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Phylogenetic and Complementation Analysis of a Single-Stranded DNA Binding Protein Family from Lactococcal Phages Indicates a Non-Bacterial Origin

BACKGROUND: The single-stranded-nucleic acid binding (SSB) protein superfamily includes proteins encoded by different organisms from Bacteria and their phages to Eukaryotes. SSB proteins share common structural characteristics and have been suggested to descend from an ancestor polypeptide. However,...

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Autores principales: Szczepankowska, Agnieszka K., Prestel, Eric, Mariadassou, Mahendra, Bardowski, Jacek K., Bidnenko, Elena
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2011
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3208561/
https://www.ncbi.nlm.nih.gov/pubmed/22073223
http://dx.doi.org/10.1371/journal.pone.0026942
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author Szczepankowska, Agnieszka K.
Prestel, Eric
Mariadassou, Mahendra
Bardowski, Jacek K.
Bidnenko, Elena
author_facet Szczepankowska, Agnieszka K.
Prestel, Eric
Mariadassou, Mahendra
Bardowski, Jacek K.
Bidnenko, Elena
author_sort Szczepankowska, Agnieszka K.
collection PubMed
description BACKGROUND: The single-stranded-nucleic acid binding (SSB) protein superfamily includes proteins encoded by different organisms from Bacteria and their phages to Eukaryotes. SSB proteins share common structural characteristics and have been suggested to descend from an ancestor polypeptide. However, as other proteins involved in DNA replication, bacterial SSB proteins are clearly different from those found in Archaea and Eukaryotes. It was proposed that the corresponding genes in the phage genomes were transferred from the bacterial hosts. Recently new SSB proteins encoded by the virulent lactococcal bacteriophages (Orf14(bIL67)-like proteins) have been identified and characterized structurally and biochemically. METHODOLOGY/PRINCIPAL FINDINGS: This study focused on the determination of phylogenetic relationships between Orf14(bIL67)-like proteins and other SSBs. We have performed a large scale phylogenetic analysis and pairwise sequence comparisons of SSB proteins from different phyla. The results show that, in remarkable contrast to other phage SSBs, the Orf14(bIL67)–like proteins form a distinct, self-contained and well supported phylogenetic group connected to the archaeal SSBs. Functional studies demonstrated that, despite the structural and amino acid sequence differences from bacterial SSBs, Orf14(bIL67) protein complements the conditional lethal ssb-1 mutation of Escherichia coli. CONCLUSIONS/SIGNIFICANCE: Here we identified for the first time a group of phages encoded SSBs which are clearly distinct from their bacterial counterparts. All methods supported the recognition of these phage proteins as a new family within the SSB superfamily. Our findings suggest that unlike other phages, the virulent lactococcal phages carry ssb genes that were not acquired from their hosts, but transferred from an archaeal genome. This represents a unique example of a horizontal gene transfer between Archaea and bacterial phages.
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spelling pubmed-32085612011-11-09 Phylogenetic and Complementation Analysis of a Single-Stranded DNA Binding Protein Family from Lactococcal Phages Indicates a Non-Bacterial Origin Szczepankowska, Agnieszka K. Prestel, Eric Mariadassou, Mahendra Bardowski, Jacek K. Bidnenko, Elena PLoS One Research Article BACKGROUND: The single-stranded-nucleic acid binding (SSB) protein superfamily includes proteins encoded by different organisms from Bacteria and their phages to Eukaryotes. SSB proteins share common structural characteristics and have been suggested to descend from an ancestor polypeptide. However, as other proteins involved in DNA replication, bacterial SSB proteins are clearly different from those found in Archaea and Eukaryotes. It was proposed that the corresponding genes in the phage genomes were transferred from the bacterial hosts. Recently new SSB proteins encoded by the virulent lactococcal bacteriophages (Orf14(bIL67)-like proteins) have been identified and characterized structurally and biochemically. METHODOLOGY/PRINCIPAL FINDINGS: This study focused on the determination of phylogenetic relationships between Orf14(bIL67)-like proteins and other SSBs. We have performed a large scale phylogenetic analysis and pairwise sequence comparisons of SSB proteins from different phyla. The results show that, in remarkable contrast to other phage SSBs, the Orf14(bIL67)–like proteins form a distinct, self-contained and well supported phylogenetic group connected to the archaeal SSBs. Functional studies demonstrated that, despite the structural and amino acid sequence differences from bacterial SSBs, Orf14(bIL67) protein complements the conditional lethal ssb-1 mutation of Escherichia coli. CONCLUSIONS/SIGNIFICANCE: Here we identified for the first time a group of phages encoded SSBs which are clearly distinct from their bacterial counterparts. All methods supported the recognition of these phage proteins as a new family within the SSB superfamily. Our findings suggest that unlike other phages, the virulent lactococcal phages carry ssb genes that were not acquired from their hosts, but transferred from an archaeal genome. This represents a unique example of a horizontal gene transfer between Archaea and bacterial phages. Public Library of Science 2011-11-04 /pmc/articles/PMC3208561/ /pubmed/22073223 http://dx.doi.org/10.1371/journal.pone.0026942 Text en Szczepankowska et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Szczepankowska, Agnieszka K.
Prestel, Eric
Mariadassou, Mahendra
Bardowski, Jacek K.
Bidnenko, Elena
Phylogenetic and Complementation Analysis of a Single-Stranded DNA Binding Protein Family from Lactococcal Phages Indicates a Non-Bacterial Origin
title Phylogenetic and Complementation Analysis of a Single-Stranded DNA Binding Protein Family from Lactococcal Phages Indicates a Non-Bacterial Origin
title_full Phylogenetic and Complementation Analysis of a Single-Stranded DNA Binding Protein Family from Lactococcal Phages Indicates a Non-Bacterial Origin
title_fullStr Phylogenetic and Complementation Analysis of a Single-Stranded DNA Binding Protein Family from Lactococcal Phages Indicates a Non-Bacterial Origin
title_full_unstemmed Phylogenetic and Complementation Analysis of a Single-Stranded DNA Binding Protein Family from Lactococcal Phages Indicates a Non-Bacterial Origin
title_short Phylogenetic and Complementation Analysis of a Single-Stranded DNA Binding Protein Family from Lactococcal Phages Indicates a Non-Bacterial Origin
title_sort phylogenetic and complementation analysis of a single-stranded dna binding protein family from lactococcal phages indicates a non-bacterial origin
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3208561/
https://www.ncbi.nlm.nih.gov/pubmed/22073223
http://dx.doi.org/10.1371/journal.pone.0026942
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