Insights into the genome architecture and evolution of Shiga toxin encoding bacteriophages of Escherichia coli
Autor(a) principal: | |
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Data de Publicação: | 2021 |
Outros Autores: | , , , , |
Tipo de documento: | Artigo |
Idioma: | eng |
Título da fonte: | Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
Texto Completo: | http://hdl.handle.net/1822/72809 |
Resumo: | Background: A total of 179 Shiga toxin-producing Escherichia coli (STEC) complete genomes were analyzed in terms of serotypes, prophage coding regions, and stx gene variants and their distribution. We further examined the genetic diversity of Stx-converting phage genomes (Stx phages), focusing on the lysis-lysogeny decision and lytic cassettes. Results: We show that most STEC isolates belong to non-O157 serotypes (73 %), regardless the sources and geographical regions. While the majority of STEC genomes contain a single stx gene (61 %), strains containing two (35 %), three (3 %) and four (1 %) stx genes were also found, being stx2 the most prevalent gene variant. Their location is exclusively found in intact prophage regions, indicating that they are phage-borne. We further demonstrate that Stx phages can be grouped into four clusters (A, B, C and D), three subclusters (A1, A2 and A3) and one singleton, based on their shared gene content. This cluster distribution is in good agreement with their predicted virion morphologies. Stx phage genomes are highly diverse with a vast number of 1,838 gene phamilies (phams) of related sequences (of which 677 are orphams i.e. unique genes) and, although having high mosaicism, they are generally organized into three major transcripts. While the mechanisms that guide lysis–lysogeny decision are complex, there is a strong selective pressure to maintain the stx genes location close to the lytic cassette composed of predicted SAR-endolysin and pin-holin lytic proteins. The evolution of STEC Stx phages seems to be strongly related to acquiring genetic material, probably from horizontal gene transfer events. Conclusions: This work provides novel insights on the genetic structure of Stx phages, showing a high genetic diversity throughout the genomes, where the various lysis-lysogeny regulatory systems are in contrast with an uncommon, but conserved, lytic system always adjacent to stx genes. |
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Insights into the genome architecture and evolution of Shiga toxin encoding bacteriophages of Escherichia coliSTECShiga toxin-encoding bacteriophagesGenomesClustersScience & TechnologyBackground: A total of 179 Shiga toxin-producing Escherichia coli (STEC) complete genomes were analyzed in terms of serotypes, prophage coding regions, and stx gene variants and their distribution. We further examined the genetic diversity of Stx-converting phage genomes (Stx phages), focusing on the lysis-lysogeny decision and lytic cassettes. Results: We show that most STEC isolates belong to non-O157 serotypes (73 %), regardless the sources and geographical regions. While the majority of STEC genomes contain a single stx gene (61 %), strains containing two (35 %), three (3 %) and four (1 %) stx genes were also found, being stx2 the most prevalent gene variant. Their location is exclusively found in intact prophage regions, indicating that they are phage-borne. We further demonstrate that Stx phages can be grouped into four clusters (A, B, C and D), three subclusters (A1, A2 and A3) and one singleton, based on their shared gene content. This cluster distribution is in good agreement with their predicted virion morphologies. Stx phage genomes are highly diverse with a vast number of 1,838 gene phamilies (phams) of related sequences (of which 677 are orphams i.e. unique genes) and, although having high mosaicism, they are generally organized into three major transcripts. While the mechanisms that guide lysis–lysogeny decision are complex, there is a strong selective pressure to maintain the stx genes location close to the lytic cassette composed of predicted SAR-endolysin and pin-holin lytic proteins. The evolution of STEC Stx phages seems to be strongly related to acquiring genetic material, probably from horizontal gene transfer events. Conclusions: This work provides novel insights on the genetic structure of Stx phages, showing a high genetic diversity throughout the genomes, where the various lysis-lysogeny regulatory systems are in contrast with an uncommon, but conserved, lytic system always adjacent to stx genes.This study was supported by the Portuguese Foundation for Science and Technology (FCT) under the scope of the strategic funding of UIDB/04469/2020 unit and the project PhageSTEC PTDC/CVT-CVT/29628/2017 [POCI-01-0145-FEDER-029628] funded by FEDER through COMPETE2020 (Programa Operacional Competitividade e Internacionalização) and by National Funds thought FCT. GP is recipient of a FCT PhD grant with the reference SFRH/BD/117365/2016. The funding body had no role in the design of the study and collection, analysis, and interpretation of data and in writing the manuscriptinfo:eu-repo/semantics/publishedVersionSpringer NatureUniversidade do MinhoPinto, GraçaSampaio, MartaDias, OscarAlmeida, CarinaAzeredo, JoanaOliveira, Hugo Alexandre Mendes20212021-01-01T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/1822/72809engPinto, Graça; Sampaio, Marta; Dias, Oscar; Almeida, Carina; Azeredo, Joana; Oliveira, Hugo, Insights into the genome architecture and evolution of Shiga toxin encoding bacteriophages of Escherichia coli. BMC Genomics, 22(366), 20211471-216410.1186/s12864-021-07685-034011288https://bmcgenomics.biomedcentral.com/articles/10.1186/s12864-021-07685-0info:eu-repo/semantics/openAccessreponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãoinstacron:RCAAP2023-07-21T12:36:13Zoai:repositorium.sdum.uminho.pt:1822/72809Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireopendoar:71602024-03-19T19:32:14.687718Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãofalse |
