Is the Evolution of <named-content content-type="genus-species">Salmonella enterica</named-content> subsp. <italic toggle="yes">enterica</italic> Linked to Restriction-Modification Systems?

ABSTRACT Salmonella enterica subsp. enterica bacteria are highly diverse foodborne pathogens that are subdivided into more than 1,500 serovars. The diversity is believed to result from mutational evolution, as well as intra- and interspecies recombination that potentially could be influenced by rest...

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Autores principales: Louise Roer, Rene S. Hendriksen, Pimlapas Leekitcharoenphon, Oksana Lukjancenko, Rolf Sommer Kaas, Henrik Hasman, Frank M. Aarestrup
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Publicado: American Society for Microbiology 2016
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spelling oai:doaj.org-article:57ae4c5a57344586abf18540dd66fc652021-12-02T19:47:34ZIs the Evolution of <named-content content-type="genus-species">Salmonella enterica</named-content> subsp. <italic toggle="yes">enterica</italic> Linked to Restriction-Modification Systems?10.1128/mSystems.00009-162379-5077https://doaj.org/article/57ae4c5a57344586abf18540dd66fc652016-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00009-16https://doaj.org/toc/2379-5077ABSTRACT Salmonella enterica subsp. enterica bacteria are highly diverse foodborne pathogens that are subdivided into more than 1,500 serovars. The diversity is believed to result from mutational evolution, as well as intra- and interspecies recombination that potentially could be influenced by restriction-modification (RM) systems. The aim of this study was to investigate whether RM systems were linked to the evolution of Salmonella enterica subsp. enterica. The study included 221 Salmonella enterica genomes, of which 68 were de novo sequenced and 153 were public available genomes from ENA. The data set covered 97 different serovars of Salmonella enterica subsp. enterica and an additional five genomes from four other Salmonella subspecies as an outgroup for constructing the phylogenetic trees. The phylogenetic trees were constructed based on multiple alignment of core genes, as well as the presence or absence of pangenes. The topology of the trees was compared to the presence of RM systems, antimicrobial resistance (AMR) genes, Salmonella pathogenicity islands (SPIs), and plasmid replicons. We did not observe any correlation between evolution and the RM systems in S. enterica subsp. enterica. However, sublineage correlations and serovar-specific patterns were observed. Additionally, we conclude that plasmid replicons, SPIs, and AMR were all better correlated to serovars than to RM systems. This study suggests a limited influence of RM systems on the evolution of Salmonella enterica subsp. enterica, which could be due to the conjugational mode of horizontal gene transfer in Salmonella. Thus, we conclude that other factors must be involved in shaping the evolution of bacteria. IMPORTANCE The evolution of bacterial pathogens, their plasticity and ability to rapidly change and adapt to new surroundings are crucial for understanding the epidemiology and public health. With the application of genomics, it became clear that horizontal gene transfer played a key role in evolution. To understand the evolution and diversification of pathogens, we need to understand the processes that drive the horizontal gene transfer. Restriction-modification systems are thought to cause rearrangements within the chromosome, as well as act as a barrier to horizontal gene transfer. However, here we show that the correlation between restriction-modification systems and evolution in other bacterial species does not apply to Salmonella enterica subsp. enterica. In summary, from this work, we conclude that other mechanisms might be involved in controlling and shaping the evolution of Salmonella enterica subsp. enterica.Louise RoerRene S. HendriksenPimlapas LeekitcharoenphonOksana LukjancenkoRolf Sommer KaasHenrik HasmanFrank M. AarestrupAmerican Society for Microbiologyarticlerestriction-modification systemsevolutionSalmonella phylogenetic analysisnext-generation sequencingwhole-genome sequencingMicrobiologyQR1-502ENmSystems, Vol 1, Iss 3 (2016)
institution DOAJ
collection DOAJ
language EN
topic restriction-modification systems
evolution
Salmonella phylogenetic analysis
next-generation sequencing
whole-genome sequencing
Microbiology
QR1-502
spellingShingle restriction-modification systems
evolution
Salmonella phylogenetic analysis
next-generation sequencing
whole-genome sequencing
Microbiology
QR1-502
Louise Roer
Rene S. Hendriksen
Pimlapas Leekitcharoenphon
Oksana Lukjancenko
Rolf Sommer Kaas
Henrik Hasman
Frank M. Aarestrup
Is the Evolution of <named-content content-type="genus-species">Salmonella enterica</named-content> subsp. <italic toggle="yes">enterica</italic> Linked to Restriction-Modification Systems?
