As a part of our initiative aimed at a large-scale comparative analysis of fungal mitochondrial genomes, we determined the complete DNA sequence of the mitochondrial genome of the yeast Candida subhashii and found that it exhibits a number of peculiar features. First, the mitochondrial genome is represented by linear dsDNA molecules of uniform length (29 795 bp), with an unusually high content of guanine and cytosine residues (52.7 %). Second, the coding sequences lack introns; thus, the genome has a relatively compact organization. Third, the termini of the linear molecules consist of long inverted repeats and seem to contain a protein covalently bound to terminal nucleotides at the 5′ ends. This architecture resembles the telomeres in a number of linear viral and plasmid DNA genomes classified as invertrons, in which the terminal proteins serve as specific primers for the initiation of DNA synthesis. Finally, although the mitochondrial genome of C. subhashii contains essentially the same set of genes as other closely related pathogenic Candida species, we identified additional ORFs encoding two homologues of the family B protein-priming DNA polymerases and an unknown protein. The terminal structures and the genes for DNA polymerases are reminiscent of linear mitochondrial plasmids, indicating that this genome architecture might have emerged from fortuitous recombination between an ancestral, presumably circular, mitochondrial genome and an invertron-like element.
AdamH.,
GroenewaldM.,
MohanS.,
RichardsonS.,
BunnU.,
GibasC. F.,
PoutanenS.,
SiglerL.2009; Identification of a new species, Candida subhashii, as a cause of peritonitis. Med Mycol 47:305–311
AndersonJ. B.,
WickensC.,
KhanM.,
CowenL. E.,
FederspielN.,
JonesT.,
KohnL. M.2001; Infrequent genetic exchange and recombination in the mitochondrial genome of Candida albicans. J Bacteriol 183:865–872
BlaisonneauJ.,
NosekJ.,
FukuharaH.1999; Linear DNA plasmid pPK2 of Pichia kluyveri: distinction between cytoplasmic and mitochondrial linear plasmids in yeasts. Yeast 15:781–791
BurgerG.,
LangB. F.,
GrayM. W.2000; Phylogenetic relationships of stramenopile algae, based on complete mitochondrial genome sequences. Genbank Acc.no. AF287134
ChanB. S.,
CourtD. A.,
VierulaP. J.,
BertrandH.1991; The kalilo linear senescence-inducing plasmid of Neurospora is an invertron and encodes DNA and RNA polymerases. Curr Genet 20:225–237
ColemanA. W.,
ThompsonW.,
GoffL. J.1991; Identification of the mitochondrial genome in the chrysophyte alga Ochromonas danica. J Eukaryot Microbiol 38:129–135
DinouelN.,
DrissiR.,
MiyakawaI.,
SorF.,
RoussetS.,
FukuharaH.1993; Linear mitochondrial DNAs of yeasts: closed-loop structure of the termini and possible linear-circular conversion mechanisms. Mol Cell Biol 13:2315–2323
FitzpatrickD. A.,
LogueM. E.,
StajichJ. E.,
ButlerG.2006; A fungal phylogeny based on 42 complete genomes derived from supertree and combined gene analysis. BMC Evol Biol 6:99
ForgetL.,
UstinovaJ.,
WangZ.,
HussV. A.,
LangB. F.2002; Hyaloraphidium curvatum: a linear mitochondrial genome, tRNA editing, and an evolutionary link to lower fungi. Mol Biol Evol 19:310–319
FukuharaH.,
SorF.,
DrissiR.,
DinouelN.,
MiyakawaI.,
RoussetS.,
ViolaA. M.1993; Linear mitochondrial DNAs of yeasts: frequency of occurrence and general features. Mol Cell Biol 13:2309–2314
HermannsJ.,
OsiewaczH. D.1992; The linear mitochondrial plasmid pAL2-1 of a long-lived Podospora anserina mutant is an invertron encoding a DNA and RNA polymerase. Curr Genet 22:491–500
KayalE.,
LavrovD. V.2008; The mitochondrial genome of Hydra oligactis (Cnidaria, Hydrozoa) sheds new light on animal mtDNA evolution and cnidarian phylogeny. Gene 410:177–186
KimE. K.,
JeongJ. H.,
YounH. S.,
KooY. B.,
RoeJ. H.2000; The terminal protein of a linear mitochondrial plasmid is encoded in the N-terminus of the DNA polymerase gene in white-rot fungus Pleurotus ostreatus. Curr Genet 38:283–290
KlassenR.,
MeinhardtF.2007; Linear protein-primed replicating plasmids in eukaryotic microbes. In Microbial Linear Plasmids pp 187–226 Edited by
MeinhardtF.,
KlassenR.