dc.title.none.fl_str_mv |
Insights into the genome architecture and evolution of Shiga toxin encoding bacteriophages of Escherichia coli |
title |
Insights into the genome architecture and evolution of Shiga toxin encoding bacteriophages of Escherichia coli |
spellingShingle |
Insights into the genome architecture and evolution of Shiga toxin encoding bacteriophages of Escherichia coli Pinto, Graça STEC Shiga toxin-encoding bacteriophages Genomes Clusters Science & Technology |
title_short |
Insights into the genome architecture and evolution of Shiga toxin encoding bacteriophages of Escherichia coli |
title_full |
Insights into the genome architecture and evolution of Shiga toxin encoding bacteriophages of Escherichia coli |
title_fullStr |
Insights into the genome architecture and evolution of Shiga toxin encoding bacteriophages of Escherichia coli |
title_full_unstemmed |
Insights into the genome architecture and evolution of Shiga toxin encoding bacteriophages of Escherichia coli |
title_sort |
Insights into the genome architecture and evolution of Shiga toxin encoding bacteriophages of Escherichia coli |
author |
Pinto, Graça |
author_facet |
Pinto, Graça Sampaio, Marta Dias, Oscar Almeida, Carina Azeredo, Joana Oliveira, Hugo Alexandre Mendes |
author_role |
author |
author2 |
Sampaio, Marta Dias, Oscar Almeida, Carina Azeredo, Joana Oliveira, Hugo Alexandre Mendes |
author2_role |
author author author author author |
dc.contributor.none.fl_str_mv |
Universidade do Minho |
dc.contributor.author.fl_str_mv |
Pinto, Graça Sampaio, Marta Dias, Oscar Almeida, Carina Azeredo, Joana Oliveira, Hugo Alexandre Mendes |
dc.subject.por.fl_str_mv |
STEC Shiga toxin-encoding bacteriophages Genomes Clusters Science & Technology |
topic |
STEC Shiga toxin-encoding bacteriophages Genomes Clusters Science & Technology |
description |
Background: A total of 179 Shiga toxin-producing Escherichia coli (STEC) complete genomes were analyzed in terms of serotypes, prophage coding regions, and stx gene variants and their distribution. We further examined the genetic diversity of Stx-converting phage genomes (Stx phages), focusing on the lysis-lysogeny decision and lytic cassettes. Results: We show that most STEC isolates belong to non-O157 serotypes (73 %), regardless the sources and geographical regions. While the majority of STEC genomes contain a single stx gene (61 %), strains containing two (35 %), three (3 %) and four (1 %) stx genes were also found, being stx2 the most prevalent gene variant. Their location is exclusively found in intact prophage regions, indicating that they are phage-borne. We further demonstrate that Stx phages can be grouped into four clusters (A, B, C and D), three subclusters (A1, A2 and A3) and one singleton, based on their shared gene content. This cluster distribution is in good agreement with their predicted virion morphologies. Stx phage genomes are highly diverse with a vast number of 1,838 gene phamilies (phams) of related sequences (of which 677 are orphams i.e. unique genes) and, although having high mosaicism, they are generally organized into three major transcripts. While the mechanisms that guide lysis–lysogeny decision are complex, there is a strong selective pressure to maintain the stx genes location close to the lytic cassette composed of predicted SAR-endolysin and pin-holin lytic proteins. The evolution of STEC Stx phages seems to be strongly related to acquiring genetic material, probably from horizontal gene transfer events. Conclusions: This work provides novel insights on the genetic structure of Stx phages, showing a high genetic diversity throughout the genomes, where the various lysis-lysogeny regulatory systems are in contrast with an uncommon, but conserved, lytic system always adjacent to stx genes. |
publishDate |
2021 |
dc.date.none.fl_str_mv |
2021 2021-01-01T00:00:00Z |
dc.type.status.fl_str_mv |
info:eu-repo/semantics/publishedVersion |
dc.type.driver.fl_str_mv |
info:eu-repo/semantics/article |
format |
article |
status_str |
publishedVersion |
dc.identifier.uri.fl_str_mv |
http://hdl.handle.net/1822/72809 |
url |
http://hdl.handle.net/1822/72809 |
dc.language.iso.fl_str_mv |
eng |
language |
eng |
dc.relation.none.fl_str_mv |
Pinto, Graça; Sampaio, Marta; Dias, Oscar; Almeida, Carina; Azeredo, Joana; Oliveira, Hugo, Insights into the genome architecture and evolution of Shiga toxin encoding bacteriophages of Escherichia coli. BMC Genomics, 22(366), 2021 1471-2164 10.1186/s12864-021-07685-0 34011288 https://bmcgenomics.biomedcentral.com/articles/10.1186/s12864-021-07685-0 |
dc.rights.driver.fl_str_mv |
info:eu-repo/semantics/openAccess |
eu_rights_str_mv |
openAccess |
dc.format.none.fl_str_mv |
application/pdf |
dc.publisher.none.fl_str_mv |
Springer Nature |
publisher.none.fl_str_mv |
Springer Nature |
dc.source.none.fl_str_mv |
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Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
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