediploidyoriginMicrobiologyQR1-502ENmBio, Vol 8, Iss 3 (2017)
institution DOAJ
collection DOAJ
language EN
topic Corynebacterium
ParA
ParB
cell cycle
diploidy
origin
Microbiology
QR1-502
spellingShingle Corynebacterium
ParA
ParB
cell cycle
diploidy
origin
Microbiology
QR1-502
Kati Böhm
Fabian Meyer
Agata Rhomberg
Jörn Kalinowski
Catriona Donovan
Marc Bramkamp
Novel Chromosome Organization Pattern in <italic toggle="yes">Actinomycetales</italic>—Overlapping Replication Cycles Combined with Diploidy
description ABSTRACT Bacteria regulate chromosome replication and segregation tightly with cell division to ensure faithful segregation of DNA to daughter generations. The underlying mechanisms have been addressed in several model species. It became apparent that bacteria have evolved quite different strategies to regulate DNA segregation and chromosomal organization. We have investigated here how the actinobacterium Corynebacterium glutamicum organizes chromosome segregation and DNA replication. Unexpectedly, we found that C. glutamicum cells are at least diploid under all of the conditions tested and that these organisms have overlapping C periods during replication, with both origins initiating replication simultaneously. On the basis of experimental data, we propose growth rate-dependent cell cycle models for C. glutamicum. IMPORTANCE Bacterial cell cycles are known for few model organisms and can vary significantly between species. Here, we studied the cell cycle of Corynebacterium glutamicum, an emerging cell biological model organism for mycolic acid-containing bacteria, including mycobacteria. Our data suggest that C. glutamicum carries two pole-attached chromosomes that replicate with overlapping C periods, thus initiating a new round of DNA replication before the previous one is terminated. The newly replicated origins segregate to midcell positions, where cell division occurs between the two new origins. Even after long starvation or under extremely slow-growth conditions, C. glutamicum cells are at least diploid, likely as an adaptation to environmental stress that may cause DNA damage. The cell cycle of C. glutamicum combines features of slow-growing organisms, such as polar origin localization, and fast-growing organisms, such as overlapping C periods.
format article
author Kati Böhm
Fabian Meyer
Agata Rhomberg
Jörn Kalinowski
Catriona Donovan
Marc Bramkamp
author_facet Kati Böhm
Fabian Meyer
Agata Rhomberg
Jörn Kalinowski
Catriona Donovan
Marc Bramkamp
author_sort Kati Böhm
title Novel Chromosome Organization Pattern in <italic toggle="yes">Actinomycetales</italic>—Overlapping Replication Cycles Combined with Diploidy
title_short Novel Chromosome Organization Pattern in <italic toggle="yes">Actinomycetales</italic>—Overlapping Replication Cycles Combined with Diploidy
title_full Novel Chromosome Organization Pattern in <italic toggle="yes">Actinomycetales</italic>—Overlapping Replication Cycles Combined with Diploidy
title_fullStr Novel Chromosome Organization Pattern in <italic toggle="yes">Actinomycetales</italic>—Overlapping Replication Cycles Combined with Diploidy
title_full_unstemmed Novel Chromosome Organization Pattern in <italic toggle="yes">Actinomycetales</italic>—Overlapping Replication Cycles Combined with Diploidy
title_sort novel chromosome organization pattern in <italic toggle="yes">actinomycetales</italic>—overlapping replication cycles combined with diploidy
publisher American Society for Microbiology
publishDate 2017
url https://doaj.org/article/c20b8e55caab4c56875c2245e35e2846
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