Bacteria belonging to the family Deinococcaceae survive exposure to >1.5 megarads of ionizing irradiation or to extreme desiccation without lethality or mutagenesis [2, 31, 35] . This tolerancederives from the ability of these species to accurately mendnumerous double-strand DNA breaks [DSBs], thus reassemblingan intact genome from hundreds of fragments in a manner thatrestores chromosomal continuity . The only known mechanism thatenables accurate repair of DSBs in bacteria is RecA-dependenthomologous recombination, whereby information lost at a lesionis restored by a homologous DNA sequence that acts as a template[22-24] . As such, DNA repair via homologous recombination strictlydepends upon the ability of cellular systems to perform a rapidand efficient genomewide search for homologous DNA sites [27].However, following extensive DNA fragmentation, no intact templateremains . Homologous search conducted under such circumstanceswould necessarily entail repetitive reinspection of multiplerandomly dispersed DNA fragments, rendering the process inherentlyfutile [9a, 36] . Indeed, the first phase of DNA repair in Deinococcus radiodurans was shown to be RecA independent [9], implying thatthis phase does not rely on homologous recombination.

The high resistance of bacterial spores to irradiation and desiccation indicates that DSBs inflicted by these assaults on dormant spores are efficiently and accurately mended upon germination . However, DNA repair involving homologous search processes cannot occur in germinating spores, because bacterial spores regularly carryonly one copy of their genomes [5] . Consequently, germinating spores lack the template required for accurate homologous-recombination-mediatedrepair of DSBs.

 
Biochemical and genetic studies, including the complete sequencingof the D . radiodurans genome, indicated that this organism possesses a typical bacterial complement of DNA repair enzymes [50] andthat these proteins are, by and large, similar to those found in other bacteria [3, 4] . A recent analysis of the effects exertedby acute irradiation upon D . radiodurans gene expression didnot elucidate a genetic basis of DNA repair [29] . These observations,which imply that the complement of DNA repair proteins in D.radiodurans is not sufficient to confer resistance, led to thesuggestion that repair of DSBs in this organism is promotedby a continuous alignment of genome copies [36; Daly and Minton,Science 270:1318, 1995] . Such an alignment, presumably maintainedby multiple four-stranded Holliday junctions, would providea means for error-free DNA repair by supplying an ever-presentnearby template, hence eliminating the need for a logisticallyimpractical homologous search . Multiple Holliday junctions betweenDNA molecules would, however, represent a major obstacle toDNA transactions, and indeed, they were shown by optical mappinganalysis to be absent in the D . radiodurans genome [28].

An alternative to genome alignment by Holliday junctions was implied by structural studies of D . radiodurans, which demonstrated that chromatin in the organism adopts a toroidal shape . It was suggested that within this tightly packed shape, ends of DNA fragments generated by DSBs are continuously held in close physical proximity, thus enabling their accurate repair in a template-independent pathway [26, 33] . Such repair processes may proceed throughnonhomologous end joining [NHEJ], as well as via homologousannealing of protruding single strands that are present at theends of DNA fragments [9].

In this commentary, we survey recently reported findings, which indicate that toroidal DNA conformations represent a commonfeature in highly resistant life forms, such as members of thefamily Deinococcaceae, as well as dormant and germinating bacterial spores . We discuss other observations that imply that the complement of DNA repair enzymes in these life forms evolved specificallyto enable accurate repair of DSBs through end joining withina tightly packed DNA organization . Taken together, these findingssupport the notion that a toroidal DNA conformation is usedin bacteria to facilitate the mending of DSBs when RecA-dependenthomologous repair cannot be effectively employed.

 
Cryoelectron microscopy of DNA toroids obtained in vitro indicated that within these structures, DNA molecules attain a high degreeof order and compactness [17] . The inherent lateral order and high packaging density make DNA toroids rigid matrices in which diffusion of DNA fragments generated by irradiation or desiccationis substantially restricted [33] . Indeed, in vitro studies demonstratedthat within toroidal DNA structures, annealing of cohesive DNAends, as well as enzymatic ligation of cohesive and blunt DNAends, is enhanced by 5 to 6 orders of magnitude relative to its rate and efficiency in dispersed DNA structures [18, 51].As such, DNA toroids, in which free DNA ends are kept closetogether and their local concentration is substantially enhanced,provide uniquely suitable scaffolds for DNA repair through high-fidelityDNA end-joining processes.

