Distinct co-evolution patterns of genes associated to DNA polymerase III DnaE and PolC

BMC Genomics. 2012 Feb 14:13:69. doi: 10.1186/1471-2164-13-69.

Abstract

Background: Bacterial genomes displaying a strong bias between the leading and the lagging strand of DNA replication encode two DNA polymerases III, DnaE and PolC, rather than a single one. Replication is a highly unsymmetrical process, and the presence of two polymerases is therefore not unexpected. Using comparative genomics, we explored whether other processes have evolved in parallel with each polymerase.

Results: Extending previous in silico heuristics for the analysis of gene co-evolution, we analyzed the function of genes clustering with dnaE and polC. Clusters were highly informative. DnaE co-evolves with the ribosome, the transcription machinery, the core of intermediary metabolism enzymes. It is also connected to the energy-saving enzyme necessary for RNA degradation, polynucleotide phosphorylase. Most of the proteins of this co-evolving set belong to the persistent set in bacterial proteomes, that is fairly ubiquitously distributed. In contrast, PolC co-evolves with RNA degradation enzymes that are present only in the A+T-rich Firmicutes clade, suggesting at least two origins for the degradosome.

Conclusion: DNA replication involves two machineries, DnaE and PolC. DnaE co-evolves with the core functions of bacterial life. In contrast PolC co-evolves with a set of RNA degradation enzymes that does not derive from the degradosome identified in gamma-Proteobacteria. This suggests that at least two independent RNA degradation pathways existed in the progenote community at the end of the RNA genome world.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacteria / enzymology*
  • Bacteria / genetics*
  • Bacterial Proteins / genetics*
  • DNA Polymerase III / genetics*
  • DNA-Directed DNA Polymerase / genetics*
  • Endoribonucleases / genetics
  • Evolution, Molecular*
  • Genes, Bacterial / genetics*
  • Genomics
  • Multienzyme Complexes / genetics
  • Phylogeny
  • Polyribonucleotide Nucleotidyltransferase / genetics
  • RNA Helicases / genetics

Substances

  • Bacterial Proteins
  • Multienzyme Complexes
  • degradosome
  • DNA polymerase III, alpha subunit
  • PolC protein, bacteria
  • DNA Polymerase III
  • DNA-Directed DNA Polymerase
  • Polyribonucleotide Nucleotidyltransferase
  • Endoribonucleases
  • RNA Helicases