Coordination of Polyploid Chromosome Replication with Cell Size and Growth in a Cyanobacterium

ABSTRACT Homologous chromosome number (ploidy) has diversified among bacteria, archaea, and eukaryotes over evolution. In bacteria, model organisms such as Escherichia coli possess a single chromosome encoding the entire genome during slow growth. In contrast, other bacteria, including cyanobacteria...

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Autores principales:	Ryudo Ohbayashi, Ai Nakamachi, Tetsuhiro S. Hatakeyama, Satoru Watanabe, Yu Kanesaki, Taku Chibazakura, Hirofumi Yoshikawa, Shin-ya Miyagishima
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	DNA replication DnaA polyploidy RpoC cyanobacteria Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/3a209cca49224ceabb18d4e0daee2e1c
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spelling	oai:doaj.org-article:3a209cca49224ceabb18d4e0daee2e1c2021-11-15T15:55:26ZCoordination of Polyploid Chromosome Replication with Cell Size and Growth in a Cyanobacterium10.1128/mBio.00510-192150-7511https://doaj.org/article/3a209cca49224ceabb18d4e0daee2e1c2019-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00510-19https://doaj.org/toc/2150-7511ABSTRACT Homologous chromosome number (ploidy) has diversified among bacteria, archaea, and eukaryotes over evolution. In bacteria, model organisms such as Escherichia coli possess a single chromosome encoding the entire genome during slow growth. In contrast, other bacteria, including cyanobacteria, maintain multiple copies of individual chromosomes (polyploid). Although a correlation between ploidy level and cell size has been observed in bacteria and eukaryotes, it is poorly understood how replication of multicopy chromosomes is regulated and how ploidy level is adjusted to cell size. In addition, the advantages conferred by polyploidy are largely unknown. Here we show that only one or a few multicopy chromosomes are replicated at once in the cyanobacterium Synechococcus elongatus and that this restriction depends on regulation of DnaA activity. Inhibiting the DnaA intrinsic ATPase activity in S. elongatus increased the number of replicating chromosomes and chromosome number per cell but did not affect cell growth. In contrast, when cell growth rate was increased or decreased, DnaA level, DnaA activity, and the number of replicating chromosomes also increased or decreased in parallel, resulting in nearly constant chromosome copy number per unit of cell volume at constant temperature. When chromosome copy number was increased by inhibition of DnaA ATPase activity or reduced culture temperature, cells exhibited greater resistance to UV light. Thus, it is suggested that the stepwise replication of the genome enables cyanobacteria to maintain nearly constant gene copy number per unit of cell volume and that multicopy chromosomes function as backup genetic information to compensate for genomic damage. IMPORTANCE Polyploidy has evolved many times across the kingdom of life. The relationship between cell growth and chromosome replication in bacteria has been studied extensively in monoploid model organisms such as Escherichia coli but not in polyploid organisms. Our study of the polyploid cyanobacterium Synechococcus elongatus demonstrates that replicating chromosome number is restricted and regulated by DnaA to maintain a relatively stable gene copy number/cell volume ratio during cell growth. In addition, our results suggest that polyploidy confers resistance to UV, which damages DNA. This compensatory polyploidy is likely necessitated by photosynthesis, which requires sunlight and generates damaging reactive oxygen species, and may also explain how polyploid bacteria can adapt to extreme environments with high risk of DNA damage.Ryudo OhbayashiAi NakamachiTetsuhiro S. HatakeyamaSatoru WatanabeYu KanesakiTaku ChibazakuraHirofumi YoshikawaShin-ya MiyagishimaAmerican Society for MicrobiologyarticleDNA replicationDnaApolyploidyRpoCcyanobacteriaMicrobiologyQR1-502ENmBio, Vol 10, Iss 2 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	DNA replication DnaA polyploidy RpoC cyanobacteria Microbiology QR1-502
