Abstract
BackgroundThe 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.ResultsIn 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 Clostridia) 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.ConclusionThe 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.
Highlights
The universal ribosomal protein S4 is essential for the initiation of small subunit ribosomal assembly and translational accuracy
Considering the fact that the S4 gene is part of a highly conserved gene cluster in bacteria consisting of the S10-spc-α operons [27], we see surprising evidence for the endogenous origin of the C- form in some phyla and hypothesize that both the C+ and C- forms may have been present before the bacterial phyla diverged with different lineages sampling from the variants according to the local environment. In accordance with this hypothesis, we present evidence that C- paralogous copies in genomes containing both variants of S4, as well as all S4 genes outside the α-operon, are results of horizontal gene transfer (HGT) events
Sequence alignment and classification of bacterial rprotein S4 To study the history of S4 in bacteria, we first extracted 688 sequences of S4 and paralogs from 660 complete and draft bacterial genomes
Summary
The universal ribosomal protein S4 is essential for the initiation of small subunit ribosomal assembly and translational accuracy. The ribosome is an elaborate ribonucleoprotein complex whose evolution is intrinsically linked with that of the cell It has been recognized since the 1970's that the molecular core of the ribosome was in place before the divergence of the three primary organismal lineages, Bacteria, Archaea, and Eucarya (the domains of life). Despite conservation of a large portion of the ribosomal structure among the lineages, the ribosomes of each domain of life contain certain sequence and structural signatures that are unique to and constant within the domain Such signatures have been identified in both the rRNA and ribosomal proteins (r-proteins), including many r-proteins that are specific to one of the primary lineages. Studying the pattern by which such a signature spread among the evolving lineages can help resolve the dynamics of the evolutionary process at the time
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