{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,11]],"date-time":"2026-05-11T10:04:23Z","timestamp":1778493863262,"version":"3.51.4"},"reference-count":73,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2022,1,5]],"date-time":"2022-01-05T00:00:00Z","timestamp":1641340800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e Tecnologia","doi-asserted-by":"publisher","award":["PTDC\/BIAMIC\/5184\/2014"],"award-info":[{"award-number":["PTDC\/BIAMIC\/5184\/2014"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e Tecnologia","doi-asserted-by":"publisher","award":["PD\/BD\/150584\/2020"],"award-info":[{"award-number":["PD\/BD\/150584\/2020"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e Tecnologia","doi-asserted-by":"publisher","award":["CEECINST\/0007772018"],"award-info":[{"award-number":["CEECINST\/0007772018"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Norte 2020","award":["NORTE-08\u20135369-FSE-000060 \/UMINHO\/BD\/25\/2016"],"award-info":[{"award-number":["NORTE-08\u20135369-FSE-000060 \/UMINHO\/BD\/25\/2016"]}]},{"name":"Norte 2020","award":["NORTE-01\u20130145-FEDER-000009"],"award-info":[{"award-number":["NORTE-01\u20130145-FEDER-000009"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JoF"],"abstract":"<jats:p>The yeast Cyberlindnera jadinii has great potential in the biotechnology industry due to its ability to produce a variety of compounds of interest, including carboxylic acids. In this work, we identified genes encoding carboxylate transporters from this yeast species. The functional characterization of sixteen plasma membrane carboxylate transporters belonging to the AceTr, SHS, TDT, MCT, SSS, and DASS families was performed by heterologous expression in Saccharomyces cerevisiae. The newly identified C. jadinii transporters present specificity for mono-, di-, and tricarboxylates. The transporters CjAto5, CjJen6, CjSlc5, and CjSlc13-1 display the broadest substrate specificity; CjAto2 accepts mono- and dicarboxylates; and CjAto1,3,4, CjJen1-5, CjSlc16, and CjSlc13-2 are specific for monocarboxylic acids. A detailed characterization of these transporters, including phylogenetic reconstruction, 3D structure prediction, and molecular docking analysis is presented here. The properties presented by these transporters make them interesting targets to be explored as organic acid exporters in microbial cell factories.<\/jats:p>","DOI":"10.3390\/jof8010051","type":"journal-article","created":{"date-parts":[[2022,1,7]],"date-time":"2022-01-07T01:14:02Z","timestamp":1641518042000},"page":"51","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Uncovering Novel Plasma Membrane Carboxylate Transporters in the Yeast Cyberlindnera jadinii"],"prefix":"10.3390","volume":"8","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-1622-4888","authenticated-orcid":false,"given":"Maria","family":"Sousa-Silva","sequence":"first","affiliation":[{"name":"Centre of Molecular and Environmental Biology (CBMA), Department of Biology, University of Minho, Campus de Gualtar, 4710-057 Braga, Portugal"},{"name":"Institute of Science and Innovation for Bio-Sustainability (IB-S), University of Minho, 4710-057 Braga, Portugal"}]},{"given":"Pedro","family":"Soares","sequence":"additional","affiliation":[{"name":"Centre of Molecular and Environmental Biology (CBMA), Department of Biology, University of Minho, Campus de Gualtar, 4710-057 Braga, Portugal"},{"name":"Institute of Science and Innovation for Bio-Sustainability (IB-S), University of Minho, 4710-057 Braga, Portugal"}]},{"given":"Jo\u00e3o","family":"Alves","sequence":"additional","affiliation":[{"name":"Centre of Molecular and Environmental Biology (CBMA), Department of Biology, University of Minho, Campus de Gualtar, 4710-057 Braga, Portugal"},{"name":"Institute of Science and Innovation for Bio-Sustainability (IB-S), University of Minho, 4710-057 Braga, Portugal"}]},{"given":"Daniel","family":"Vieira","sequence":"additional","affiliation":[{"name":"Centre of Molecular and Environmental Biology (CBMA), Department of Biology, University of Minho, Campus de Gualtar, 4710-057 Braga, Portugal"},{"name":"Institute of Science and Innovation for Bio-Sustainability (IB-S), University of Minho, 4710-057 Braga, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0143-9758","authenticated-orcid":false,"given":"Margarida","family":"Casal","sequence":"additional","affiliation":[{"name":"Centre