Comparative genomics of Thermus thermophilus and Deinococcus radiodurans: divergent routes of adaptation to thermophily and radiation resistance

Abstract

Background: Thermus thermophilus and Deinococcus radiodurans belong to a distinct bacterial clade but have remarkably different phenotypes. T. thermophilus is a thermophile, which is relatively sensitive to ionizing radiation and desiccation, whereas D. radiodurans is a mesophile, which is highly radiation- and desiccation-resistant. Here we present an in-depth comparison of the genomes of these two related but differently adapted bacteria.

Results: By reconstructing the evolution of Thermus and Deinococcus after the divergence from their common ancestor, we demonstrate a high level of post-divergence gene flux in both lineages. Various aspects of the adaptation to high temperature in Thermus can be attributed to horizontal gene transfer from archaea and thermophilic bacteria; many of the horizontally transferred genes are located on the single megaplasmid of Thermus. In addition, the Thermus lineage has lost a set of genes that are still present in Deinococcus and many other mesophilic bacteria but are not common among thermophiles. By contrast, Deinococcus seems to have acquired numerous genes related to stress response systems from various bacteria. A comparison of the distribution of orthologous genes among the four partitions of the Deinococcus genome and the two partitions of the Thermus genome reveals homology between the Thermus megaplasmid (pTT27) and Deinococcus megaplasmid (DR177).

Conclusion: After the radiation from their common ancestor, the Thermus and Deinococcus lineages have taken divergent paths toward their distinct lifestyles. In addition to extensive gene loss, Thermus seems to have acquired numerous genes from thermophiles, which likely was the decisive contribution to its thermophilic adaptation. By contrast, Deinococcus lost few genes but seems to have acquired many bacterial genes that apparently enhanced its ability to survive different kinds of environmental stresses. Notwithstanding the accumulation of horizontally transferred genes, we also show that the single megaplasmid of Thermus and the DR177 megaplasmid of Deinococcus are homologous and probably were inherited from the common ancestor of these bacteria.

Figure 1

Radiation resistance of T. thermophilus (ATCC BAA-163), D. radiodurans (ATCC BAA-816) and E. coli (K-12 MG1655, provided by M. Cashel, NIH) (⁶⁰Co irradiation). Standard deviations for the data points are shown.

Figure 2

Desiccation resistance of T. thermophilus (ATCC BAA-163), D. radiodurans (ATCC BAA-816) and E. coli (K-12 MG1655) (room temperature). Note that no surviving cells were obtained for cells desiccated at 65°C. Standard deviations for five data points are shown.

Figure 3

Gene content tree constructed for 66 species included in the COG database on the basis of the patterns of presence-absence in the COGs. The Thermus-Deinococcus clade is marked by bold type. Black, bacteria; yellow, archaea; blue, eukaryotes.

Figure 4

The reconstructed evolutionary scenario for the Thermus-Deinococcus clade. LBCA – Last Bacterial Common Ancestor; DR-TT – the common ancestor of Thermus-Deinococcus clade; TT – T. thermophilus; DR- D. radiodurans. Total number of COGs is shown in boxes for each node. '+' indicates inferred gene (COG) gain, and '-' indicates inferred loss.

Figure 7

A. Organization of genes encoding the putative thermophyle-specific DNA repair system in two Thermus strains and the draft genome of D. geothermalis. The boxes on top of the figure show COG numbers. Genes are shown by block arrows indicating the direction of transcription and identified by their systematic names. For each column of the alignment, the corresponding COG number and predicted function is indicated. D. geothermalis' genes are connected with respective orthologs in both TT strains by a straight line. Generally, orthologous genes are shown by the same color and pattern. The exceptions are the RAMP proteins of COGs 1336, 1367, 1604, 1337 and 1332, which are all shown in pink. Other, more distant RAMPs are also shown in pink, with different patterns [16]. Proteins that do not belong to COGs but have homologs in other species are marked by diamonds. Abbreviations: HEL, predicted helicase, HD nuclease – HD conserved motif containing predicted nuclease conserved region; POL – novel predicted polymerase, RECB – predicted nuclease of RecB family; B. Comparison of gene organization in the region of the megaplasmid coding for reverse gyrase in two TT strains. The shorter gyrase gene in HB27 indicates truncation. Abbreviations: REVGYR, reverse gyrase, MET_PR – predicted metal-dependent protease; REC_DNA – three-domain fusion protein (DnaQ endonuclease, DinG helicase, and RecQ helicase).

Figure 5

Taxonomic affinities of TT and DR proteins. A. Distribution of the numbers of best hits to proteins from thermophiles for core and non-core proteins of DR and TT. B. Distribution of phylogenetic affinities of proteins from the DR-TT core that have best hit to proteins from thermophiles.

Figure 6

Phylogenetic trees for selected TT genes with apparent XGD involving an ortholog from a thermophilic species. Maximum-likelihood unrooted trees were constructed and bootstrap probabilities were computed using the MOLPHY program. Branches with bootstrap probability >70% are marked by black circles. Each leaf is denoted by the standard gene identifier (for the the complete list of correspondence between genes and species, see Additional file 1: "Gene identifiers and species names for figure 6"). The DR and TT genes are boxed. Genes from thermophilic species are shown in red. A. Ribosomal protein L30. B. Ribosomal protein L15. C. Thiamin biosynthesis protein ThiC. D. tRNA thiolation enzyme TtcA.