Horizontal gene transfer of zinc and non-zinc forms of bacterial ribosomal protein S4

<p>Abstract</p> <p>Background</p> <p>The universal ribosomal protein S4 is essential for the initiation of small subunit ribosomal assembly and translational accuracy. Being part of the information processing machinery of the cell, the gene for S4 is generally thought o...

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Main Authors: Luthey-Schulten Zaida, Roberts Elijah, Chen Ke
Format: Article
Language:English
Published: BMC 2009-07-01
Series:BMC Evolutionary Biology
Online Access:http://www.biomedcentral.com/1471-2148/9/179
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spelling doaj-666031228a674a8fa0e06ccceda3c0d12021-09-02T02:45:55ZengBMCBMC Evolutionary Biology1471-21482009-07-019117910.1186/1471-2148-9-179Horizontal gene transfer of zinc and non-zinc forms of bacterial ribosomal protein S4Luthey-Schulten ZaidaRoberts ElijahChen Ke<p>Abstract</p> <p>Background</p> <p>The universal ribosomal protein S4 is essential for the initiation of small subunit ribosomal assembly and translational accuracy. Being part of the information processing machinery of the cell, the gene for S4 is generally thought of as being inherited vertically and has been used in concatenated gene phylogenies. Here we report the evolution of ribosomal protein S4 in relation to a broad sharing of zinc/non-zinc forms of the gene and study the scope of horizontal gene transfer (HGT) of S4 during bacterial evolution.</p> <p>Results</p> <p>In this study we present the complex evolutionary history of ribosomal protein S4 using 660 bacterial genomes from 16 major bacterial phyla. According to conserved characteristics in the sequences, S4 can be classified into C+ (zinc-binding) and C- (zinc-free) variants, with 26 genomes (mainly from the class <it>Clostridia</it>) containing genes for both. A maximum likelihood phylogenetic tree of the S4 sequences was incongruent with the standard bacterial phylogeny, indicating a departure from strict vertical inheritance. Further analysis using the genome content near the S4 genes, which are usually located in a conserved gene cluster, showed not only that HGT of the C- gene had occurred at various stages of bacterial evolution, but also that both the C- and C+ genes were present before the individual phyla diverged. To explain the latter, we theorize that a gene pool existed early in bacterial evolution from which bacteria could sample S4 gene variants, according to environmental conditions. The distribution of the C+/- variants for seven other zinc-binding ribosomal proteins in these 660 bacterial genomes is consistent with that seen for S4 and may shed light on the evolutionary pressures involved.</p> <p>Conclusion</p> <p>The complex history presented for "core" protein S4 suggests the existence of a gene pool before the emergence of bacterial lineages and reflects the pervasive nature of HGT in subsequent bacterial evolution. This has implications for both theoretical models of evolution and practical applications of phylogenetic reconstruction as well as the control of zinc economy in bacterial cells.</p> http://www.biomedcentral.com/1471-2148/9/179
collection DOAJ
language English
format Article
sources DOAJ
author Luthey-Schulten Zaida
Roberts Elijah
Chen Ke
spellingShingle Luthey-Schulten Zaida
Roberts Elijah
Chen Ke
Horizontal gene transfer of zinc and non-zinc forms of bacterial ribosomal protein S4
BMC Evolutionary Biology
author_facet Luthey-Schulten Zaida
Roberts Elijah
Chen Ke
author_sort Luthey-Schulten Zaida
title Horizontal gene transfer of zinc and non-zinc forms of bacterial ribosomal protein S4
title_short Horizontal gene transfer of zinc and non-zinc forms of bacterial ribosomal protein S4
title_full Horizontal gene transfer of zinc and non-zinc forms of bacterial ribosomal protein S4
title_fullStr Horizontal gene transfer of zinc and non-zinc forms of bacterial ribosomal protein S4
title_full_unstemmed Horizontal gene transfer of zinc and non-zinc forms of bacterial ribosomal protein S4
title_sort horizontal gene transfer of zinc and non-zinc forms of bacterial ribosomal protein s4
publisher BMC
series BMC Evolutionary Biology
issn 1471-2148
publishDate 2009-07-01
description <p>Abstract</p> <p>Background</p> <p>The universal ribosomal protein S4 is essential for the initiation of small subunit ribosomal assembly and translational accuracy. Being part of the information processing machinery of the cell, the gene for S4 is generally thought of as being inherited vertically and has been used in concatenated gene phylogenies. Here we report the evolution of ribosomal protein S4 in relation to a broad sharing of zinc/non-zinc forms of the gene and study the scope of horizontal gene transfer (HGT) of S4 during bacterial evolution.</p> <p>Results</p> <p>In this study we present the complex evolutionary history of ribosomal protein S4 using 660 bacterial genomes from 16 major bacterial phyla. According to conserved characteristics in the sequences, S4 can be classified into C+ (zinc-binding) and C- (zinc-free) variants, with 26 genomes (mainly from the class <it>Clostridia</it>) containing genes for both. A maximum likelihood phylogenetic tree of the S4 sequences was incongruent with the standard bacterial phylogeny, indicating a departure from strict vertical inheritance. Further analysis using the genome content near the S4 genes, which are usually located in a conserved gene cluster, showed not only that HGT of the C- gene had occurred at various stages of bacterial evolution, but also that both the C- and C+ genes were present before the individual phyla diverged. To explain the latter, we theorize that a gene pool existed early in bacterial evolution from which bacteria could sample S4 gene variants, according to environmental conditions. The distribution of the C+/- variants for seven other zinc-binding ribosomal proteins in these 660 bacterial genomes is consistent with that seen for S4 and may shed light on the evolutionary pressures involved.</p> <p>Conclusion</p> <p>The complex history presented for "core" protein S4 suggests the existence of a gene pool before the emergence of bacterial lineages and reflects the pervasive nature of HGT in subsequent bacterial evolution. This has implications for both theoretical models of evolution and practical applications of phylogenetic reconstruction as well as the control of zinc economy in bacterial cells.</p>
url http://www.biomedcentral.com/1471-2148/9/179
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