GENOMIC CONFESSION OF Deinococcus radiodurans: IT STARTED OUT AS A
RADIATION RESISTANT ORGANISM
Haïtham Sghaier1,2, Hiroshi Mitomo2 and Issay Narumi1*
1

Research Group for Gene Resources, Japan Atomic Energy Agency, 1233 Watanuki, Takasaki, Gunma
370-1292, Japan
2

Material Science Laboratory, Department of Biological and Chemical Engineering, Faculty ofEngineering, Gunma University, 1-5-1 Tenjin, Kiryu, Gunma 376-8515, Japan
Fax: +81-27-346-9688
Email: narumi.issei@jaea.go.jp (Issay Narumi)(Received 6 October, 2005 Accepted 16 November, 2005)(Abstract)
Previously, analyses of ionizing-radiation-sensitive mutants of Deinococcus radiodurans andinvestigation into the genomic expression profile of the wild-type organism indicated a positive
correlation between radiation resistance and desiccation tolerance phenotypes.

Mainly because aterrestrial selective force for acquiring resistance to ionizing radiation was unfound, it has been assumed
that the radiation resistance of D. radiodurans is an incidental phenotype due to its anhydrobiosis defense
abilities. Here, following the stratification of the D. radiodurans genome, we discuss these issues fromevolutionary, genomic, and experimental perspectives.

Through the data collected we propose areconciliatory model wherein radiation resistance is a unique molecular reflection of the early Earthresilience and desiccation tolerance is a mark of cells that colonized land during the Archaean epoch.

(Keywords)
desiccation tolerance, early ancestral genes, gene sharing, genome categorization, land colonization,
radiation resistance

Viva Origino Vol.33 No.4 (2005) 243-257© 2005 by SSOEL Japan-243-

Viva Origino 33 (2005) 243-257

Introduction

and

his

colleague

hypothesized

that

D.

radiodurans is an organism that has adapted to
Deinococcus radiodurans is a nonsporing

dehydration and that its DNA repair ability is aeubacteria-type organism that is characterized bymanifestation of that evolutionary adaptation

extreme resistance to a variety of DNA-damaging(desiccation

agents, with an unusually high resistance toTranscriptome analysis revealed a significant

ionizing radiation [1]. The most striking featureoverlap in the gene expression profiles of D.

of D. radiodurans is its capacity for repairingradiodurans cultures recovering from ionizing

ionizing-radiation-induced DNA double-strand

radiation and desiccation. During the first hour

breaks.

after a sublethal dose of ionizing radiation, 72

This bacterium can mend over 100

genomic DNA double-strand breaks

adaptation

hypothesis)[3].

duringgenes were upregulated in D. radiodurans.

post-irradiation incubation, whereas just few

Thirty-three of these loci were also among a set of

double-strand breaks are lethal in Escherichia coli

73 genes expressed in D. radiodurans cultures[2].

recoveringTheionizing-radiation

This
that

showedradiodurans has been considered to be difficult toionizing-radiation

resistanceandexplain from an evolutionary point of view.

tolerance are functionally interrelated phenomena

Battista and his colleague [3] argued that thefor D. radiodurans. However, it does not provide

radiation resistance of D. radiodurans might be aany substantial evidence for the desiccation

fortuitous consequence of an evolutionary processadaptationthat permitted this bacterium to cope with an

ionizing-radiation-resistant fractions of two soil

environmental stress other than ionizing radiation

bacterial communities were investigated byfor the following reason: (1) there is no selective

exposing an arid soil from desert area and aadvantage to being ionizing-radiation-resistant innonarid soil from forest area to ionizing radiation

the natural world, (2) there is no terrestrial[5].

environment that generates such a high flux ofargued that recovery of large numbers ofionizing radiation.

Based on their experiments

ionizing-radiation-resistant bacteria including new

showing that dehydration induces DNA damage

species of the genus Deinococcus from arid soil

including DNA double-strand breaks in D.

and not from nonarid soil provides ecologicalradiodurans

almostsupport for the desiccation adaptation hypothesis.

thisHowever, all the data cannot rule out a possibility

thatmutants

of

D.

