The transcriptome of Candida albicans mitochondria and the evolution of organellar transcription units in yeasts

Kolondra, Adam; Labedzka-Dmoch, Karolina; Wenda, Joanna M.; Drzewicka, Katarzyna; Golik, Pawel

doi:10.1186/s12864-015-2078-z

Cited by 33Fungal and yeast genetics researchMitochondrial Function and PathologyRNA Research and Splicing

The transcriptome of Candida albicans mitochondria and the evolution of organellar transcription units in yeasts

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Kolondra, Adam, Labedzka-Dmoch, Karolina, Wenda, Joanna M., Drzewicka, Katarzyna, Golik, Pawel·2015·BMC Genomics

DOI 10.1186/s12864-015-2078-zPMC PMC4618339

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Abstract

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.

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The activation of AOX by the Rtg pathway suggests that its function in the retrograde response to mitochondrial dysfunction could be conserved in C. albicans despite the considerable evolutionary distance from S. cerevisiae and many changes in the components of the pathway, the mitochondrial genome and respiratory metabolism.
“The activation of AOX by the Rtg pathway suggests that its function in the retrograde response to mitochondrial dysfunction could be conserved in C. albicans despite the considerable evolutionary distance from S. cerevisiae and many changes in the components of the pathway”
From Mitochondrial retrograde control of transcription evolves with respiratory stress, metabolic adaptation, and virulence in budding yeasts (2026) · cites this paper as Kolondra et al. 2015
The Background (page not provided) describes differences between C. albicans and S. cerevisiae in respiratory metabolism and mitochondrial genome content. It does not address AOX activation by the Rtg pathway or whether the pathway’s retrograde-response function is conserved; those central parts of the claim are unsupported by this paper. (LLM, conf=0.78)
Experimental — accuracy not yet measured
In Cappr13Δ, NAD4L and NAD5 probe signals are lost; other mRNAs and rRNAs were not affected; native level restored by reintroducing WT CaPPR13.
“In the Cappr13Δ mutant, we observed the loss of signal detected by the NAD4L and NAD5 probes (Fig. 4a) that hybridize to a single bicistronic transcript (Kolondra et al. 2015). Other mRNAs and rRNAs were not affected by the deletion of CaPPR13 (Supplementary Fig. 6). We could restore the native level of the NAD4L–NAD5 bicistron by reintroducing the WT CaPPR13 allele.”
From Candida albicans PPR proteins are required for the expression of respiratory Complex I subunits (2024) · cites this paper as Kolondra et al. 2015
In C. albicans, ATP9, ATP6, and ATP8 originate from a single polycistronic transcription unit (TU4) controlled by the same promoter and later separated into ATP9 and the bicistronic ATP6-ATP8 mRNA, whereas in S. cerevisiae they are transcribed separately.
“In C. albicans, ATP9, ATP6, and ATP8 originate from a single polycistronic transcription unit (TU4) controlled by the same promoter and later separated into ATP9 and the bicistronic ATP6–ATP8 mRNA, whereas in S. cerevisiae, ATP9 and the ATP6–ATP8 bicistron are transcribed separately (Kolondra et al. 2015; Golik 2024).”
From Candida albicans PPR proteins are required for the expression of respiratory Complex I subunits (2024) · cites this paper as Kolondra et al. 2015
The effect of CaPpr7p on splicing cannot be explained by a maturase deficiency due to impaired translation, because the ORF encoded in COB intron I contains the GIY-YIG motif typical of homing endonucleases rather than maturases.
“Organellar translation and splicing are mechanistically connected by the intron-encoded maturase proteins (Pel and Grivell 1993), but the ORF encoded in COB intron I contains the GIY–YIG motif (Kolondra et al. 2015) that is typical of homing endonucleases rather than maturases (Dunin-Horkawicz et al. 2006), suggesting that the effect of CaPpr7p on splicing cannot be explained by a maturase”
From Candida albicans PPR proteins are required for the expression of respiratory Complex I subunits (2024) · cites this paper as Kolondra et al. 2015
The stop codon of NAD4L is contiguous with the start codon of downstream NAD5, and the two mRNAs are co-translated.
“The stop codon of NAD4L is contiguous with the start codon of downstream NAD5. It is rather clear that the 2 mRNA are co-translated (Kolondra et al. 2015), as we do not detect individual NAD4L and NAD5 transcripts.”
From Candida albicans PPR proteins are required for the expression of respiratory Complex I subunits (2024) · cites this paper as Kolondra et al. 2015

