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Prevalence of phase variable epigenetic invertons among host-associated bacteria

Type I restriction-modification (R-M) systems consist of a DNA endonuclease (HsdR, HsdM and HsdS subunits) and methyltransferase (HsdM and HsdS subunits). The hsdS sequences flanked by inverted repeats (referred to as epigenetic invertons) in certain Type I R-M systems undergo invertase-catalyzed in...

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Autores principales: Huang, Xueting, Wang, Juanjuan, Li, Jing, Liu, Yanni, Liu, Xue, Li, Zeyao, Kurniyati, Kurni, Deng, Yijie, Wang, Guilin, Ralph, Joseph D, De Ste Croix, Megan, Escobar-Gonzalez, Sara, Roberts, Richard J, Veening, Jan-Willem, Lan, Xun, Oggioni, Marco R, Li, Chunhao, Zhang, Jing-Ren
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7672463/
https://www.ncbi.nlm.nih.gov/pubmed/33119758
http://dx.doi.org/10.1093/nar/gkaa907
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author Huang, Xueting
Wang, Juanjuan
Li, Jing
Liu, Yanni
Liu, Xue
Li, Zeyao
Kurniyati, Kurni
Deng, Yijie
Wang, Guilin
Ralph, Joseph D
De Ste Croix, Megan
Escobar-Gonzalez, Sara
Roberts, Richard J
Veening, Jan-Willem
Lan, Xun
Oggioni, Marco R
Li, Chunhao
Zhang, Jing-Ren
author_facet Huang, Xueting
Wang, Juanjuan
Li, Jing
Liu, Yanni
Liu, Xue
Li, Zeyao
Kurniyati, Kurni
Deng, Yijie
Wang, Guilin
Ralph, Joseph D
De Ste Croix, Megan
Escobar-Gonzalez, Sara
Roberts, Richard J
Veening, Jan-Willem
Lan, Xun
Oggioni, Marco R
Li, Chunhao
Zhang, Jing-Ren
author_sort Huang, Xueting
collection PubMed
description Type I restriction-modification (R-M) systems consist of a DNA endonuclease (HsdR, HsdM and HsdS subunits) and methyltransferase (HsdM and HsdS subunits). The hsdS sequences flanked by inverted repeats (referred to as epigenetic invertons) in certain Type I R-M systems undergo invertase-catalyzed inversions. Previous studies in Streptococcus pneumoniae have shown that hsdS inversions within clonal populations produce subpopulations with profound differences in the methylome, cellular physiology and virulence. In this study, we bioinformatically identified six major clades of the tyrosine and serine family invertases homologs from 16 bacterial phyla, which potentially catalyze hsdS inversions in the epigenetic invertons. In particular, the epigenetic invertons are highly enriched in host-associated bacteria. We further verified hsdS inversions in the Type I R-M systems of four representative host-associated bacteria and found that each of the resultant hsdS allelic variants specifies methylation of a unique DNA sequence. In addition, transcriptome analysis revealed that hsdS allelic variations in Enterococcus faecalis exert significant impact on gene expression. These findings indicate that epigenetic switches driven by invertases in the epigenetic invertons broadly operate in the host-associated bacteria, which may broadly contribute to bacterial host adaptation and virulence beyond the role of the Type I R-M systems against phage infection.
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spelling pubmed-76724632020-11-24 Prevalence of phase variable epigenetic invertons among host-associated bacteria Huang, Xueting Wang, Juanjuan Li, Jing Liu, Yanni Liu, Xue Li, Zeyao Kurniyati, Kurni Deng, Yijie Wang, Guilin Ralph, Joseph D De Ste Croix, Megan Escobar-Gonzalez, Sara Roberts, Richard J Veening, Jan-Willem Lan, Xun Oggioni, Marco R Li, Chunhao Zhang, Jing-Ren Nucleic Acids Res Gene regulation, Chromatin and Epigenetics Type I restriction-modification (R-M) systems consist of a DNA endonuclease (HsdR, HsdM and HsdS subunits) and methyltransferase (HsdM and HsdS subunits). The hsdS sequences flanked by inverted repeats (referred to as epigenetic invertons) in certain Type I R-M systems undergo invertase-catalyzed inversions. Previous studies in Streptococcus pneumoniae have shown that hsdS inversions within clonal populations produce subpopulations with profound differences in the methylome, cellular physiology and virulence. In this study, we bioinformatically identified six major clades of the tyrosine and serine family invertases homologs from 16 bacterial phyla, which potentially catalyze hsdS inversions in the epigenetic invertons. In particular, the epigenetic invertons are highly enriched in host-associated bacteria. We further verified hsdS inversions in the Type I R-M systems of four representative host-associated bacteria and found that each of the resultant hsdS allelic variants specifies methylation of a unique DNA sequence. In addition, transcriptome analysis revealed that hsdS allelic variations in Enterococcus faecalis exert significant impact on gene expression. These findings indicate that epigenetic switches driven by invertases in the epigenetic invertons broadly operate in the host-associated bacteria, which may broadly contribute to bacterial host adaptation and virulence beyond the role of the Type I R-M systems against phage infection. Oxford University Press 2020-10-29 /pmc/articles/PMC7672463/ /pubmed/33119758 http://dx.doi.org/10.1093/nar/gkaa907 Text en © The Author(s) 2020. Published by Oxford University Press on behalf of Nucleic Acids Research. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Gene regulation, Chromatin and Epigenetics
Huang, Xueting
Wang, Juanjuan
Li, Jing
Liu, Yanni
Liu, Xue
Li, Zeyao
Kurniyati, Kurni
Deng, Yijie
Wang, Guilin
Ralph, Joseph D
De Ste Croix, Megan
Escobar-Gonzalez, Sara
Roberts, Richard J
Veening, Jan-Willem
Lan, Xun
Oggioni, Marco R
Li, Chunhao
Zhang, Jing-Ren
Prevalence of phase variable epigenetic invertons among host-associated bacteria
title Prevalence of phase variable epigenetic invertons among host-associated bacteria
title_full Prevalence of phase variable epigenetic invertons among host-associated bacteria
title_fullStr Prevalence of phase variable epigenetic invertons among host-associated bacteria
title_full_unstemmed Prevalence of phase variable epigenetic invertons among host-associated bacteria
title_short Prevalence of phase variable epigenetic invertons among host-associated bacteria
title_sort prevalence of phase variable epigenetic invertons among host-associated bacteria
topic Gene regulation, Chromatin and Epigenetics
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7672463/
https://www.ncbi.nlm.nih.gov/pubmed/33119758
http://dx.doi.org/10.1093/nar/gkaa907
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