[4].

clearly

ionizing-radiation-sensitiveofdesiccation

experiments

andresistancefrombacterium are sensitive to desiccation, Battista

-244-

that

hypothesis.

desiccation

Recently,the

The authors of the above investigation

earlybacterial

community

acquiredViva Origino 33 (2005) 243-257

ionizing-radiation resistance prior to acquisition

genomes with which it finds a match. An ORF

of desiccation tolerance.

found only within members of the genus

Luckily,

ancient

events

to

which

D.

Deinococcus, for instance, would have a lower

radiodurans was subjected during its evolution

value for ES than an ORF distributed more

can be theoretically reconstructed on the basis ofbroadly [6]. Through analysis of D. radiodurans

its present-day genome sequence.

We havegenome using PDS and ES values, we haveaddressed this problem by considering that thegathered evidence that contradicts the desiccation

history of each open reading frame (ORF) in D.

adaptation hypothesis, and we have proposed aradiodurans could be defined based on the degree

new model. In this model, the radiation resistanceto which it reflects the whole genome evolutionof D. radiodurans is a unique molecular reflection

and the genomes with which it finds a match.

of the early Earth resilience and its desiccation

Charlebois et al. [6] has developed a system, thetolerance is a mark of cells that colonized land

NeuroGadgets

Bioinformatics

Webduring the Archaean epoch.

(NGIBWS),

specializinginevolutionary

genomics.

Servicemicrobial

First,

the

Methods‘phylogenetically discordant sequence’ (PDS)
option within NGIBWS determines if the ORF

PDS and ES values were obtained using the

evolved concordantly (core gene pool) with the

NeuroGadgets

rest of the genome.

(http://www.neurogadgets.com)

Phylogenetic discordance

Inc.

well

service[6].

correlatedTo

among ORFs (discordant gene pool) in D.

determineradiodurans was assessed by comparison of theirrelationships to its orthologs in other species, PDS

rankings using a defined statistical strategy.

values were calculated with BLASTP (1e–5). A

Generally, removal of PDSs should leave sets of

PDS is defined as an ORF that exhibits patterns ofgenes which, analyzed jointly, should yield asimilarity

phylogeny that better corresponds with thedistinguishable from those of most other ORFs in

phylogenetic grouping of D. radiodurans. Also,

the same genome, and therefore confuse genome

PDSs, as they include many true species-specificphylogenies.

genes, are a useful genomic measure for studying

ORFs was assessed by statistical comparison of

the evolutionary forces that shaped the genome of

their rankings. Thus, a high PDS value indicates

D. radiodurans [7].

Second, the ‘evolutionarythat the gene's relationships track the genome's

scope’ (ES) option is a measure of the mean

relationships well [7]. ES of an ORF's matches

distance, computed from the mean normalized

was computed as the mean distance between D.

BLASTP, between an ORF’s genome and theradiodurans and 233 complete genomes available

-245-

how

web

relationships

agene'sstatisticallyPhylogenetic discordance among

Viva Origino 33 (2005) 243-257

for analysis (206 Eubacteria, 21 Archaea, 6(http://129.79.232.60/islands/Dra18R.html) [10].

Eukaryota) using the genomic distance matrix

For proteic analysis we employed a clustering

calculated at a BLASTP cutoff e-value of 1e–5.

algorithm

If an ORF from D. radiodurans does not match[11]. Proteic families and domains were obtained

any other ORF from available species, then ES

using Superfamily [12].

value of that ORF is equal to zero. In this report,

genes was used here to describe any genomic

an ORF’s PDS and ES values are indicated withinsegment of DNA containing adjacent ORFs thatbrackets as follow: [PDS, ES].

can be transcribed together.

