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Comparative genomic analysis of 142 bacteriophages infecting Salmonella enterica subsp. enterica

BACKGROUND: Bacteriophages are bacterial parasites and are considered the most abundant and diverse biological entities on the planet. Previously we identified 154 prophages from 151 serovars of Salmonella enterica subsp. enterica. A detailed analysis of Salmonella prophage genomics is required give...

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Autores principales: Gao, Ruimin, Naushad, Sohail, Moineau, Sylvain, Levesque, Roger, Goodridge, Lawrence, Ogunremi, Dele
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
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Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7251866/
https://www.ncbi.nlm.nih.gov/pubmed/32456612
http://dx.doi.org/10.1186/s12864-020-6765-z
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author Gao, Ruimin
Naushad, Sohail
Moineau, Sylvain
Levesque, Roger
Goodridge, Lawrence
Ogunremi, Dele
author_facet Gao, Ruimin
Naushad, Sohail
Moineau, Sylvain
Levesque, Roger
Goodridge, Lawrence
Ogunremi, Dele
author_sort Gao, Ruimin
collection PubMed
description BACKGROUND: Bacteriophages are bacterial parasites and are considered the most abundant and diverse biological entities on the planet. Previously we identified 154 prophages from 151 serovars of Salmonella enterica subsp. enterica. A detailed analysis of Salmonella prophage genomics is required given the influence of phages on their bacterial hosts and should provide a broader understanding of Salmonella biology and virulence and contribute to the practical applications of phages as vectors and antibacterial agents. RESULTS: Here we provide a comparative analysis of the full genome sequences of 142 prophages of Salmonella enterica subsp. enterica which is the full complement of the prophages that could be retrieved from public databases. We discovered extensive variation in genome sizes (ranging from 6.4 to 358.7 kb) and guanine plus cytosine (GC) content (ranging from 35.5 to 65.4%) and observed a linear correlation between the genome size and the number of open reading frames (ORFs). We used three approaches to compare the phage genomes. The NUCmer/MUMmer genome alignment tool was used to evaluate linkages and correlations based on nucleotide identity between genomes. Multiple sequence alignment was performed to calculate genome average nucleotide identity using the Kalgin program. Finally, genome synteny was explored using dot plot analysis. We found that 90 phage genome sequences grouped into 17 distinct clusters while the remaining 52 genomes showed no close relationships with the other phage genomes and are identified as singletons. We generated genome maps using nucleotide and amino acid sequences which allowed protein-coding genes to be sorted into phamilies (phams) using the Phamerator software. Out of 5796 total assigned phamilies, one phamily was observed to be dominant and was found in 49 prophages, or 34.5% of the 142 phages in our collection. A majority of the phamilies, 4330 out of 5796 (74.7%), occurred in just one prophage underscoring the high degree of diversity among Salmonella bacteriophages. CONCLUSIONS: Based on nucleotide and amino acid sequences, a high diversity was found among Salmonella bacteriophages which validate the use of prophage sequence analysis as a highly discriminatory subtyping tool for Salmonella. Thorough understanding of the conservation and variation of prophage genomic characteristics will facilitate their rational design and use as tools for bacterial strain construction, vector development and as anti-bacterial agents.
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spelling pubmed-72518662020-06-07 Comparative genomic analysis of 142 bacteriophages infecting Salmonella enterica subsp. enterica Gao, Ruimin Naushad, Sohail Moineau, Sylvain Levesque, Roger Goodridge, Lawrence Ogunremi, Dele BMC Genomics Research Article BACKGROUND: Bacteriophages are bacterial parasites and are considered the most abundant and diverse biological entities on the planet. Previously we identified 154 prophages from 151 serovars of Salmonella enterica subsp. enterica. A detailed analysis of Salmonella prophage genomics is required given the influence of phages on their bacterial hosts and should provide a broader understanding of Salmonella biology and virulence and contribute to the practical applications of phages as vectors and antibacterial agents. RESULTS: Here we provide a comparative analysis of the full genome sequences of 142 prophages of Salmonella enterica subsp. enterica which is the full complement of the prophages that could be retrieved from public databases. We discovered extensive variation in genome sizes (ranging from 6.4 to 358.7 kb) and guanine plus cytosine (GC) content (ranging from 35.5 to 65.4%) and observed a linear correlation between the genome size and the number of open reading frames (ORFs). We used three approaches to compare the phage genomes. The NUCmer/MUMmer genome alignment tool was used to evaluate linkages and correlations based on nucleotide identity between genomes. Multiple sequence alignment was performed to calculate genome average nucleotide identity using the Kalgin program. Finally, genome synteny was explored using dot plot analysis. We found that 90 phage genome sequences grouped into 17 distinct clusters while the remaining 52 genomes showed no close relationships with the other phage genomes and are identified as singletons. We generated genome maps using nucleotide and amino acid sequences which allowed protein-coding genes to be sorted into phamilies (phams) using the Phamerator software. Out of 5796 total assigned phamilies, one phamily was observed to be dominant and was found in 49 prophages, or 34.5% of the 142 phages in our collection. A majority of the phamilies, 4330 out of 5796 (74.7%), occurred in just one prophage underscoring the high degree of diversity among Salmonella bacteriophages. CONCLUSIONS: Based on nucleotide and amino acid sequences, a high diversity was found among Salmonella bacteriophages which validate the use of prophage sequence analysis as a highly discriminatory subtyping tool for Salmonella. Thorough understanding of the conservation and variation of prophage genomic characteristics will facilitate their rational design and use as tools for bacterial strain construction, vector development and as anti-bacterial agents. BioMed Central 2020-05-26 /pmc/articles/PMC7251866/ /pubmed/32456612 http://dx.doi.org/10.1186/s12864-020-6765-z Text en © The Author(s). 2020 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. 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 in a credit line to the data.
spellingShingle Research Article
Gao, Ruimin
Naushad, Sohail
Moineau, Sylvain
Levesque, Roger
Goodridge, Lawrence
Ogunremi, Dele
Comparative genomic analysis of 142 bacteriophages infecting Salmonella enterica subsp. enterica
title Comparative genomic analysis of 142 bacteriophages infecting Salmonella enterica subsp. enterica
title_full Comparative genomic analysis of 142 bacteriophages infecting Salmonella enterica subsp. enterica
title_fullStr Comparative genomic analysis of 142 bacteriophages infecting Salmonella enterica subsp. enterica
title_full_unstemmed Comparative genomic analysis of 142 bacteriophages infecting Salmonella enterica subsp. enterica
title_short Comparative genomic analysis of 142 bacteriophages infecting Salmonella enterica subsp. enterica
title_sort comparative genomic analysis of 142 bacteriophages infecting salmonella enterica subsp. enterica
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7251866/
https://www.ncbi.nlm.nih.gov/pubmed/32456612
http://dx.doi.org/10.1186/s12864-020-6765-z
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