The metabolic growth limitations of petite cells lacking the mitochondrial genome

Vowinckel, Jakob; Hartl, Johannes; Marx, Hans; Kerick, Martin; Runggatscher, Kathrin; Keller, Markus A.; Mülleder, Michael; Day, Jason; Weber, Manuela; Rinnerthaler, Mark; Yu, Jason S. L.; Aulakh, Simran Kaur; Lehmann, Andrea; Mattanovich, Diethard; Timmermann, Bernd; Zhang, Nianshu; Dunn, Cory D.; MacRae, James I.; Breitenbach, Michael; Ralser, Markus

doi:10.1038/s42255-021-00477-6

Cited by 48Mitochondrial Function and PathologyFungal and yeast genetics researchAutophagy in Disease and Therapy

The metabolic growth limitations of petite cells lacking the mitochondrial genome

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Vowinckel, Jakob, Hartl, Johannes, Marx, Hans, Kerick, Martin, Runggatscher, Kathrin, Keller, Markus A., Mülleder, Michael, Day, Jason +12 more·2021·Nature Metabolism

DOI 10.1038/s42255-021-00477-6PMC PMC7612105

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Abstract

Eukaryotic cells can survive the loss of their mitochondrial genome, but consequently suffer from severe growth defects. 'Petite yeasts', characterized by mitochondrial genome loss, are instrumental for studying mitochondrial function and physiology. However, the molecular cause of their reduced growth rate remains an open question. Here we show that petite cells suffer from an insufficient capacity to synthesize glutamate, glutamine, leucine and arginine, negatively impacting their growth. Using a combination of molecular genetics and omics approaches, we demonstrate the evolution of fast growth overcomes these amino acid deficiencies, by alleviating a perturbation in mitochondrial iron metabolism and by restoring a defect in the mitochondrial tricarboxylic acid cycle, caused by aconitase inhibition. Our results hence explain the slow growth of mitochondrial genome-deficient cells with a partial auxotrophy in four amino acids that results from distorted iron metabolism and an inhibited tricarboxylic acid cycle.

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Petite mutants of S. cerevisiae exhibit deficiencies in leucine, arginine, glutamate, and glutamine but not in amino acids derived from the reductive part of the TCA cycle, such as aspartate.
“petite mutants of S. cerevisiae exhibit deficiencies in leucine, arginine, glutamate, and glutamine but not in amino acids derived from the reductive part of the TCA cycle, such as aspartate (10).”
From Overlooked Candida glabrata petites are echinocandin tolerant, induce host inflammatory responses, and display poor in vivo fitness (2023) · cites this paper as [10]
The Introduction and Discussion say that petite cells have insufficient biosynthetic capacity for leucine, arginine, glutamate and glutamine. The passages from the Results on amino-acid supply and TCA-cycle inhibition do not establish the claimed contrast with amino acids derived from the reductive part of the TCA cycle, such as aspartate; a search for aspartate found no such finding in our copy. Page numbers were not available for these passages. (LLM, conf=0.84)
Experimental — accuracy not yet measured
Petites are not considered an end-stage phenotype, as they can convert to mitochondrial proficient cells under certain in vitro and in-host conditions.
“petites are not considered an end-stage phenotype, as they can convert to mitochondrial proficient cells under certain in vitro (10) and in-host (38) conditions.”
From Overlooked Candida glabrata petites are echinocandin tolerant, induce host inflammatory responses, and display poor in vivo fitness (2023) · cites this paper as [10]
The Introduction and Results describe petite cells adapting in vitro to grow nearly as fast as wild type, supporting the idea that the slow-growth phenotype is not fixed. But the adapted cells remain without mitochondrial DNA; the paper does not show them converting to mitochondrially proficient cells. The in-host condition is cited to a different source (38), not this paper (10). (LLM, conf=0.84)
Experimental — accuracy not yet measured
Mitochondrial pathways are important for amino acid production.
“given the importance of mitochondrial pathways for amino acid production (10, 18).”
From Overlooked Candida glabrata petites are echinocandin tolerant, induce host inflammatory responses, and display poor in vivo fitness (2023) · cites this paper as [10]