To identify(http://www.protonet.cs.huji.ac.il./)

The term cluster oflaterally transferred alien genes and genomic
islands (GIs) we performed analyses based on
statistical

Results

parameters(http://www.fut.es/~debb/HGT/) [8], dinucleotide

To probe early evolutionary history of D.

bias

radiodurans, PDS (from -1 to 1) against ES (from(http://www.pathogenomics.sfu.ca/islandpath) [9],0 to 0.77) values of 3182 ORFs were plottedand(Figure 1).

integration

sites

PDS against ES plot shows four

Figure 1. PDS/ES plot of D. radiodurans R1.
Using PDS values ranging from –1 to 1 on the horizontal axis and ES values from 0 to 0.77 on the vertical axis
3182 ORFs from D. radiodurans were plotted. Plots reveal that the genome of D. radiodurans is characterized
by the presence of four evolutionary families (I, II, III, and IV) containing 2198, 249, 63, and 672 ORFs,
respectively. The first evolutionary family represents the core gene pool of D. radiodurans. The second, third,
and fourth evolutionary families form the discordant gene pool of D. radiodurans. These four families are
separated by three gaps reflecting that they were shaped through distinct genetic sources and pathways under
different pressure forces.

-246-

Viva Origino 33 (2005) 243-257

evolutionary families (I, II, III, and IV) containing

involving 27 proteic superfamilies, that were2198, 249, 63, and 672 ORFs, respectively.

unfound in other genomes. Interestingly, DR0467

These four families are separated by three gaps

issuggesting that the selective forces shaping thepolymerase beta domain adjacent to Rad51

evolution of D. radiodurans total gene pool set

domainhave not been uniform. One possibility is that

nucleotidyltransferase domain as a core string,these lacuna represent major evolutionary events

andduring which many preexisting genes or part of

Phosphatase) domain as a C-terminal chain.

ahypothetical

in

PHP

proteinits(Polymerase

that

has

DNA

N-terminal

and

side,

Histidinol

them were transformed to produce new functions

Secondly, D. radiodurans developed newwith more complex regulations, a phenomenon

regulatory pathways governed by pprI (DR0167

called “molecular tinkering/opportunism” [13].

[–1, 0.70]), a general switch for DNA repair [16],Correlated to PDS and ES values, D. radiodurans

within an extensive network of orphan genes, andgenome exhibits at least two strategies related toa laterally acquired genomic island R1GI1“molecular opportunism”: (i) domain duplication,(DR0511-DR0533) tailed with an alien genes

differentiation, combination, and fusion, and (ii)segment (DR0534-DR0547).

rapid evolution and lateral gene transfer.

The first evolutionary family, with high PDS

The first strategy is exemplified with the(> 0) and ES (> 0.65) values, represents the coreancient duplication event of mutS1 (DR1039 [0.50,

gene pool of D. radiodurans.

0.71]) and mutS2 (DR1976 [0.99, 0.71]) [14].

including the minimal set of essential genes,

Also, for example, D. radiodurans tyrosine

shouldrecombinases (DR1555 [0.22, 0.71], DRA0155“organismal sporadic matches set” because it[0.31, 0.71], DRB0104 [0.98, 0.71], DRC0018

represents the subset of genes shared by distinct[0.18, 0.71]) and topoisomerase IB (DR0690

organisms.

[0.98, 0.70]) evolved by differentiation of the C

includes two categories of ORFs depending on

terminal followed by gene fusion [15]. Moreover,whether ES value is inferior or superior to 0.71.

D. radiodurans has 16 domain combination pairs,

Generally, ORFs with ES value superior to 0.71

including DRA0207 [–1, 0], DRA0297 [0.57,(1503 ORFs) code for very ancient enzymes

0.70], DR0603 [0.55, 0.71], DR2168 [0.98, 0.70],

shared among the three primary kingdoms of all

DRA0202 [0.94, 0.71], DR1103 [1, 0.71],

extant organisms, with the potential existence of

DR0467 [0.99, 0.71], DR1417 [0.99, 0.70],

aboriginal lateral gene transfer events.

