Specialization Of Bacterial DnaE Polymerases And Contributions To Bacterial Genome Evolution

Although it has already been well documented that, in contrast to translation and transcription systems, DNA replication systems are not universally conserved among the three domains of life (Bacteria, Archaea, and Eukaryotes), it came as a great surprise that even within eubacteria the functional DNA polymerase dimers may be encoded by different genes. Here, by a large-scale comparative analysis we found that there are mainly two types of replication systems, symmetric dnaE1-dnaE1and asymmetric polC-dnaE3、reponsible for leading and lagging strand, respectively. By combining the presence of dnaE2or TLS polV, we further dividived the eubacteria into three categories, i.e., dnaEl-dnaE1|polV, dnaE1-dnaE1|dnaE2, and polC-dnaE3|polV. Besides, we provided more potential evidences indicating that it is mainly dnaE2and polC which are navigating GC and AT increase, respectively. Other factors like mutator gene defect, genome size, oxygen requirement, and environment, etc. only play subsidiary roles in casting the coin. In addition, we extended our analysis to strand-biased nucleotide composition and gene distribution and found that the compositional alpha-dimer asymmetry also has a fundamental role in shaping the strand-biased nucleotide composition which in turn leads to the more biased gene distribution in polC group bacteria. What’s more, by combining the sequential, structural, functional and distributional disparities, we proposed two most possible models, namely, dnaEl-first and polC-first model, elucidating the origin order of all four kinds of dnaE polymerases and discussed their potential implications for bacterial genome evolution in details. According to the first model, the dnaE1-bearing ancestor of bacteria should have a medium GC content and is evolving toward two opposite directions, one along the GC rich route because of dnaE2insertion whereas the other towards GC poor because of polC insertion. According to the second scenario, the bacteria are evolving mono-directional form GC poor to GC rich and to GC poor again in partial bacteria because of host/enviroment changes and dramatic genome reduction. We also provided potential evidences that indicating that dnaE2is a hidden hero playing crucial roles in bacterial land colonization. Finally, we found dnaEl and dnaE3are another groups of gene markers that are very useful in constructing bacterial phylogeny. We believe these results will provide deep insights for our understanding of bacterial genome evolution and will also be helpful for the following protein structure and function investigations.