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We would like to thank Ladislav Kovac and Jordan Kolarov (Comenius University in Bratislava) for stimulating discussions and support, Johannes H. Hegemann (Heinrich-Heine-Universitat, Dusseldorf, Germany) for the plasmid pUG36, and Geraldine Butler (University College Dublin, Ireland) for the C. parapsilosis strain CDUl. We acknowledge the technical support of the sequencing core facility at the Centre for Genomic Regulation. This work was supported by the Slovak grant agency (VEGA) (1/0333/15 and 1/0052/16) and the Slovak Research and Development Agency (APVV) (14-0253 and 15-0022). The T.G. group is supported in part by a grant from the Spanish ministry of Economy and Competitiveness (BI02012-37161), a grant from the Qatar National Research Fund (NPRP 5-298-3-086), and a grant from the European Research Council (ERC) under the European Union's Seventh Framework Program (FP/2007-2013)/ERC (grant agreement no. ERC-2012-StG-310325).

Analysis of institutional authors

Pryszcz, Leszek P.AuthorGabaldon, ToniAuthor

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June 15, 2019
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Article

Mitochondrial Carriers Link the Catabolism of Hydroxyaromatic Compounds to the Central Metabolism in Candida parapsilosis

Publicated to:G3-Genes Genomes Genetics. 6 (12): 4047-4058 - 2016-12-01 6(12), DOI: 10.1534/g3.116.034389

Authors: Zeman, I; Nebohácová, M; Gérecová, G; Katonová, K; Jánosíková, E; Jakúbková, M; Centárová, I; Duncková, I; Tomáska, L; Pryszcz, LP; Gabaldón, T; Nosek, J

Affiliations

Comenius Univ, Fac Nat Sci, Dept Biochem, Mlynska Dolina CH-1,Ilkovicova 6, Bratislava 84215, Slovakia - Author
Comenius Univ, Fac Nat Sci, Dept Genet, Bratislava 84215, Slovakia - Author
Ctr Genom Regulat, Bioinformat & Genom Programme, Barcelona 08003, Spain - Author
Inst Catalana Recerca & Estudis Avancats, Barcelona 08010, Spain - Author
Int Inst Mol & Cell Biol Warsaw, Lab Zebrafish Dev Genom, 4 Ks Trojdena St, PL-02109 Warsaw, Poland - Author
Univ Pompeu Fabra, Dept Ciencies Expt Salut, Barcelona 08003, Spain - Author
Univ Vienna, Dept Biochem & Cell Biol, Max F Perutz Labs, Dr Bohr Gasse 9, A-1030 Vienna, Austria - Author
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Abstract

The pathogenic yeast Candida parapsilosis metabolizes hydroxyderivatives of benzene and benzoic acid to compounds channeled into central metabolism, including the mitochondrially localized tricarboxylic acid cycle, via the 3-oxoadipate and gentisate pathways. The orchestration of both catabolic pathways with mitochondrial metabolism as well as their evolutionary origin is not fully understood. Our results show that the enzymes involved in these two pathways operate in the cytoplasm with the exception of the mitochondrially targeted 3-oxoadipate CoA-transferase (Osc1p) and 3-oxoadipyl-CoA thiolase (Oct1p) catalyzing the last two reactions of the 3-oxoadipate pathway. The cellular localization of the enzymes indicates that degradation of hydroxyaromatic compounds requires a shuttling of intermediates, cofactors, and products of the corresponding biochemical reactions between cytosol and mitochondria. Indeed, we found that yeast cells assimilating hydroxybenzoates increase the expression of genes SFC1, LEU5, YHM2, and MPC1 coding for succinate/fumarate carrier, coenzyme A carrier, oxoglutarate/citrate carrier, and the subunit of pyruvate carrier, respectively. A phylogenetic analysis uncovered distinct evolutionary trajectories for sparsely distributed gene clusters coding for enzymes of both pathways. Whereas the 3-oxoadipate pathway appears to have evolved by vertical descent combined with multiple losses, the gentisate pathway shows a striking pattern suggestive of horizontal gene transfer to the evolutionarily distant Mucorales.

Keywords

3-oxoadipate pathwaycatabolism of hydroxybenzoatesevolution of biochemical pathwaysgentisate pathway3-oxoadipate coa-transferase3-oxoadipate pathway3-oxoadipyl-coenzyme a thiolaseAcetyl-coaAcetyl-coa c-acyltransferaseAscomycotaBiological evolutionCatabolism of hydroxybenzoatesCoenzyme a-transferasesDicarboxylate carrierEvolution of biochemical pathwaysFungal proteinsGene expression regulation, fungalGene-expressionGentisate pathwayHydrocarbons, aromaticIdentificationMetabolic networks and pathwaysMitochondriaMitochondrial carrierMutationOleic-acidPhylogenyProteinProtein transportPyruvate carrierSaccharomyces cerevisiaeSaccharomyces-cerevisiaeSubstrate specificityTransportYeast

Quality index

Bibliometric impact. Analysis of the contribution and dissemination channel

The work has been published in the journal G3-Genes Genomes Genetics due to its progression and the good impact it has achieved in recent years, according to the agency Scopus (SJR), it has become a reference in its field. In the year of publication of the work, 2016, it was in position , thus managing to position itself as a Q1 (Primer Cuartil), in the category Medicine (Miscellaneous). Notably, the journal is positioned above the 90th percentile.

Independientemente del impacto esperado determinado por el canal de difusión, es importante destacar el impacto real observado de la propia aportación.

Según las diferentes agencias de indexación, el número de citas acumuladas por esta publicación hasta la fecha 2025-07-25:

  • WoS: 7
  • Scopus: 5
  • Europe PMC: 4

Impact and social visibility

From the perspective of influence or social adoption, and based on metrics associated with mentions and interactions provided by agencies specializing in calculating the so-called "Alternative or Social Metrics," we can highlight as of 2025-07-25:

  • The use, from an academic perspective evidenced by the Altmetric agency indicator referring to aggregations made by the personal bibliographic manager Mendeley, gives us a total of: 33.
  • The use of this contribution in bookmarks, code forks, additions to favorite lists for recurrent reading, as well as general views, indicates that someone is using the publication as a basis for their current work. This may be a notable indicator of future more formal and academic citations. This claim is supported by the result of the "Capture" indicator, which yields a total of: 36 (PlumX).

With a more dissemination-oriented intent and targeting more general audiences, we can observe other more global scores such as:

  • The Total Score from Altmetric: 8.85.
  • The number of mentions on the social network X (formerly Twitter): 3 (Altmetric).

It is essential to present evidence supporting full alignment with institutional principles and guidelines on Open Science and the Conservation and Dissemination of Intellectual Heritage. A clear example of this is:

  • The work has been submitted to a journal whose editorial policy allows open Open Access publication.

Leadership analysis of institutional authors

This work has been carried out with international collaboration, specifically with researchers from: Austria; Poland; Slovakia.