description ABSTRACT Salmonella enterica subsp. enterica bacteria are highly diverse foodborne pathogens that are subdivided into more than 1,500 serovars. The diversity is believed to result from mutational evolution, as well as intra- and interspecies recombination that potentially could be influenced by restriction-modification (RM) systems. The aim of this study was to investigate whether RM systems were linked to the evolution of Salmonella enterica subsp. enterica. The study included 221 Salmonella enterica genomes, of which 68 were de novo sequenced and 153 were public available genomes from ENA. The data set covered 97 different serovars of Salmonella enterica subsp. enterica and an additional five genomes from four other Salmonella subspecies as an outgroup for constructing the phylogenetic trees. The phylogenetic trees were constructed based on multiple alignment of core genes, as well as the presence or absence of pangenes. The topology of the trees was compared to the presence of RM systems, antimicrobial resistance (AMR) genes, Salmonella pathogenicity islands (SPIs), and plasmid replicons. We did not observe any correlation between evolution and the RM systems in S. enterica subsp. enterica. However, sublineage correlations and serovar-specific patterns were observed. Additionally, we conclude that plasmid replicons, SPIs, and AMR were all better correlated to serovars than to RM systems. This study suggests a limited influence of RM systems on the evolution of Salmonella enterica subsp. enterica, which could be due to the conjugational mode of horizontal gene transfer in Salmonella. Thus, we conclude that other factors must be involved in shaping the evolution of bacteria. IMPORTANCE The evolution of bacterial pathogens, their plasticity and ability to rapidly change and adapt to new surroundings are crucial for understanding the epidemiology and public health. With the application of genomics, it became clear that horizontal gene transfer played a key role in evolution. To understand the evolution and diversification of pathogens, we need to understand the processes that drive the horizontal gene transfer. Restriction-modification systems are thought to cause rearrangements within the chromosome, as well as act as a barrier to horizontal gene transfer. However, here we show that the correlation between restriction-modification systems and evolution in other bacterial species does not apply to Salmonella enterica subsp. enterica. In summary, from this work, we conclude that other mechanisms might be involved in controlling and shaping the evolution of Salmonella enterica subsp. enterica.
format article
author Louise Roer
Rene S. Hendriksen
Pimlapas Leekitcharoenphon
Oksana Lukjancenko
Rolf Sommer Kaas
Henrik Hasman
Frank M. Aarestrup
author_facet Louise Roer
Rene S. Hendriksen
Pimlapas Leekitcharoenphon
Oksana Lukjancenko
Rolf Sommer Kaas
Henrik Hasman
Frank M. Aarestrup
author_sort Louise Roer
title Is the Evolution of <named-content content-type="genus-species">Salmonella enterica</named-content> subsp. <italic toggle="yes">enterica</italic> Linked to Restriction-Modification Systems?
title_short Is the Evolution of <named-content content-type="genus-species">Salmonella enterica</named-content> subsp. <italic toggle="yes">enterica</italic> Linked to Restriction-Modification Systems?
title_full Is the Evolution of <named-content content-type="genus-species">Salmonella enterica</named-content> subsp. <italic toggle="yes">enterica</italic> Linked to Restriction-Modification Systems?
title_fullStr Is the Evolution of <named-content content-type="genus-species">Salmonella enterica</named-content> subsp. <italic toggle="yes">enterica</italic> Linked to Restriction-Modification Systems?
title_full_unstemmed Is the Evolution of <named-content content-type="genus-species">Salmonella enterica</named-content> subsp. <italic toggle="yes">enterica</italic> Linked to Restriction-Modification Systems?
title_sort is the evolution of <named-content content-type="genus-species">salmonella enterica</named-content> subsp. <italic toggle="yes">enterica</italic> linked to restriction-modification systems?
publisher American Society for Microbiology
publishDate 2016
url https://doaj.org/article/57ae4c5a57344586abf18540dd66fc65
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