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Clade II Candida auris possess genomic structural variations related to an ancestral strain
Sekizuka, T., Iguchi, S., Umeyama, T., Inamine, Y., Makimura, K., Kuroda, M., Miyazaki, Y., & Kikuchi, K. (2019) · PLoS ONE · doi:10.1371/journal.pone.0223433 · Cited by 60 · see citing works
The (in)complete organelle genome: exploring the use and nonuse of available technologies for characterizing mitochondrial and plastid chromosomes
Lima, M. S., Woods, L. C., Cartwright, M. W., & Smith, D. R. (2016) · Molecular Ecology Resources · doi:10.1111/1755-0998.12585 · Cited by 38 · see citing works
The S. pombe mitochondrial transcriptome
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Mitochondrial genome of Cordyceps blackwelliae: organization, transcription, and evolutionary insights into Cordyceps
Zhang, Y., Fan, X.-P., Li, J., & Zhang, S. (2023) · IMA Fungus · doi:10.1186/s43008-023-00118-5 · Cited by 18 · see citing works
Respiration supports intraphagosomal filamentation and escape of Candida albicans from macrophages
Case, N. T., Westman, J., Hallett, M. T., Plumb, J. D., Farheen, A., Maxson, M. E., MacAlpine, J., Liston, S. D., Hube, B., Robbins, N., et al. (2023) · mBio · doi:10.1128/mbio.02745-23 · Cited by 17 · see citing works
Traditional and novel tools to probe the mitochondrial metabolism in health and disease
Zhang, Y., & Avalos‬, J. L. (2017) · WIREs Systems Biology and Medicine · doi:10.1002/wsbm.1373 · Cited by 16 · see citing works
Editorial: Mitochondrial Genomes and Mitochondrion Related Gene Insights to Fungal Evolution
Kouvelis, V. N., & Hausner, G. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.897981 · Cited by 17 · see citing works
The mitochondrial genome of the grape powdery mildew pathogen Erysiphe necator is intron rich and exhibits a distinct gene organization
Zaccaron, A. Z., de Souza, J. T., & Stergiopoulos, I. (2021) · Scientific Reports · doi:10.1038/s41598-021-93481-5 · Cited by 13 · see citing works
Differential actinodin1 regulation in embryonic development and adult fin regeneration in Danio rerio
Phan, H.-E., Northorp, M., Lalonde, R. L., Ngo, D. M., & Akimenko, M. (2019) · PLoS ONE · doi:10.1371/journal.pone.0216370 · Cited by 12 · see citing works
The Evolution of Mitochondrial Genomes in Fungi
Kouvelis, V. N., Kortsinoglou, A. M., & James, T. Y. (2023) · The mycota · doi:10.1007/978-3-031-29199-9_3 · Cited by 11 · see citing works
Evidence for Mitochondrial Genome Methylation in the Yeast Candida albicans: A Potential Novel Epigenetic Mechanism Affecting Adaptation and Pathogenicity?
Bartelli, T. F., Bruno, D. D. C. F., & Briones, M. R. S. (2018) · Frontiers in Genetics · doi:10.3389/fgene.2018.00166 · Cited by 11 · see citing works
<scp>RNA</scp> processing and degradation mechanisms shaping the mitochondrial transcriptome of budding yeasts
Golik, P. (2024) · IUBMB Life · doi:10.1002/iub.2779 · Cited by 9 · see citing works
The Pet127 protein is a mitochondrial 5′-to-3′ exoribonuclease from the PD-(D/E)XK superfamily involved in RNA maturation and intron degradation in yeasts
Łabędzka-Dmoch, K., Rażew, M., Gapińska, M., Piątkowski, J., Kolondra, A., Salmonowicz, H., Wenda, J. M., Nowotny, M., & Golik, P. (2022) · RNA · doi:10.1261/rna.079083.121 · Cited by 9 · see citing works
Pervasive transcription of the mitochondrial genome in Candida albicans is revealed in mutants lacking the mtEXO RNase complex
Łabędzka-Dmoch, K., Kolondra, A., Karpińska, M. A., Dębek, S., Grochowska, J., Grochowski, M., Piątkowski, J., Hoang Diu Bui, T., & Golik, P. (2021) · RNA Biology · doi:10.1080/15476286.2021.1943929 · Cited by 8 · see citing works
Mitochondrial RNA maturation
Chrzanowska‐Lightowlers, Z. M., & Lightowlers, R. N. (2024) · RNA Biology · doi:10.1080/15476286.2024.2414157 · Cited by 8 · see citing works