DR2168 [0.98, 0.70], DR1252 [0.16, 0.71],

number of genes in this subset is almost identical

DR2506 [0.86, 0.69], DR1247 [0.99, 0.71],

to that of the smallest sequenced genome of a

DR0337free-living organism, Thermoplasma acidophilum[–1,0.69],

DR0058[0.99,

0.71]

-247-

be

preferentially

Such a core,

perceivedasan

We observed that the first family

TheViva Origino 33 (2005) 243-257(1482 genes). For example, glutamine synthase

implicated in D. radiodurans radiation resistance(DR0451 [0.28, 0.71] and DR2033 [0.52, 0.71]),or desiccation tolerance, but it includes a

RecA (DR2340 [1, 0.71]), GTP-binding protein

hypothetical protein (DR0060 [–1, 0.57]) withObg (DR0084 [1, 0.71]), ribosomal protein S12

FAD binding domain of DNA photolyase. The(DR0305 [0.99, 0.71]), (DR2128 [1, 0.71]),

fourth family [–1, 0] is composed of 672 genes

NAD-dependent ligase (DR2069 [1, 0.71]), andthat orphan genes [21, 22] form the majority.

ribonuclease PH (DR1585 [0.98, 0.71]) are early

In a previous DNA microarray analysis [4], 40

ancient gene candidates based on [PDS, ES]

ORFs were implied as specific, because they werecriterion, a candidacy supported by other data [17,undetected18]. Proteins with ES value strictly inferior todesiccation

0.71 (695 ORFs) seem to be acquired in a laterradiodurans. PDS and ES values of these ORFs

stage, including SSB (DR0099 [0.99, 0.70]), PriA

are listed in Table 1.

Specific genes to each

(DR2606 [0.99, 0.70]), RuvA (DR1274 [0.96,

phenotype,by0.70]), RadA (DR1105 [1, 0.70]), RecO (DR0819

response, included mainly genes related to[0.05, 0.70]), RecN (DR1477 [0.83, 0.70]), andmetabolism

RecX (DR1310 [0.83, 0.69]) [19]. Also, the firstradioresistance and many hypothetical proteins

family encloses conserved hypothetical andfor anhydrobiosis.

hypothetical proteins.

related to the general stress response of D.

after

ionizing

tolerance

obtainedandradiation, tophenotypeenergy

the

of

the
D.

transcriptional

acquisition

forFive molecular chaperones,

The second, third, and fourth evolutionary

radiodurans [42], appeared during its response tofamilies constitute together the discordant genedesiccation, and only a single hsp20 (DR1114)

pool of D. radiodurans with PDS = –1.

The

chaperoned this bacterium’s radiation response

second family contains very diverged homologous(see Discussion Section). By PDS and ES means,relative to the first family, like ATP-dependent

plotting

ligase (DRB0100 [–1, 0.71]) [20].

anhydrobiosis related ORFs (data not shown)

The third

togetherradioresistanceandfamily does not contain any known key player
Table 1. Functions with PDS and ES values of ORFs specific to the desiccation tolerance phenotype of D.
radiodurans R1.
PDSESFunction
Mutational
inactivation㻃㻃㻃
DR1172–1
0
Hypothetical protein
DRB0118
0.66
0.67
Desiccation-associated protein
Transcriptional
response㻃㻃㻃
DR0138–1
0.71
Hypothetical protein
DR0145–1
0.7
Hypothetical protein
DR02030.74
0.7
Putative ABC-2 type transport system permease protein
DR0253–1

0

Hypothetical protein-248-

Viva Origino 33 (2005) 243-257
DR0270

*

0.92
–1
–1

0.72
0.69
0

Ribonuclease
Hypothetical protein
Hypothetical protein

–1
0.96
0.96
0.81

0
0.71
0.71
0.7

Hypothetical protein
Trans-aconitate 2-methyltransferase
ABC transporter
Conserved hypothetical

0.94
0.99
1
0.99

0.71
0.71
0.71
0.71

Threonine dehydratase
Chaperonin
GroEL protein
AAA+ ATPase

–1
–1
0
–1

0
0
0.71
0

Hypothetical protein
Hypothetical protein
50S ribosomal protein L31
Hypothetical protein

