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SMRT sequencing of the Campylobacter coli BfR-CA-9557 genome sequence reveals unique methylation motifs

BACKGROUND: Campylobacter species are the most prevalent bacterial pathogen causing acute enteritis worldwide. In contrast to Campylobacter jejuni, about 5 % of Campylobacter coli strains exhibit susceptibility to restriction endonuclease digestion by DpnI cutting specifically 5’-G(m)ATC-3’ motifs....

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Autores principales: Zautner, Andreas E., Goldschmidt, Anne-Marie, Thürmer, Andrea, Schuldes, Jörg, Bader, Oliver, Lugert, Raimond, Groß, Uwe, Stingl, Kerstin, Salinas, Gabriela, Lingner, Thomas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4687069/
https://www.ncbi.nlm.nih.gov/pubmed/26689587
http://dx.doi.org/10.1186/s12864-015-2317-3
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author Zautner, Andreas E.
Goldschmidt, Anne-Marie
Thürmer, Andrea
Schuldes, Jörg
Bader, Oliver
Lugert, Raimond
Groß, Uwe
Stingl, Kerstin
Salinas, Gabriela
Lingner, Thomas
author_facet Zautner, Andreas E.
Goldschmidt, Anne-Marie
Thürmer, Andrea
Schuldes, Jörg
Bader, Oliver
Lugert, Raimond
Groß, Uwe
Stingl, Kerstin
Salinas, Gabriela
Lingner, Thomas
author_sort Zautner, Andreas E.
collection PubMed
description BACKGROUND: Campylobacter species are the most prevalent bacterial pathogen causing acute enteritis worldwide. In contrast to Campylobacter jejuni, about 5 % of Campylobacter coli strains exhibit susceptibility to restriction endonuclease digestion by DpnI cutting specifically 5’-G(m)ATC-3’ motifs. This indicates significant differences in DNA methylation between both microbial species. The goal of the study was to analyze the methylome of a C. coli strain susceptible to DpnI digestion, to identify its methylation motifs and restriction modification systems (RM-systems), and compare them to related organisms like C. jejuni and Helicobacter pylori. RESULTS: Using one SMRT cell and the PacBio RS sequencing technology followed by PacBio Modification and Motif Analysis the complete genome of the DpnI susceptible strain C. coli BfR-CA-9557 was sequenced to 500-fold coverage and assembled into a single contig of 1.7 Mbp. The genome contains a CJIE1-like element prophage and is phylogenetically closer to C. coli clade 1 isolates than clade 3. 45,881 6-methylated adenines (ca. 2.7 % of genome positions) that are predominantly arranged in eight different methylation motifs and 1,788 4-methylated cytosines (ca. 0.1 %) have been detected. Only two of these motifs correspond to known restriction modification motifs. Characteristic for this methylome was the very high fraction of methylation of motifs with mostly above 99 %. CONCLUSIONS: Only five dominant methylation motifs have been identified in C. jejuni, which have been associated with known RM-systems. C. coli BFR-CA-9557 shares one (RAATTY) of these, but four ORFs could be assigned to putative Type I RM-systems, seven ORFs to Type II RM-systems and three ORFs to Type IV RM-systems. In accordance with DpnI prescreening RM-system IIP, methylation of GATC motifs was detected in C. coli BfR-CA-9557. A homologous IIP RM-system has been described for H. pylori. The remaining methylation motifs are specific for C. coli BfR-CA-9557 and have been neither detected in C. jejuni nor in H. pylori. The results of this study give us new insights into epigenetics of Campylobacteraceae and provide the groundwork to resolve the function of RM-systems in C. coli. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-015-2317-3) contains supplementary material, which is available to authorized users.