Berlin: Springer-Verlag;
LongasE.,
de VegaM.,
LazaroJ. M.,
SalasM.2006; Functional characterization of highly processive protein-primed DNA polymerases from phages Nf and GA-1, endowed with a potent strand displacement capacity. Nucleic Acids Res 34:6051–6063
NosekJ.,
TomaskaL.2002; Mitochondrial telomeres: alternative solutions to the end-replication problem. In Telomeres, Telomerases and Cancer pp 396–417 Edited by
KruppG.,
ParwareschR.
New York: Kluwer Academic/Plenum Publishers;
NosekJ.,
TomaskaL.2008; Mitochondrial telomeres: an evolutionary paradigm for the emergence of telomeric structures and their replication strategies. In Origin and Evolution of Telomeres pp 163–171 Edited by
NosekJ.,
TomaskaL.
New York: Landes Bioscience;
NosekJ.,
NovotnaM.,
HlavatovicovaZ.,
UsseryD. W.,
FajkusJ.,
TomaskaL.2004; Complete DNA sequence of the linear mitochondrial genome of the pathogenic yeast Candida parapsilosis. Mol Genet Genomics 272:173–180
NosekJ.,
RycovskaA.,
MakhovA. M.,
GriffithJ. D.,
TomaskaL.2005; Amplification of telomeric arrays via rolling-circle mechanism. J Biol Chem 280:10840–10845
OlovnikovA. M.1973; A theory of marginotomy. The incomplete copying of template margin in enzymic synthesis of polynucleotides and biological significance of the phenomenon. J Theor Biol 41:181–190
RodriguezI.,
LazaroJ. M.,
SalasM.,
De VegaM.2004; phi29 DNA polymerase–terminal protein interaction. Involvement of residues specifically conserved among protein-primed DNA polymerases. J Mol Biol 337:829–841
SakaguchiK.1990; Invertrons, a class of structurally and functionally related genetic elements that includes linear DNA plasmids, transposable elements, and genomes of adeno-type viruses. Microbiol Rev 54:66–74
SambrookJ.,
RussellD.2001Molecular Cloning: a Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
SchardlC. L.,
LonsdaleD. M.,
PringD. R.,
RoseK. R.1984; Linearization of maize mitochondrial chromosomes by recombination with linear episomes. Nature 310:292–296
ShaoZ.,
GrafS.,
ChagaO. Y.,
LavrovD. V.2006; Mitochondrial genome of the moon jelly Aurelia aurita (Cnidaria, Scyphozoa): a linear DNA molecule encoding a putative DNA-dependent DNA polymerase. Gene 381:92–101
SmithD. R.,
LeeR. W.2008; Mitochondrial genome of the colorless green alga Polytomella capuana: a linear molecule with an unprecedented GC content. Mol Biol Evol 25:487–496
TakanoH.,
KawanoS.,
KuroiwaT.1994; Genetic organization of a linear mitochondrial plasmid (mF) that promotes mitochondrial fusion in Physarum polycephalum. Curr Genet 26:506–511
TakanoH.,
MoriK.,
KawanoS.,
KuroiwaT.1996; Rearrangements of mitochondrial DNA and the mitochondrial fusion-promoting plasmid (mF) are associated with defective mitochondrial fusion in Physarum polycephalum. Curr Genet 29:257–264
TakedaM.,
HiraishiH.,
TakesakoT.,
TanaseS.,
GungeN.1996; The terminal protein of the linear DNA plasmid pGKL2 shares an N-terminal domain of the plasmid-encoded DNA polymerase. Yeast 12:241–246
TomaskaL.,
NosekJ.,
MakhovA. M.,
PastorakovaA.,
GriffithJ. D.2000; Extragenomic double-stranded DNA circles in yeast with linear mitochondrial genomes: potential involvement in telomere maintenance. Nucleic Acids Res 28:4479–4487
TrunigerV.,
BonninA.,
LazaroJ. M.,
de VegaM.,
SalasM.2005; Involvement of the “linker” region between the exonuclease and polymerization domains of phi29 DNA polymerase in DNA and TP binding. Gene 348:89–99
VierulaP. J.,
ChengC. K.,
CourtD. A.,
HumphreyR. W.,
ThomasD. Y.,
BertrandH.1990; The kalilo senescence plasmid of Neurospora intermedia has covalently-linked 5′ terminal proteins. Curr Genet 17:195–201
VoigtO.,
ErpenbeckD.,
WorheideG.2008; A fragmented metazoan organellar genome: the two mitochondrial chromosomes of Hydra magnipapillata. BMC Genomics 9:350