0.41
0.46
1
–1

0.7
0.7
0.71
0

Heat shock protein
Multidrug resistance protein
ATP-dependent Clp protease
Hypothetical protein

1
0.65
0.68
0.56

0.71
0.71
0.71
0.71

50S ribosomal protein L7/L12
Amino acid transport system ATP-binding protein
Putative transmembrane protein
Putative Band 7 family protein

0.68
0.37
0.23
0.61

0.71
0.7
0.71
0.7

Putative cyclopropane-fatty-acyl-phospholipid synthase
Hypothetical protein
Alcohol dehydrogenase
Transcriptional regulator, MerR family

–1
0.41
0.4
–1

0.71
0.67
0.71
0

Hypothetical protein
DNA-directed RNA polymerase subunit omega
Putative 3-demethylubiquinone-9 3-methyltransferase
Hypothetical protein

DRA0345
DRA0346
DRC0020

0.7
–1
–1
0.32

0.71
0.71
0
0.7

Iron transport system permease protein
Hypothetical protein
Hypothetical protein
Putative modification methylase

DRC0021–1

0

Hypothetical protein

DR0337
DR0338DR0404*
DR0422*
DR0475
DR0492*
DR0567*DR0606*DR0607*DR0621
DR0661
DR0800*DR0825
DR0955
DR0985
DR1004*
DR1046
DR1994*
DR2043*
DR2118*DR2142*
DR2143
DR2187*

DR2218*
DR2279DR2306
DR2436
DR2494*
DR2562
DR2573*
DR2589This table includes two desiccation tolerance-related proteins from D. radiodurans that were previously analyzed bymutational inactivation [58]. Also, it contains 40 genes, without any water stress-associated ORF, that were induced
in response to dry but not to ionizing radiation [4]. Here, by making two simple assumptions – that (i) ORFs withhigh PDS and ES values (PDS > 0, ES > 0.71) were possessed by the first microbial populations, and that (ii) before
3.05-2.78 billion years ago prokaryotes did not need to be dry tolerant as there was no land – it was possible toconstrain the evolutionary distribution of desiccation tolerance-specific ORFs to the discordant gene pool of D.
radiodurans. Furthermore, the presence of general stress-associated chaperones (DR0606, DR0607, DR0621,
DR0985, DR1046) favors the perception of D. radiodurans dry tolerance as a general stress response.
*
These ORFs are early ancestral genes (PDS > 0, ES > 0.71) in high conflict with evolutionary (most likely
desiccation tolerance appeared with Terrabacteria formed by Actinobacteria, Deinococcus, and Cyanobacteria) andgenomic (indications that desiccation tolerance is a general stress response) information if they were assumed as
specific to anhydrobiosis.

-249-

Viva Origino 33 (2005) 243-257

reconfirmed the positive correlation between

ecosystem in sugar-phosphate polymers carrying

these two phenotypes [3], and contradicted thenitrogenous bases as UV-protectors [29]; besides,“desiccation adaptation hypothesis”.

evidence has been presented that a string of
nucleotides is able to repair itself from UVDiscussion

damage[30].

Theoretical

calculations

demonstrated that DNA repair abilities of D.
A number of scientific elements are pertinent

radiodurans might have been adequate to deal

to the idea that affiliates life with radiation.

with a high Archaean UV flux and would be

Irradiation is widely invoked as a mechanism by

sufficient to survive in the mixed layer underwhich simple carbon-bearing molecules may besurface waters [25, 31].

polymerizedor otherwise reacted

to form

Cosmic rays, extremely heavy during the earlyprogressively more complex molecules that could

stage of evolution, consist of an ionizing radiation

ultimately synthesize life [23].