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spelling pubmed-46870692015-12-23 SMRT sequencing of the Campylobacter coli BfR-CA-9557 genome sequence reveals unique methylation motifs Zautner, Andreas E. Goldschmidt, Anne-Marie Thürmer, Andrea Schuldes, Jörg Bader, Oliver Lugert, Raimond Groß, Uwe Stingl, Kerstin Salinas, Gabriela Lingner, Thomas BMC Genomics Research Article BACKGROUND: Campylobacter species are the most prevalent bacterial pathogen causing acute enteritis worldwide. In contrast to Campylobacter jejuni, about 5 % of Campylobacter coli strains exhibit susceptibility to restriction endonuclease digestion by DpnI cutting specifically 5’-G(m)ATC-3’ motifs. This indicates significant differences in DNA methylation between both microbial species. The goal of the study was to analyze the methylome of a C. coli strain susceptible to DpnI digestion, to identify its methylation motifs and restriction modification systems (RM-systems), and compare them to related organisms like C. jejuni and Helicobacter pylori. RESULTS: Using one SMRT cell and the PacBio RS sequencing technology followed by PacBio Modification and Motif Analysis the complete genome of the DpnI susceptible strain C. coli BfR-CA-9557 was sequenced to 500-fold coverage and assembled into a single contig of 1.7 Mbp. The genome contains a CJIE1-like element prophage and is phylogenetically closer to C. coli clade 1 isolates than clade 3. 45,881 6-methylated adenines (ca. 2.7 % of genome positions) that are predominantly arranged in eight different methylation motifs and 1,788 4-methylated cytosines (ca. 0.1 %) have been detected. Only two of these motifs correspond to known restriction modification motifs. Characteristic for this methylome was the very high fraction of methylation of motifs with mostly above 99 %. CONCLUSIONS: Only five dominant methylation motifs have been identified in C. jejuni, which have been associated with known RM-systems. C. coli BFR-CA-9557 shares one (RAATTY) of these, but four ORFs could be assigned to putative Type I RM-systems, seven ORFs to Type II RM-systems and three ORFs to Type IV RM-systems. In accordance with DpnI prescreening RM-system IIP, methylation of GATC motifs was detected in C. coli BfR-CA-9557. A homologous IIP RM-system has been described for H. pylori. The remaining methylation motifs are specific for C. coli BfR-CA-9557 and have been neither detected in C. jejuni nor in H. pylori. The results of this study give us new insights into epigenetics of Campylobacteraceae and provide the groundwork to resolve the function of RM-systems in C. coli. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-015-2317-3) contains supplementary material, which is available to authorized users. BioMed Central 2015-12-21 /pmc/articles/PMC4687069/ /pubmed/26689587 http://dx.doi.org/10.1186/s12864-015-2317-3 Text en © Zautner et al. 2015 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Zautner, Andreas E.
Goldschmidt, Anne-Marie
Thürmer, Andrea
Schuldes, Jörg
Bader, Oliver
Lugert, Raimond
Groß, Uwe
Stingl, Kerstin
Salinas, Gabriela
Lingner, Thomas
SMRT sequencing of the Campylobacter coli BfR-CA-9557 genome sequence reveals unique methylation motifs
title SMRT sequencing of the Campylobacter coli BfR-CA-9557 genome sequence reveals unique methylation motifs
title_full SMRT sequencing of the Campylobacter coli BfR-CA-9557 genome sequence reveals unique methylation motifs
title_fullStr SMRT sequencing of the Campylobacter coli BfR-CA-9557 genome sequence reveals unique methylation motifs
title_full_unstemmed SMRT sequencing of the Campylobacter coli BfR-CA-9557 genome sequence reveals unique methylation motifs
title_short SMRT sequencing of the Campylobacter coli BfR-CA-9557 genome sequence reveals unique methylation motifs
title_sort smrt sequencing of the campylobacter coli bfr-ca-9557 genome sequence reveals unique methylation motifs
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4687069/
https://www.ncbi.nlm.nih.gov/pubmed/26689587
http://dx.doi.org/10.1186/s12864-015-2317-3
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