DNA toroids in vivo. DNA molecules in D . radiodurans cells adopt a distinct toroidalshape that sets the species apart from most other bacteria,in which a dispersed and amorphous morphology of the genomeis regularly discerned [26] . Studies conducted in our laboratorydemonstrated that the genomes of two additional members of thefamily Deinococcaceae, Deinococcus radiopugnans and Deinococcusradiophilus, are also assembled as toroids [Fig . 1] . A similar toroidal DNA shape was detected in dormant spores of Bacillus subtilis [13] . Notably, the toroidal structure was shown topersist in germinating spores of both B . subtilis and Bacillusmegaterium [43].

 
The observation that members of the family Deinococcaceae, as well as bacterial spores, adopt a toroidal DNA conformationis significant, because both life forms cannot promote conventional high-fidelity DNA repair pathways . Following extensive DNA fragmentation in deinococcal species, homologous search processes, and hence repair of DSBs through homologous recombination, become ineffective[36] . Analogously, DNA repair through homologous search cannotoccur in germinating spores, because bacterial spores regularlycarry only one copy of their genomes [5] . Thus, species belonging to the family Deinococcaceae and bacterial spores share three conspicuous features . Both life forms survive irradiation and desiccation in doses that are lethal to other species [2, 39,47], both forms are incapable of repairing DSBs through homologousrecombination, and most significantly, both species belongingto the family Deinococcaceae and spores maintain their DNA complementsin a toroidal conformation, within which accurate DNA repairby NHEJ processes may occur.

DNA toroids and cellular morphology. D . radiodurans cells reveal a tetrad morphology [26] and carry4 to 10 genome copies [16], which are segregated within the four compartments [26] . Further studies have indicated thatD . radiopugnans and D . radiophilus are diplococcal, composedof two compartments within which genome copies are segregated[Fig . 2] . The multicoccal morphology is significant becauseof the notion that when bacteria contain several segregatedgenome copies, these copies reveal different levels of transcriptionalactivity and hence different extents of packaging [41] . In speciesof the family Deinococcaceae, in which individual chromosomesare segregated into two or four compartments, such differentialpackaging would explain how a single vegetative cell could haveboth metabolically active chromosomes that allow growth andcondensed toroidal nucleoids that promote resistance . This notionis supported by the finding that D . radiodurans cells carryseveral genome copies [16], whereas dormant spores, which donot need an active decondensed genome, maintain only one copy[5] . The notion is further buttressed by the existence of orificesin the membranes that separate the compartments in species ofthe family Deinococcaceae, indicating that the compartmentsare not fully separated [26] . Indeed, the nucleoid in one ortwo compartments of vegetative D . radiodurans cells exhibitsa dispersed morphology, whereas the chromatin in the other compartmentsadopts a toroidal structure [26] . Notably, the metabolicallydormant spores do not contain active chromosomes and hence donot require multicoccal morphology.

 
In vitro studies have indicated that a toroidal DNA shape represents a particularly stable mode of DNA condensation [6, 40] . Severalfactors combine to further enhance the intrinsic stability ofthis particular shape in Deinococcaceae and in bacterial spores.

Temperature. The toroidal DNA shape in species of the family Deinococcaceaebecomes substantially more pronounced at low temperature yetis hardly discernible as the temperature is raised to 42°C[J . Englander and A . Minsky, unpublished results] . Consistent with this finding is the observation that the radioresistance of deinococcal species is decreased by 2 orders of magnitudeat elevated temperatures [21].

Mn²⁺ ions. In vitro studies have demonstrated that the divalent ion Mn²⁺ is uniquely efficient in promoting ordered, toroidal DNA condensation[7, 30, 44] . This observation is significant, because the genomeof D . radiodurans maintains an exceptionally large concentrationof Mn²⁺ ions [25] . The ability of Mn²⁺ ions to specificallystabilize condensed DNA morphologies under dehydrating conditions[44] is particularly notable, as D . radiodurans DNA damage tolerance has been proposed to reflect an evolutionary adaptation to dehydration [32].