Bioastrologicalthat is higher in energy (multimegaelectronvolt

andsuggeststhatlevels) compared to radioactive substances [24].

radiation was a driving force during the chemicalRadioactive potassium, uranium and thoriumand early biochemical evolutions [24, 25]. The

constituted the basis of the radioactive heating of

early Earth was dominated by water as an oceanic

the Earth's interior at least 3.5 Gyr [32, 33]. Withlithosphere [25], and as a strong greenhouse gas

a higher intensity than cosmic radiation that emit[26]. If so, this environmental view implies, but

few particles per second, radioactive minerals

does not prove, that in the early microbial(thousands of millions of particles per second)

population, life was irradiated, probably hot, buthave been concentrated at the Earth's surface, andnot desiccated.

accumulated accretionary coatings of carbon due

paleoenvironmental

data

In the first 300,000 years after the big bang,theenergyofphotons

inthe

Early nuclear reactors of some 3.1-4.1 Gyr were

range

at

formed in a period shorter than 100 years by atemperatures between 1011 and 104 degrees Kelvinprocess, which requires neither oxygen nor[24]. During the formation of the Earth, the Sunorganic matter for the accumulation of uranium,

was emitting an intensity of ultraviolet (UV)based on a cycle of successive steps ofradiation probably 10,000 times greater thanweathering-erosion-transportation,

today and still four times greater at 3.5 Gyr [27].

sedimentation [24].

Simulations confirmed that UV irradiation could

reactors originated 2 Gyr [35] after the major

have worked as a mutagen and a selective factor

Proterozoic rise in oxygen nearly at 2.3 Gyr,[28] leading to a relative enrichment of thetermed the Great Oxidation Event (GOE) [36]. It

megaelectronvolt-electronvolt

lies

to irradiation, since early Archean times [34].

-250-

and

Then, Oklo type nuclear

Viva Origino 33 (2005) 243-257

can be calculated that about 100 million

bacteria very close to hyperthermophiles and to

Oklo-type reactor sites could have been active inthe root [45]. Two recombinases, represented by

the past [24]. A typical natural nuclear reactor

RecA of D. radiodurans and RadB of Pyrococcus

with a core radius of 2 meters has a total dose rate

furiosus, branch very deeply in the same tree [46].

of 47.4 Gy/h [24]. At this end, it is important toCorrelated to the earliest biomarker evidence

notice that the genotoxic effects, notably DNA(~3.4 Gyr) [47], the Deinococcus-Thermus group

double-strand breaks, of radiations (UV, β-, x-, ordate back to 2.7-3.4 Gyr. Indeed, phylogenetic

γ-rays) may occur at energies above the onset ofanalysis and signature sequences support theionizing [37, 38], a process that might have been

appearance of this group before cyanobacteria

substantially(before 2.7 Gyr) [48], and before the rise in O2

higherconsidering

the

early

predominance of a hot and reducing terrestrial

concentrations (before 2.45 Gyr) [49].

milieu [26]. Similarly, heat stress can occur ineubacterial lineage of Deinococcus forms withseemingly cold environments [39]. Indeed, stress

Actinobacteria

depends

Terrabacteria group that colonized land 3.05-2.78

not

only

on

local

environmental

conditions, but also on the behavior, morphology,

and

The

CyanobacteriatheGyr [50, 51].

and physiology of a particular organism [40]. The

Luckily, genomic sequences retain traces ofreport of UNSCEAR (United Nations Scientificextremely ancient evolutionary events, including

Committee on the Effects of Atomic Radiation)

the very first steps of life on Earth [52]. Protein[41], adopted by a previous study [42] to suggest

sequences do contain information about theirthat

historical pasts [53, 54], and do form similartheionizing

radioresistanceofD.

radiodurans cannot be an adaptation, needs aevolutionary

families.

careful critical appraisal. Briefly, one “atypical”

genome-wide

evolutionary

nuclear reactor with high ionizing-radiation dose

proteins in D. radiodurans, whose natural history

rates situated beneath the ocean bed would be

is little known, can be inferred from bioinformatic

enough as an adaptation site of abundant radiation

analyses.

biochemistry in the early Earth environment.

categorizing a genome is based on the codon

If rates and patterns of prokaryotic evolution

usage [55].

