Genome of the extremely radiation-resistant bacterium Deinococcus radiodurans viewed from the perspective of comparative genomics - PubMed (original) (raw)

Review

Genome of the extremely radiation-resistant bacterium Deinococcus radiodurans viewed from the perspective of comparative genomics

K S Makarova et al. Microbiol Mol Biol Rev. 2001 Mar.

Abstract

The bacterium Deinococcus radiodurans shows remarkable resistance to a range of damage caused by ionizing radiation, desiccation, UV radiation, oxidizing agents, and electrophilic mutagens. D. radiodurans is best known for its extreme resistance to ionizing radiation; not only can it grow continuously in the presence of chronic radiation (6 kilorads/h), but also it can survive acute exposures to gamma radiation exceeding 1,500 kilorads without dying or undergoing induced mutation. These characteristics were the impetus for sequencing the genome of D. radiodurans and the ongoing development of its use for bioremediation of radioactive wastes. Although it is known that these multiple resistance phenotypes stem from efficient DNA repair processes, the mechanisms underlying these extraordinary repair capabilities remain poorly understood. In this work we present an extensive comparative sequence analysis of the Deinococcus genome. Deinococcus is the first representative with a completely sequenced genome from a distinct bacterial lineage of extremophiles, the Thermus-Deinococcus group. Phylogenetic tree analysis, combined with the identification of several synapomorphies between Thermus and Deinococcus, supports the hypothesis that it is an ancient group with no clear affinities to any of the other known bacterial lineages. Distinctive features of the Deinococcus genome as well as features shared with other free-living bacteria were revealed by comparison of its proteome to the collection of clusters of orthologous groups of proteins. Analysis of paralogs in Deinococcus has revealed several unique protein families. In addition, specific expansions of several other families including phosphatases, proteases, acyltransferases, and Nudix family pyrophosphohydrolases were detected. Genes that potentially affect DNA repair and recombination and stress responses were investigated in detail. Some proteins appear to have been horizontally transferred from eukaryotes and are not present in other bacteria. For example, three proteins homologous to plant desiccation resistance proteins were identified, and these are particularly interesting because of the correlation between desiccation and radiation resistance. Compared to other bacteria, the D. radiodurans genome is enriched in repetitive sequences, namely, IS-like transposons and small intergenic repeats. In combination, these observations suggest that several different biological mechanisms contribute to the multiple DNA repair-dependent phenotypes of this organism.

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Figures

FIG. 1

FIG. 1

Examples of unique domain architectures of Deinococcus proteins.

FIG. 2

FIG. 2

Distinct domain architectures of selected proteins implicated in signal transduction in Deinococcus.

FIG. 3

FIG. 3

Specific protein family expansion in Deinococcus.

FIG. 4

FIG. 4

Distinct domain architectures of proteins containing the MutT-like domain. aa, amino acids; SAM, _S_-adenosylmethionine.

FIG. 5

FIG. 5

Multiple alignment of the conserved core of the DinB/YfiT protein family. The alignment was generated by parsing the PSI-BLAST HSPs and realigning them with the ALITRE program (181). The numbers between aligned blocks indicate the lengths of variable inserts that are not shown; the numbers at the end of each sequence indicate the distances from the protein termini to the proximal and distal aligned blocks. The shading of conserved residues is according to the 85% consensus. The three predicted metal ligand residues are shown in inverse shading (white against a black background); Consensus sequence was obtained by a “consensus” program (

http://www.bork.embl-heidelberg.de/Alignment/consensus.html

) with default amino acid grouping assignments (h, s, t, p, +, etc.). The coloring of conserved position is as follows: h, hydrophobic residues (yellow background); s, small residues (bold with green background); t, turn-like residues (bold with cyan background); +, positively charged and polar (red). In front of each sequence, the GenBank identifier number (GI) and a two-letter code of species are shown. DR, D. radiodurans; BS, B. subtilis; SC, Streptomyces coelicolor; MT, M. tuberculosis, Ssp, Synecocystis sp.

FIG. 6

FIG. 6

Multiple alignment of the selected members of the LEA14 family of desiccation related proteins. The numbers and coloring in this alignment are the same as in Fig. 5. The two-letter code for species is as follows: AF, Archaeaoglobus fulgidus; MJ, Methanococcus jannaschii; PH, Pyrococcus horikoshii; PA, Pyrococcus abyssi; PH, Pyrococcus furiosus; AT, Arabidopsis thaliana; LE, Lycopersicon esculentum; CP, Craterostigma plantagineum; PM, Pseudotsuga menziesii.

FIG. 7

FIG. 7

(A) Structure of the full-length repeated member of the SNR2 family. Inverted repeats are marked by arrows. Roman numerals and different colors mark the five conserved modules. (B) Number of SNR2 members with the indicated modular configuration. Each class of module is represented by a different color.

FIG. 8

FIG. 8

Taxonomic affinities of Deinococcus proteins. We defined a hit to a particular lineage as the best one if it had a BLAST E-value for a protein from this lineage 100 times lower than to any protein from another lineage. Hits to Thermus-Deinococcus group species were disregarded.

FIG. 9

FIG. 9

Phylogenetic trees. (A) All ribosomal proteins shared by selected organisms with a completely sequenced genome; (B) all ribosomal proteins shared by Thermus and selected organisms; (C) RNA polymerase subunit A; (D) fragment of RNA polymerase subunit A shared by Thermus and selected organisms. Proteins were aligned by CLUSTALW. Alignments were checked manually, and unaligned fragments were removed. Subsequently, alignments were used for tree reconstruction using the PHYLIP program (default parameters throughout). Abbreviations of species in the trees: Mthe, Methanobacterium thermoautotrophicum; Bsub, B. subtilis; Mpneu, Mycoplasma pneumoniae; Mgen, Mycoplasma genitalium; Mtub, Mycobacterium tuberculosis; Ecol, E. coli; Hinf, Haemophilus influenzae; Rpro, Rickettsia prowazekii; Bbur, Borrelia burgdorferi; Tpal, Treponema pallidum; Hpyl, Helicobacter pylori; Ctra, Chlamydia trachomatis; Synech, Synechocystis sp.; Aaeo, Aquifex aeolicus; Tmar, Thermotoga maritima; The, Thermus thermophilus; Scer, Saccharomyces cerevisiae.

FIG. 10

FIG. 10

Comparison of shared “thermophilic” genes in different species.

References

    1. Agostini H J, Carroll J D, Minton K W. Identification and characterization of uvrA, a DNA repair gene of Deinococcus radiodurans. J Bacteriol. 1996;178:6759–6765. - PMC - PubMed
    1. Aizenman E, Engelberg-Kulka H, Glaser G. An Escherichia coli chromosomal “addiction module” regulated by guanosine [corrected] 3′,5′-bispyrophosphate: a model for programmed bacterial cell death. Proc Natl Acad Sci USA. 1996;93:6059–6063. . (Erratum, 93:9991.) - PMC - PubMed
    1. Al-Bakri G H, Mackay M W, Whittaker P A, Moseley B E. Cloning of the DNA repair genes mtcA, mtcB, uvsC, uvsD, uvsE and the leuB gene from Deinococcus radiodurans. Gene. 1985;33:305–311. - PubMed
    1. Albert S, Bhattacharya D, Klaudiny J, Schmitzova J, Simuth J. The family of major royal jelly proteins and its evolution. J Mol Evol. 1999;49:290–297. - PubMed
    1. Altschul S F, Koonin E V. Iterated profile searches with PSI-BLAST–a tool for discovery in protein databases. Trends Biochem Sci. 1998;23:444–447. - PubMed

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