However, it has been demonstrated that when the concentrationof DNA-condensing factors is increased beyond a given threshold,DNA decondensation and resolubilization are effected, possiblydue to DNA charge reversal [10, 38, 42] . Notably, relativelyhigh [>2.5 µM] concentrations of Mn²⁺ ions sensitizeD . radiodurans cells to irradiation without affecting theirviability or growth under unstressed conditions [8] . Indeed,when exposed to large concentrations of Mn²⁺, the D . radioduransgenome reveals an amorphous, nontoroidal morphology [26] . Itthus appears that factors that modulate the formation and stabilityof DNA toroids, such as temperature and divalent ions, correspondinglyaffect damage tolerance.

DNA-binding proteins. Small DNA-binding, acid-soluble proteins [SASPs], which areubiquitous in bacterial spores, specifically stabilize toroidalDNA packaging in vitro [15], as well as within spores [13, 43]. In vitro studies have indicated that the DNA-SASP toroidal complex is ordered and highly condensed [13] . Indeed, spores that lackSASPs do not form a ringlike DNA structure and are substantiallymore sensitive to UV light and desiccation than wild-type spores[47] . Similarly, the absence of toroidal DNA structures in D.radiodurans renders the organism susceptible to irradiation,as mentioned above.

The D . radiodurans DNA-binding protein HU has recently been shown to reveal a particularly high affinity for prebent DNA sequences, thus specifically stabilizing these structural motifs[14] . Apparently, in addition to the factors mentioned aboveand in analogy to the sporal SASP, the ubiquitous HU proteinacts to promote toroidal DNA packaging in the species of thefamily Deinococcaceae by stabilizing a highly curved DNA trajectory.

Growth phase. Starved stationary-state D . radiodurans cells are threefoldmore resistant to ionizing irradiation than actively growingcells [35] . This observation is consistent with the findingthat the toroidal DNA organization is substantially more pronouncedin stationary-state D . radiodurans cells than in actively growingbacteria [26] . This finding is, however, inconsistent with thepremise that DNA repair in D . radiodurans is promoted solelyby induced enzymatic pathways, because these pathways becomeincreasingly inefficient during prolonged starvation [34].

 
Whereas the sequencing and analysis of the D . radiodurans genome indicated that the complement of DNA repair enzymes in this resistant species is similar to that found in nonresistant bacteria[50], several intriguing differences were discerned.

RecA and RecBCD. RecA and RecA-like proteins play critical roles in homologousrecombination [22, 45] . Studies conducted with a recA-defective mutant indicated that the initial DSB repair phase in D . radiodurans is, however, RecA independent [9] . This phase, which is initiatedimmediately following acute irradiation and which proceeds forseveral hours, is highly efficient, resulting in error-free mending of more than one-third of the multiple DSBs . This finding has been taken to imply the presence of RecA-independent annealing between complementary single-stranded DNA segments created at the ends of the fragments [9] . We claim that while such annealingmay indeed assist DNA repair, its contribution would be limitedrelative to NHEJ processes because single strands generated at DSB sites are unlikely to become long enough to allow significant annealing in the absence of RecBCD exonuclease in D . radiodurans [31] [see below] . We note that, regardless of the relative contributionsof NHEJ and single-strand annealing to DNA repair, both processeswould be substantially facilitated and accelerated within thescaffold of tightly packed DNA toroids, in which the continuityof DNA fragments is physically preserved [33].

The RecA protein in D . radiodurans, which exhibits 53% sequence identity with Escherichia coli RecA, is constitutively expressed at low levels but is transiently induced to higher levels following extensive DNA damage [19, 20] . Significantly, in contrast tothe RecA proteins in other bacterial strains, D . radioduransRecA binds preferentially to double-stranded rather than tosingle-stranded DNA and hydrolyzes ATP more rapidly upon bindingto double-stranded DNA than to single-stranded molecules [19,20] . These unique traits, as well as recent observations whichimply that the recombination activity of RecA in D . radioduransdoes not represent a critical factor in DNA repair processes[37, 46], highlight the notion that the actual modes through which RecA exerts its functions in D . radiodurans remain poorly understood.

