Deinococcus geothermalis: the pool of extreme radiation resistance genes shrinks.
Bacteria of the genus Deinococcus are extremely resistant to ionizing radiation (IR), ultraviolet light (UV) and desiccation. The mesophile Deinococcus radiodurans was the first member of this group whose genome was completely sequenced. Analysis of the genome sequence of D. radiodurans, however, failed to identify unique DNA repair systems. To further delineate the genes underlying the resistance phenotypes, we report the whole-genome sequence of a second Deinococcus species, the thermophile Deinococcus geothermalis, which at its optimal growth temperature is as resistant to IR, UV and desiccation as D. radiodurans, and a comparative analysis of the two Deinococcus genomes. Many D. radiodurans genes previously implicated in resistance, but for which no sensitive phenotype was observed upon disruption, are absent in D. geothermalis. In contrast, most D. radiodurans genes whose mutants displayed a radiation-sensitive phenotype in D. radiodurans are conserved in D. geothermalis. Supporting the existence of a Deinococcus radiation response regulon, a common palindromic DNA motif was identified in a conserved set of genes associated with resistance, and a dedicated transcriptional regulator was predicted. We present the case that these two species evolved essentially the same diverse set of gene families, and that the extreme stress-resistance phenotypes of the Deinococcus lineage emerged progressively by amassing cell-cleaning systems from different sources, but not by acquisition of novel DNA repair systems. Our reconstruction of the genomic evolution of the Deinococcus-Thermus phylum indicates that the corresponding set of enzymes proliferated mainly in the common ancestor of Deinococcus. Results of the comparative analysis weaken the arguments for a role of higher-order chromosome alignment structures in resistance; more clearly define and substantially revise downward the number of uncharacterized genes that might participate in DNA repair and contribute to resistance; and strengthen the case for a role in survival of systems involved in manganese and iron homeostasis.
Makarova
Kira S
KS
National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Maryland, USA. makarova@ncbi.nlm.nih.gov
Omelchenko
Marina V
MV
Gaidamakova
Elena K
EK
Matrosova
Vera Y
VY
Vasilenko
Alexander
A
Zhai
Min
M
Lapidus
Alla
A
Copeland
Alex
A
Kim
Edwin
E
Land
Miriam
M
Mavrommatis
Konstantinos
K
Pitluck
Samuel
S
Richardson
Paul M
PM
Detter
Chris
C
Brettin
Thomas
T
Saunders
Elizabeth
E
Lai
Barry
B
Ravel
Bruce
B
Kemner
Kenneth M
KM
Wolf
Yuri I
YI
Sorokin
Alexander
A
Gerasimova
Anna V
AV
Gelfand
Mikhail S
MS
Fredrickson
James K
JK
Koonin
Eugene V
EV
Daly
Michael J
MJ
D000595:Amino Acid Sequence; D002876:Chromosomes, Bacterial / Q000235:genetics / Q000528:radiation effects; D004269:DNA, Bacterial / Q000235:genetics; D034301:Deinococcus / Q000235:genetics* / Q000528:radiation effects*; D005798:Genes, Bacterial / Q000235:genetics; D016680:Genome, Bacterial; D007259:Infrared Rays; D008969:Molecular Sequence Data; D016133:Polymerase Chain Reaction; D017386:Sequence Homology, Amino Acid; D013052:Spectrometry, X-Ray Emission; D014466:Ultraviolet Rays
D004269:DNA, Bacterial