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...
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2017-07-01
|
| Series: | mBio |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.00511-17 |
| _version_ | 1818825904733814784 |
|---|---|
| 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 |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-19T00:19:11Z |
| format | Article |
| id | doaj.art-c20b8e55caab4c56875c2245e35e2846 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-19T00:19:11Z |
| publishDate | 2017-07-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-c20b8e55caab4c56875c2245e35e28462022-12-21T20:45:37ZengAmerican Society for MicrobiologymBio2150-75112017-07-018310.1128/mBio.00511-17Novel Chromosome Organization Pattern in <italic toggle="yes">Actinomycetales</italic>—Overlapping Replication Cycles Combined with DiploidyKati Böhm0Fabian Meyer1Agata Rhomberg2Jörn Kalinowski3Catriona Donovan4Marc Bramkamp5Ludwig-Maximilians-Universität München, Fakultät Biologie, Planegg-Martinsried, GermanyLudwig-Maximilians-Universität München, Fakultät Biologie, Planegg-Martinsried, GermanyLudwig-Maximilians-Universität München, Fakultät Biologie, Planegg-Martinsried, GermanyUniversität Bielefeld, Center for Biotechnology (CeBiTec), Bielefeld, GermanyLudwig-Maximilians-Universität München, Fakultät Biologie, Planegg-Martinsried, GermanyLudwig-Maximilians-Universität München, Fakultät Biologie, Planegg-Martinsried, GermanyABSTRACT 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.https://journals.asm.org/doi/10.1128/mBio.00511-17CorynebacteriumParAParBcell cyclediploidyorigin |
| spellingShingle | 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 mBio Corynebacterium ParA ParB cell cycle diploidy origin |
| title | 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_short | 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 |
| topic | Corynebacterium ParA ParB cell cycle diploidy origin |
| url | https://journals.asm.org/doi/10.1128/mBio.00511-17 |
| work_keys_str_mv | AT katibohm novelchromosomeorganizationpatterninitalictoggleyesactinomycetalesitalicoverlappingreplicationcyclescombinedwithdiploidy AT fabianmeyer novelchromosomeorganizationpatterninitalictoggleyesactinomycetalesitalicoverlappingreplicationcyclescombinedwithdiploidy AT agatarhomberg novelchromosomeorganizationpatterninitalictoggleyesactinomycetalesitalicoverlappingreplicationcyclescombinedwithdiploidy AT jornkalinowski novelchromosomeorganizationpatterninitalictoggleyesactinomycetalesitalicoverlappingreplicationcyclescombinedwithdiploidy AT catrionadonovan novelchromosomeorganizationpatterninitalictoggleyesactinomycetalesitalicoverlappingreplicationcyclescombinedwithdiploidy AT marcbramkamp novelchromosomeorganizationpatterninitalictoggleyesactinomycetalesitalicoverlappingreplicationcyclescombinedwithdiploidy |