The heterotrimeric helicase-nuclease RecBCD plays an essential role in homologous repair of DSBs in bacteria by producing single-stranded DNA tails [24] and stimulating the loading of RecA onto thesetails [1] . As such, the RecBCD complex can formally be consideredan enzyme that extends DNA damage at a DSB site through itsnuclease activity . The unexpected absence of RecBCD in D . radiodurans[31, 50], along with the unique preferential binding of D . radiodurans RecA to double-stranded DNA [19], supports the notion that repairof DSBs in this organism relies on repair enzymes that evolved to exert their activities on double-stranded DNA species, presumably by promoting NHEJ within a rigid toroidal matrix.

DNA ligases and NHEJ. In eukaryotic cells, DSBs are repaired by homologous recombinationor by NHEJ [12] . NHEJ is specifically promoted by ATP-dependentDNA ligases that are ubiquitous in eukaryotes but are consideredto be absent in bacterial cells, which regularly encode NAD-dependentligases involved in DNA replication [12] . Until recently, itwas assumed that a NHEJ system is not present in prokaryotes,and bacterial high-fidelity repair of DSBs was thought to relysolely on homologous recombination.

Recent studies have revealed, however, that a unique familyof ATP-dependent DNA ligases is present in several bacterialspecies, including Mycobacterium tuberculosis, B . subtilis,and Bacillus halodurans, in addition to typical NAD-dependent ligases [11, 48, 49] . These bacterial species were also foundto contain Ku-like proteins, which are homologous to the eukaryoticKu protein that acts to recruit ATP-dependent DNA ligases ontoDSB sites . The presence of ATP-dependent ligases and Ku homologuesin bacteria that spend long periods of their life cycles instationary phase or that are regularly exposed to harsh environmentswas proposed to imply that an NHEJ system might represent animportant mode of repair of DSBs in these species [49].

In addition to an NAD-dependent ligase, an ATP-dependent DNA ligase was identified in D . radiodurans [50] . The ATP-dependentligase is induced by irradiation, whereas the typical NAD-dependentligase is down-regulated [29], implying that the ATP-dependentligase might be involved in postirradiation repair in D . radiodurans.Significantly, the small mass [22 kDa] of D . radiodurans ATP-dependentligase, which sets it apart from the typically much larger DNAligases, is likely to facilitate access of the enzyme to DSBswithin the tightly packed toroids.

In contrast to spore-forming bacteria, a Ku homologue was not identified in D . radiodurans . However, because Ku-dependent stimulation of ligation is partially attributed to the abilityof the protein to juxtapose two DNA ends [11], its activity in Deinococcaceae might not be required, as DNA ends are kept together within the toroidal DNA matrix.

 
The observations summarized here imply that a tight toroidalDNA organization is uniquely adjusted to promote the repairof multiple DSBs by both NHEJ and RecA-independent annealingin a manner that drastically minimizes errors . They furtherindicate that this structurally dependent strategy is specificallyadopted by prokaryotes that are inactive during significantperiods of their life cycles, e.g., dormant spores, or thatare regularly exposed to harsh environments, such as Deinococcaceae.These highly resistant life forms, in which repair of DSBs byhomologous recombination is impossible or ineffective, evolvedmechanisms [proteins such as SASPs and HU or high concentrationsof Mn²⁺ ions] that promote the formation and stability of DNAtoroids . These organisms also evolved a complement of DNA repairenzymes that enables NHEJ within toroids . In some cases [e.g.,Deinococcaceae], they adopted polycoccal morphologies that allowcellular growth while preserving tight DNA packaging . Finally,the considerations presented here corroborate the notion thatparticular genome structures represent crucial factors in themaintenance of DNA integrity in living systems exposed to harshenvironmental conditions [13, 27, 33, 34].

 
* Corresponding author . Mailing address: Department of Organic Chemistry, The Weizmann Institute of Science, Rehovot 76100, Israel . Phone: 972 8 9342003 . Fax: 972 8 9344142 . E-mail: avi.minsky@weizmann.ac.il.

The views expressed in this Commentary do not necessarily reflectthe views of the journal or of ASM.

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