Coordinated Changes in Mutation and Growth Rates Induced by Genome Reduction

ABSTRACT Genome size is determined during evolution, but it can also be altered by genetic engineering in laboratories. The systematic characterization of reduced genomes provides valuable insights into the cellular properties that are quantitatively described by the global parameters related to the...

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Autores principales:	Issei Nishimura, Masaomi Kurokawa, Liu Liu, Bei-Wen Ying
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	genome reduction mutation rate growth rate genome size experimental evolution Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/034453da380a43c496c283902f0b31f0
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spelling	oai:doaj.org-article:034453da380a43c496c283902f0b31f02021-11-15T15:51:43ZCoordinated Changes in Mutation and Growth Rates Induced by Genome Reduction10.1128/mBio.00676-172150-7511https://doaj.org/article/034453da380a43c496c283902f0b31f02017-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00676-17https://doaj.org/toc/2150-7511ABSTRACT Genome size is determined during evolution, but it can also be altered by genetic engineering in laboratories. The systematic characterization of reduced genomes provides valuable insights into the cellular properties that are quantitatively described by the global parameters related to the dynamics of growth and mutation. In the present study, we analyzed a small collection of W3110 Escherichia coli derivatives containing either the wild-type genome or reduced genomes of various lengths to examine whether the mutation rate, a global parameter representing genomic plasticity, was affected by genome reduction. We found that the mutation rates of these cells increased with genome reduction. The correlation between genome length and mutation rate, which has been reported for the evolution of bacteria, was also identified, intriguingly, for genome reduction. Gene function enrichment analysis indicated that the deletion of many of the genes encoding membrane and transport proteins play a role in the mutation rate changes mediated by genome reduction. Furthermore, the increase in the mutation rate with genome reduction was highly associated with a decrease in the growth rate in a nutrition-dependent manner; thus, poorer media showed a larger change that was of higher significance. This negative correlation was strongly supported by experimental evidence that the serial transfer of the reduced genome improved the growth rate and reduced the mutation rate to a large extent. Taken together, the global parameters corresponding to the genome, growth, and mutation showed a coordinated relationship, which might be an essential working principle for balancing the cellular dynamics appropriate to the environment. IMPORTANCE Genome reduction is a powerful approach for investigating the fundamental rules for living systems. Whether genetically disturbed genomes have any specific properties that are different from or similar to those of natively evolved genomes has been under investigation. In the present study, we found that Escherichia coli cells with reduced genomes showed accelerated nucleotide substitution errors (mutation rates), although these cells retained the normal DNA mismatch repair systems. Intriguingly, this finding of correlation between reduced genome size and a higher mutation rate was consistent with the reported evolution of mutation rates. Furthermore, the increased mutation rate was quantitatively associated with a decreased growth rate, indicating that the global parameters related to the genome, growth, and mutation, which represent the amount of genetic information, the efficiency of propagation, and the fidelity of replication, respectively, are dynamically coordinated.Issei NishimuraMasaomi KurokawaLiu LiuBei-Wen YingAmerican Society for Microbiologyarticlegenome reductionmutation rategrowth rategenome sizeexperimental evolutionMicrobiologyQR1-502ENmBio, Vol 8, Iss 4 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	genome reduction mutation rate growth rate genome size experimental evolution Microbiology QR1-502
spellingShingle	genome reduction mutation rate growth rate genome size experimental evolution Microbiology QR1-502 Issei Nishimura Masaomi Kurokawa Liu Liu Bei-Wen Ying Coordinated Changes in Mutation and Growth Rates Induced by Genome Reduction
description	ABSTRACT Genome size is determined during evolution, but it can also be altered by genetic engineering in laboratories. The systematic characterization of reduced genomes provides valuable insights into the cellular properties that are quantitatively described by the global parameters related to the dynamics of growth and mutation. In the present study, we analyzed a small collection of W3110 Escherichia coli derivatives containing either the wild-type genome or reduced genomes of various lengths to examine whether the mutation rate, a global parameter representing genomic plasticity, was affected by genome reduction. We found that the mutation rates of these cells increased with genome reduction. The correlation between genome length and mutation rate, which has been reported for the evolution of bacteria, was also identified, intriguingly, for genome reduction. Gene function enrichment analysis indicated that the deletion of many of the genes encoding membrane and transport proteins play a role in the mutation rate changes mediated by genome reduction. Furthermore, the increase in the mutation rate with genome reduction was highly associated with a decrease in the growth rate in a nutrition-dependent manner; thus, poorer media showed a larger change that was of higher significance. This negative correlation was strongly supported by experimental evidence that the serial transfer of the reduced genome improved the growth rate and reduced the mutation rate to a large extent. Taken together, the global parameters corresponding to the genome, growth, and mutation showed a coordinated relationship, which might be an essential working principle for balancing the cellular dynamics appropriate to the environment. IMPORTANCE Genome reduction is a powerful approach for investigating the fundamental rules for living systems. Whether genetically disturbed genomes have any specific properties that are different from or similar to those of natively evolved genomes has been under investigation. In the present study, we found that Escherichia coli cells with reduced genomes showed accelerated nucleotide substitution errors (mutation rates), although these cells retained the normal DNA mismatch repair systems. Intriguingly, this finding of correlation between reduced genome size and a higher mutation rate was consistent with the reported evolution of mutation rates. Furthermore, the increased mutation rate was quantitatively associated with a decreased growth rate, indicating that the global parameters related to the genome, growth, and mutation, which represent the amount of genetic information, the efficiency of propagation, and the fidelity of replication, respectively, are dynamically coordinated.
format	article
author	Issei Nishimura Masaomi Kurokawa Liu Liu Bei-Wen Ying
author_facet	Issei Nishimura Masaomi Kurokawa Liu Liu Bei-Wen Ying
author_sort	Issei Nishimura
title	Coordinated Changes in Mutation and Growth Rates Induced by Genome Reduction
title_short	Coordinated Changes in Mutation and Growth Rates Induced by Genome Reduction
title_full	Coordinated Changes in Mutation and Growth Rates Induced by Genome Reduction
title_fullStr	Coordinated Changes in Mutation and Growth Rates Induced by Genome Reduction
title_full_unstemmed	Coordinated Changes in Mutation and Growth Rates Induced by Genome Reduction
title_sort	coordinated changes in mutation and growth rates induced by genome reduction
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/034453da380a43c496c283902f0b31f0
work_keys_str_mv	AT isseinishimura coordinatedchangesinmutationandgrowthratesinducedbygenomereduction AT masaomikurokawa coordinatedchangesinmutationandgrowthratesinducedbygenomereduction AT liuliu coordinatedchangesinmutationandgrowthratesinducedbygenomereduction AT beiwenying coordinatedchangesinmutationandgrowthratesinducedbygenomereduction
_version_	1718427316248379392

Coordinated Changes in Mutation and Growth Rates Induced by Genome Reduction

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