The

Here wetraditional

showlinkages

that

among

approachforThis approach was used to detectreflect the developmental history of the Earth's

alien genes in D. radiodurans [56]. Currently, we

environments [43] where, literally no matter whatembraced a new approach to classify the genome

the physical conditions are, the boundaries of lifeof D. radiodurans. For each ORF, we adopted a

are not yet precisely defined for prokaryotes [44],PDS analysis value, based on each gene’s

radioresistant cells should existed at least 3.5 Gyr.

relationships to its orthologs and an ES analysis

Phylogenetically, rRNA trees place radioresistantvalue, based on genomic distance matrix [6]. If-251-

Viva Origino 33 (2005) 243-257

all genes within a genome have the same

sharing [59]: Gene products contributing to thephylogenetic history, usually by vertical generadioresistance of D. radiodurans were recruitedtransfer or very ancient lateral gene transfer

to serve an additional function that is dry

events, PDS and ES values for each gene vis-à-vis

tolerance. In the terminology of Gould and Vrba

the target genomes should rank similarly and have[60]: (i) the genome of D. radiodurans illustrates

the same “evolutionary status”. Contrarily, ORFs

adaptations for ionizing radiation serving as

in the discordant gene pool do not have thisexaptations for desiccation, which explains thecommon ranking, instead they are discordant withpositive correlation between the two phenotypes,

PDS = –1.

and probably during land colonization (ii) some of

Hypotheticalproteins

that

appearasathese preadaptations becoming modified, in thetranscriptional response for anhydrobiosis, but notdiscordant

gene

pool,

for ionizing radiation, and have a ES value higher

adaptations

for

the

than 0.71 (Table 1) are intriguing for thephenotype, which might explain the higher

following reason: The plausibility that thesenumber of unknown proteins in response to

ORFs

desiccation (51 proteins) versus 38 unknown

were

possessed

by

early

microbial

populations (high PDS and ES values) isbyselection

desiccation

into

tolerance

protein in response to ionizing radiation.

distinctly at odds with the absence of any
requisite for anhydrobiosis defense strategies

Conclusion

before land colonization 3.05-2.78 Gyr.
PDS and ES analysis yielded estimates of D.

Given

that

the

“desiccation

adaptation

radiodurans evolutionary families, favoring the

hypothesis” claims are founded on an unfounded

hypothesis that the radiation resistance phenotype

evidence for a terrestrial ionizing-radiation natural

is related to more ancient metabolic pathways

source, and given that a relevant literature on

includingpathwaybiophysical,

geological,(DR0702 [0.69, 0.74]; DR0970 [0.92, 0.71];

experimental

data

DR0971 [0.97, 0.71]; DR1019 [0.01, 0.71];

alternatives, it was prudent to ask: Which was

DR2195 [0.12, 0.71]; DR2206 [0.72, 0.71];

acquired first by D. radiodurans progenitors,

DR2594 [0.004, 0.72] [57]. This analysis shows

radiation resistance or desiccation tolerance?

that ORFs hypothesizable as desiccation-specific

Assuming that D. radiodurans genome should

are, with only one exception (DRB0118) [58], inharbor a clear-cut answer for this question, we

the discordant gene pool of D. radiodurans.

used two evolutionary parameters (PDS and ES

Functionally, the desiccation tolerance phenotype

values) to stratify its genome into a core genecan be explained by the phenomenon of genepool and a discordant gene pool.

theenergyacquisition

-252-

favor

evolutionary,
more

and

plausible

Then, weViva Origino 33 (2005) 243-257

adopted a simple argument: Early ancestral genes
cannot be specific to drought stress as the need for

81–98 (1977).
3.

Mattimore,

V.

and

Battista,J.

R.

the desiccation tolerance phenotype appeared with

Radioresistance of Deinococcus radiodurans:

Terrabacteria.

functions

Following the desiccation of D.

necessarytosurviveionizing

radiodurans cells, the evolutionary status ofradiation are also necessary to survive

transcriptionally activated genes, the absence of

prolonged desiccation, J. Bacteriol. 178,

water stress-related genes, the presence of633–637 (1996).

molecular chaperones have put forward an
explanationofD.

radiodurans

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