title: Horizontal gene transfer of zinc and non-zinc forms of bacterial ribosomal protein S4.
abstract: BACKGROUND
  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.
  
  
  RESULTS
  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 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.
  
  
  CONCLUSIONS
  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.
authors.affiliation: Center for Biophysics and Computational Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA. kechen2@illinois.edu
authors.forename: Ke
authors.initials: K
authors.lastname: Chen
authors.forename: Elijah
authors.initials: E
authors.lastname: Roberts
authors.forename: Zaida
authors.initials: Z
authors.lastname: Luthey-Schulten
mesh_terms: D000595:Amino Acid Sequence; D001419:Bacteria / Q000145:classification / Q000235:genetics*; D001426:Bacterial Proteins / Q000235:genetics*; D019143:Evolution, Molecular; D022761:Gene Transfer, Horizontal; D005798:Genes, Bacterial; D016680:Genome, Bacterial; D008969:Molecular Sequence Data; D010802:Phylogeny; D012269:Ribosomal Proteins / Q000235:genetics*; D016415:Sequence Alignment; D015032:Zinc
chemical_list: D001426:Bacterial Proteins; D012269:Ribosomal Proteins; C031798:ribosomal protein S4; D015032:Zinc