spellingShingle	DNA replication DnaA polyploidy RpoC cyanobacteria Microbiology QR1-502 Ryudo Ohbayashi Ai Nakamachi Tetsuhiro S. Hatakeyama Satoru Watanabe Yu Kanesaki Taku Chibazakura Hirofumi Yoshikawa Shin-ya Miyagishima Coordination of Polyploid Chromosome Replication with Cell Size and Growth in a Cyanobacterium
description	ABSTRACT Homologous chromosome number (ploidy) has diversified among bacteria, archaea, and eukaryotes over evolution. In bacteria, model organisms such as Escherichia coli possess a single chromosome encoding the entire genome during slow growth. In contrast, other bacteria, including cyanobacteria, maintain multiple copies of individual chromosomes (polyploid). Although a correlation between ploidy level and cell size has been observed in bacteria and eukaryotes, it is poorly understood how replication of multicopy chromosomes is regulated and how ploidy level is adjusted to cell size. In addition, the advantages conferred by polyploidy are largely unknown. Here we show that only one or a few multicopy chromosomes are replicated at once in the cyanobacterium Synechococcus elongatus and that this restriction depends on regulation of DnaA activity. Inhibiting the DnaA intrinsic ATPase activity in S. elongatus increased the number of replicating chromosomes and chromosome number per cell but did not affect cell growth. In contrast, when cell growth rate was increased or decreased, DnaA level, DnaA activity, and the number of replicating chromosomes also increased or decreased in parallel, resulting in nearly constant chromosome copy number per unit of cell volume at constant temperature. When chromosome copy number was increased by inhibition of DnaA ATPase activity or reduced culture temperature, cells exhibited greater resistance to UV light. Thus, it is suggested that the stepwise replication of the genome enables cyanobacteria to maintain nearly constant gene copy number per unit of cell volume and that multicopy chromosomes function as backup genetic information to compensate for genomic damage. IMPORTANCE Polyploidy has evolved many times across the kingdom of life. The relationship between cell growth and chromosome replication in bacteria has been studied extensively in monoploid model organisms such as Escherichia coli but not in polyploid organisms. Our study of the polyploid cyanobacterium Synechococcus elongatus demonstrates that replicating chromosome number is restricted and regulated by DnaA to maintain a relatively stable gene copy number/cell volume ratio during cell growth. In addition, our results suggest that polyploidy confers resistance to UV, which damages DNA. This compensatory polyploidy is likely necessitated by photosynthesis, which requires sunlight and generates damaging reactive oxygen species, and may also explain how polyploid bacteria can adapt to extreme environments with high risk of DNA damage.
format	article
author	Ryudo Ohbayashi Ai Nakamachi Tetsuhiro S. Hatakeyama Satoru Watanabe Yu Kanesaki Taku Chibazakura Hirofumi Yoshikawa Shin-ya Miyagishima
author_facet	Ryudo Ohbayashi Ai Nakamachi Tetsuhiro S. Hatakeyama Satoru Watanabe Yu Kanesaki Taku Chibazakura Hirofumi Yoshikawa Shin-ya Miyagishima
author_sort	Ryudo Ohbayashi
title	Coordination of Polyploid Chromosome Replication with Cell Size and Growth in a Cyanobacterium
title_short	Coordination of Polyploid Chromosome Replication with Cell Size and Growth in a Cyanobacterium
title_full	Coordination of Polyploid Chromosome Replication with Cell Size and Growth in a Cyanobacterium
title_fullStr	Coordination of Polyploid Chromosome Replication with Cell Size and Growth in a Cyanobacterium
title_full_unstemmed	Coordination of Polyploid Chromosome Replication with Cell Size and Growth in a Cyanobacterium
title_sort	coordination of polyploid chromosome replication with cell size and growth in a cyanobacterium
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/3a209cca49224ceabb18d4e0daee2e1c
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_version_	1718427143975731200

Coordination of Polyploid Chromosome Replication with Cell Size and Growth in a Cyanobacterium

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