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Phosphate starvation signaling increases mitochondrial membrane potential through respiration-independent mechanisms
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Genetically controlled mtDNA deletions prevent ROS damage by arresting oxidative phosphorylation
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Overlooked Candida glabrata petites are echinocandin tolerant, induce host inflammatory responses, and display poor in vivo fitness
Arastehfar, A., Daneshnia, F., Hovhannisyan, H., Fuentes, D., Cabrera, N., Quinteros, C., Ilkit, M., Ünal, N., Hilmioğlu-Polat, S., Jabeen, K., et al. (2023) · mBio · doi:10.1128/mbio.01180-23 · Cited by 27 · see citing works
“Finally, screening of a large collection of C. glabrata blood isolates from three different countries revealed that petite prevalence can vary between 0% and 3.3% of the total blood isolates and that, similar to SCVs, petites can also be found as a mixture of small and large colonies.”
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Vom Genotyp zum Phänotyp: mikrobielle Anpassung molekular entschlüsseln
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Self-citation
Mitochondrial dysfunction and apoptosis-related gene activation induced by combined ethyl acetate fractions of Uncaria sp. and Selaginella doederleinii in Saccharomyces cerevisiae
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Evolutionary rescue in toxic combinations of metal is dependent on metal interactionsPreprint
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The amino acid nutrition of respiration deficient and respiration competentSaccharomyces
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Mitochondrial respiration is required to provide amino acids during fermentative proliferation of fission yeast
Malecki, M., Kamrad, S., Ralser, M., & Bähler, J. (2020) · The EMBO Reports · doi:10.15252/embr.202050845 · Cited by 50 · see citing works
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Amino acid starvation has opposite effects on mitochondrial and cytosolic protein synthesis
Johnson, M. A., Vidoni, S., Durigon, R., Pearce, S. F., Rorbach, J., He, J., Brea-Calvo, G., Minczuk, M., Reyes, A., Holt, I. J., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0093597 · Cited by 63 · see citing works
Mitochondrial and cellular inhibition by the folate analogue pyrimethamine in Saccharomyces cerevisiae
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Suppression of the petite-phenotype in cells without mitochondrial DNA
Hartl, J. (2014)
Self-citation

Authors: Vowinckel, J., Hartl, J., Marx, H., Kerick, M., Runggatscher, K., Keller, M. A., Mülleder, M., Day, J., Weber, M., Rinnerthaler, M., Yu, J. S. L., Aulakh, S. K., Lehmann, A., Mattanovich, D., Timmermann, B., Zhang, N., Dunn, C. D., MacRae, J. I., Breitenbach, M., & Ralser, M.
Affiliations: University of Cambridge (GB)
BOKU University (AT)
Max Planck Institute for Molecular Genetics (DE)
Innsbruck Medical University (AT)
University of Salzburg (AT)
The Francis Crick Institute (GB)
Humboldt-Universität zu Berlin (DE)
University of Helsinki (FI)
Corresponding author: Ralser, Markus
ORCID: Vowinckel, Jakob
Hartl, Johannes
Marx, Hans
Kerick, Martin
Keller, Markus A.
Mülleder, Michael
Day, Jason
Rinnerthaler, Mark
Yu, Jason S. L.
Aulakh, Simran Kaur
Lehmann, Andrea
Mattanovich, Diethard
Zhang, Nianshu
Dunn, Cory D.
MacRae, James I.
Breitenbach, Michael
Ralser, Markus
Venue: Nature Metabolism
Publisher: Springer Science and Business Media LLC
Published: 2021-11-18
Volume: 3
Issue: 11
Pages: 1521-1535
ISSN: 2522-5812 (ISSN-L)
DOI: 10.1038/s42255-021-00477-6
PMC: PMC7612105
OpenAlex: W3211868415
Cited by: 48
References: 122
Citations by year: 2026: 10 · 2025: 7 · 2024: 7 · 2023: 15 · 2022: 9
FWCI: 2.43
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springernature.com/gp/researchers/text-and-data-mining (tdm)
www.springernature.com/gp/researchers/text-and-data-mining (vor)
Locations: Nature Metabolism (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
Funders: Wellcome Trust (200829, FC001134, 200829/Z/16/Z)
Francis Crick Institute (10134, 10012)
Cancer Research UK (FC001134)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
Keywords: growth defects, amino acid synthesis, glutamate, glutamine, leucine, L-arginine, auxotrophy, mitochondrial iron metabolism, TCA cycle, aconitase inhibition
MeSH terms: Amino Acids, Citric Acid Cycle, Energy Metabolism, Fungal Proteins, Mitochondria, Mutation, Phenotype, Structure-Activity Relationship, Yeasts, Biomass, Cell Proliferation, Membrane Potential, Mitochondrial, Genome, Mitochondrial

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