Horizontal transfer of tRNA genes to mitochondrial plasmids facilitates gene loss from fungal mitochondrial DNA
Nieuwenhuis, M., Groeneveld, J., & Aanen, D. K. (2022) · Current Genetics · doi:10.1007/s00294-022-01259-7 · Cited by 8 · see citing works
Uncovering the role of mitochondrial genome in pathogenicity and drug resistance in pathogenic fungi
Ni, Y., & Gao, X. (2025) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2025.1576485 · Cited by 7 · see citing works
Global view of dynamic expression and precise mapping of mitochondrial tRNAs-derived fragments during stressed conditions in S. pombe
Hu, Y., Wu, L., Zhang, P., Wang, Z., Shang, J., & Huang, Y. K. (2021) · Mitochondrion · doi:10.1016/j.mito.2021.08.012 · Cited by 7 · see citing works
Evolution of Translation in Mitochondria
García-Guerrero, A. E., Zamudio‐Ochoa, A., Camacho‐Villasana, Y., García-Villegas, R., Reyes‐Prieto, A., & Pérez-Martı́nez, X. (2016) · Springer eBooks · doi:10.1007/978-3-319-39468-8_6 · Cited by 5 · see citing works
Mitochondrial Transcription of Entomopathogenic Fungi Reveals Evolutionary Aspects of Mitogenomes
Varassas, S. P., & Kouvelis, V. N. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.821638 · Cited by 5 · see citing works
Interconnected roles of fungal nuclear- and intron-encoded maturases: at the crossroads of mitochondrial intron splicing
Mukhopadhyay, J., & Hausner, G. (2024) · Biochemistry and Cell Biology · doi:10.1139/bcb-2024-0046 · Cited by 4 · see citing works
Pentatricopeptide motifs in the N-terminal extension domain of yeast mitochondrial RNA polymerase Rpo41p are not essential for its function
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Structural analysis of the Candida albicans mitochondrial DNA maintenance factor Gcf1p reveals a dynamic DNA-bridging mechanism
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Additional file 1: of The transcriptome of Candida albicans mitochondria and the evolution of organellar transcription units in yeasts
Kolondra, A., Łabędzka-Dmoch, K., Wenda, J. M., Drzewicka, K., & Golik, P. (2015) · Figshare · doi:10.6084/m9.figshare.c.3614846_d1
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Authors: Kolondra, A., Labedzka-Dmoch, K., Wenda, J. M., Drzewicka, K., & Golik, P.
Affiliations: University of Warsaw (PL)
ORCID: Kolondra, Adam
Wenda, Joanna M.
Golik, Pawel
Venue: BMC Genomics
Publisher: Springer Science and Business Media LLC
Published: 2015-10-21
Volume: 16
Issue: 1
Pages: 827-827
ISSN: 1471-2164 (ISSN-L)
DOI: 10.1186/s12864-015-2078-z
PMC: PMC4618339
OpenAlex: W2107905700
Cited by: 33
References: 145
Citations by year: 2026: 2 · 2025: 1 · 2024: 6 · 2023: 5 · 2022: 4 · 2021: 4 · 2019: 2 · 2018: 3 · 2017: 2 · 2016: 4
FWCI: 1.18
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
Locations: BMC Genomics (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Funders: Foundation For Polish Science (TEAM/2010-6/6)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
Keywords: Candida albicans, mitochondrial transcriptome, mitochondrial genome organization, mitochondrial gene expression, promoter sequence variation, mitochondrial recombination, DNA shuffling, post-transcriptional regulation, antisense transcripts
MeSH terms: Amino Acid Sequence, Base Sequence, Candida albicans, DNA, Mitochondrial, Humans, Introns, Mitochondria, RNA, Ribosomal, RNA, Transfer, Saccharomyces cerevisiae, Schizosaccharomyces, Transcription, Genetic, Organelles, Gene Expression, Gene Expression Regulation, Fungal, Genome, Mitochondrial, High-Throughput Nucleotide Sequencing, Transcriptome

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The transcriptome of Candida albicans mitochondria and the evolution of organellar transcription units in yeasts

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