The transcriptome of Candida albicans mitochondria and the evolution of organellar transcription units in yeasts.
BACKGROUND
Yeasts show remarkable variation in the organization of their mitochondrial genomes, yet there is little experimental data on organellar gene expression outside few model species. Candida albicans is interesting as a human pathogen, and as a representative of a clade that is distant from the model yeasts Saccharomyces cerevisiae and Schizosaccharomyces pombe. Unlike them, it encodes seven Complex I subunits in its mtDNA. No experimental data regarding organellar expression were available prior to this study.


METHODS
We used high-throughput RNA sequencing and traditional RNA biology techniques to study the mitochondrial transcriptome of C. albicans strains BWP17 and SN148.


RESULTS
The 14 protein-coding genes, two ribosomal RNA genes, and 24 tRNA genes are expressed as eight primary polycistronic transcription units. We also found transcriptional activity in the noncoding regions, and antisense transcripts that could be a part of a regulatory mechanism. The promoter sequence is a variant of the nonanucleotide identified in other yeast mtDNAs, but some of the active promoters show significant departures from the consensus. The primary transcripts are processed by a tRNA punctuation mechanism into the monocistronic and bicistronic mature RNAs. The steady state levels of various mature transcripts exhibit large differences that are a result of posttranscriptional regulation. Transcriptome analysis allowed to precisely annotate the positions of introns in the RNL (2), COB (2) and COX1 (4) genes, as well as to refine the annotation of tRNAs and rRNAs. Comparative study of the mitochondrial genome organization in various Candida species indicates that they undergo shuffling in blocks usually containing 2-3 genes, and that their arrangement in primary transcripts is not conserved. tRNA genes with their associated promoters, as well as GC-rich sequence elements play an important role in these evolutionary events.


CONCLUSIONS
The main evolutionary force shaping the mitochondrial genomes of yeasts is the frequent recombination, constantly breaking apart and joining genes into novel primary transcription units. The mitochondrial transcription units are constantly rearranged in evolution shaping the features of gene expression, such as the presence of secondary promoter sites that are inactive, or act as "booster" promoters, simplified transcriptional regulation and reliance on posttranscriptional mechanisms.
Institute of Genetics and Biotechnology, Faculty of Biology, University of Warsaw, Pawinskiego 5a, 02-106, Warsaw, Poland. adamk@igib.uw.edu.pl.
Adam
A
Kolondra
Institute of Genetics and Biotechnology, Faculty of Biology, University of Warsaw, Pawinskiego 5a, 02-106, Warsaw, Poland. karolina.labedzka.dmoch@igib.uw.edu.pl.
Karolina
K
Labedzka-Dmoch
Institute of Genetics and Biotechnology, Faculty of Biology, University of Warsaw, Pawinskiego 5a, 02-106, Warsaw, Poland. joanna.wenda@student.uw.edu.pl.
Joanna M
JM
Wenda
Institute of Genetics and Biotechnology, Faculty of Biology, University of Warsaw, Pawinskiego 5a, 02-106, Warsaw, Poland. katarzyna.drzewicka@gmail.com.
Katarzyna
K
Drzewicka
Institute of Genetics and Biotechnology, Faculty of Biology, University of Warsaw, Pawinskiego 5a, 02-106, Warsaw, Poland. pgolik@igib.uw.edu.pl.|Institute of Biochemistry and Biophysics, Polish Academy of Sciences, Pawinskiego 5a, 02-106, Warsaw, Poland. pgolik@igib.uw.edu.pl.
Pawel
P
Golik
D000595:Amino Acid Sequence / Q000235:genetics; D001483:Base Sequence; D002176:Candida albicans / Q000235:genetics*; D004272:DNA, Mitochondrial / Q000235:genetics; D015870:Gene Expression; D015966:Gene Expression Regulation, Fungal; D054629:Genome, Mitochondrial / Q000235:genetics*; D059014:High-Throughput Nucleotide Sequencing; D006801:Humans; D007438:Introns / Q000235:genetics; D008928:Mitochondria / Q000235:genetics; D015388:Organelles / Q000235:genetics; D012335:RNA, Ribosomal / Q000235:genetics; D012343:RNA, Transfer / Q000235:genetics; D012441:Saccharomyces cerevisiae / Q000235:genetics; D012568:Schizosaccharomyces / Q000235:genetics; D014158:Transcription, Genetic; D059467:Transcriptome / Q000235:genetics*
D004272:DNA, Mitochondrial; D012335:RNA, Ribosomal; D012343:RNA, Transfer