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Relevance of GC content to the conservation of DNA polymerase III/mismatch repair system in Gram-positive bacteria

The mechanism of DNA replication is one of the driving forces of genome evolution. Bacterial DNA polymerase III, the primary complex of DNA replication, consists of PolC and DnaE. PolC is conserved in Gram-positive bacteria, especially in the Firmicutes with low GC content, whereas DnaE is widely co...

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Autores principales: Akashi, Motohiro, Yoshikawa, Hirofumi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3774996/
https://www.ncbi.nlm.nih.gov/pubmed/24062730
http://dx.doi.org/10.3389/fmicb.2013.00266
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author Akashi, Motohiro
Yoshikawa, Hirofumi
author_facet Akashi, Motohiro
Yoshikawa, Hirofumi
author_sort Akashi, Motohiro
collection PubMed
description The mechanism of DNA replication is one of the driving forces of genome evolution. Bacterial DNA polymerase III, the primary complex of DNA replication, consists of PolC and DnaE. PolC is conserved in Gram-positive bacteria, especially in the Firmicutes with low GC content, whereas DnaE is widely conserved in most Gram-negative and Gram-positive bacteria. PolC contains two domains, the 3′-5′exonuclease domain and the polymerase domain, while DnaE only possesses the polymerase domain. Accordingly, DnaE does not have the proofreading function; in Escherichia coli, another enzyme DnaQ performs this function. In most bacteria, the fidelity of DNA replication is maintained by 3′-5′ exonuclease and a mismatch repair (MMR) system. However, we found that most Actinobacteria (a group of Gram-positive bacteria with high GC content) appear to have lost the MMR system and chromosomes may be replicated by DnaE-type DNA polymerase III with DnaQ-like 3′-5′ exonuclease. We tested the mutation bias of Bacillus subtilis, which belongs to the Firmicutes and found that the wild type strain is AT-biased while the mutS-deletant strain is remarkably GC-biased. If we presume that DnaE tends to make mistakes that increase GC content, these results can be explained by the mutS deletion (i.e., deletion of the MMR system). Thus, we propose that GC content is regulated by DNA polymerase and MMR system, and the absence of polC genes, which participate in the MMR system, may be the reason for the increase of GC content in Gram-positive bacteria such as Actinobacteria.
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spelling pubmed-37749962013-09-23 Relevance of GC content to the conservation of DNA polymerase III/mismatch repair system in Gram-positive bacteria Akashi, Motohiro Yoshikawa, Hirofumi Front Microbiol Microbiology The mechanism of DNA replication is one of the driving forces of genome evolution. Bacterial DNA polymerase III, the primary complex of DNA replication, consists of PolC and DnaE. PolC is conserved in Gram-positive bacteria, especially in the Firmicutes with low GC content, whereas DnaE is widely conserved in most Gram-negative and Gram-positive bacteria. PolC contains two domains, the 3′-5′exonuclease domain and the polymerase domain, while DnaE only possesses the polymerase domain. Accordingly, DnaE does not have the proofreading function; in Escherichia coli, another enzyme DnaQ performs this function. In most bacteria, the fidelity of DNA replication is maintained by 3′-5′ exonuclease and a mismatch repair (MMR) system. However, we found that most Actinobacteria (a group of Gram-positive bacteria with high GC content) appear to have lost the MMR system and chromosomes may be replicated by DnaE-type DNA polymerase III with DnaQ-like 3′-5′ exonuclease. We tested the mutation bias of Bacillus subtilis, which belongs to the Firmicutes and found that the wild type strain is AT-biased while the mutS-deletant strain is remarkably GC-biased. If we presume that DnaE tends to make mistakes that increase GC content, these results can be explained by the mutS deletion (i.e., deletion of the MMR system). Thus, we propose that GC content is regulated by DNA polymerase and MMR system, and the absence of polC genes, which participate in the MMR system, may be the reason for the increase of GC content in Gram-positive bacteria such as Actinobacteria. Frontiers Media S.A. 2013-09-17 /pmc/articles/PMC3774996/ /pubmed/24062730 http://dx.doi.org/10.3389/fmicb.2013.00266 Text en Copyright © 2013 Akashi and Yoshikawa. http://creativecommons.org/licenses/by/3.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Akashi, Motohiro
Yoshikawa, Hirofumi
Relevance of GC content to the conservation of DNA polymerase III/mismatch repair system in Gram-positive bacteria
title Relevance of GC content to the conservation of DNA polymerase III/mismatch repair system in Gram-positive bacteria
title_full Relevance of GC content to the conservation of DNA polymerase III/mismatch repair system in Gram-positive bacteria
title_fullStr Relevance of GC content to the conservation of DNA polymerase III/mismatch repair system in Gram-positive bacteria
title_full_unstemmed Relevance of GC content to the conservation of DNA polymerase III/mismatch repair system in Gram-positive bacteria
title_short Relevance of GC content to the conservation of DNA polymerase III/mismatch repair system in Gram-positive bacteria
title_sort relevance of gc content to the conservation of dna polymerase iii/mismatch repair system in gram-positive bacteria
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3774996/
https://www.ncbi.nlm.nih.gov/pubmed/24062730
http://dx.doi.org/10.3389/fmicb.2013.00266
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AT yoshikawahirofumi relevanceofgccontenttotheconservationofdnapolymeraseiiimismatchrepairsystemingrampositivebacteria