of Molecular and Environmental Biology (CBMA), Department of Biology, University of Minho, Campus de Gualtar, 4710-057 Braga, Portugal"},{"name":"Institute of Science and Innovation for Bio-Sustainability (IB-S), University of Minho, 4710-057 Braga, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8431-1567","authenticated-orcid":false,"given":"Isabel","family":"Soares-Silva","sequence":"additional","affiliation":[{"name":"Centre of Molecular and Environmental Biology (CBMA), Department of Biology, University of Minho, Campus de Gualtar, 4710-057 Braga, Portugal"},{"name":"Institute of Science and Innovation for Bio-Sustainability (IB-S), University of Minho, 4710-057 Braga, Portugal"}]}],"member":"1968","published-online":{"date-parts":[[2022,1,5]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Sousa-Silva, M., Vieira, D., Soares, P., Casal, M., and Soares-Silva, I. (2021). Expanding the Knowledge on the Skillful Yeast Cyberlindnera jadinii. J. Fungi, 7.","DOI":"10.3390\/jof7010036"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"65","DOI":"10.3109\/07388559209069188","article-title":"Production of food and fodder yeasts","volume":"12","author":"Boze","year":"1992","journal-title":"Crit. Rev. Biotechnol."},{"key":"ref_3","first-page":"407","article-title":"Production of food grade yeasts","volume":"44","author":"Bekatorou","year":"2006","journal-title":"Food Technol. Biotechnol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"6981","DOI":"10.1007\/s00253-016-7700-8","article-title":"Candida utilis and Cyberlindnera (Pichia) jadinii: Yeast relatives with expanding applications","volume":"100","author":"Buerth","year":"2016","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"fnaa118","DOI":"10.1093\/femsle\/fnaa118","article-title":"Membrane transporters in the bioproduction of organic acids: State of the art and future perspectives for industrial applications","volume":"367","author":"Ribas","year":"2020","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"i259","DOI":"10.1093\/bioinformatics\/btn180","article-title":"Annotation-based inference of transporter function","volume":"24","author":"Lee","year":"2008","journal-title":"Bioinformatics"},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Mishra, N., Chang, J., and Zhao, P. (2014). Prediction of membrane transport proteins and their substrate specificities using primary sequence information. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0100278"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"2620","DOI":"10.1128\/JB.181.8.2620-2623.1999","article-title":"The lactate-proton symport of Saccharomyces cerevisiae is encoded by JEN1","volume":"181","author":"Casal","year":"1999","journal-title":"J. Bacteriol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1111\/j.1567-1364.2012.00790.x","article-title":"Lactic acid production in Saccharomyces cerevisiae is modulated by expression of the monocarboxylate transporters Jen1 and Ady2","volume":"12","author":"Pacheco","year":"2012","journal-title":"FEMS Yeast Res."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.fgb.2018.10.001","article-title":"The acetate uptake transporter family motif \u201cNPAPLGL (M\/S)\u201d is essential for substrate uptake","volume":"122","author":"Ribas","year":"2019","journal-title":"Fungal Genet. Biol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1002\/yea.1056","article-title":"Ady2p is essential for the acetate permease activity in the yeast Saccharomyces cerevisiae","volume":"21","author":"Paiva","year":"2004","journal-title":"Yeast"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"644","DOI":"10.1038\/s41422-018-0032-8","article-title":"Succinate-acetate permease from Citrobacter koseri is an anion channel that unidirectionally translocates acetate","volume":"28","author":"Qiu","year":"2018","journal-title":"Cell Res."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"19492","DOI":"10.1074\/jbc.RA118.003876","article-title":"Crystal structure of the bacterial acetate transporter SatP reveals that it forms a hexameric channel","volume":"293","author":"Sun","year":"2018","journal-title":"J. Biol. Chem."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"4412","DOI":"10.1016\/j.csbj.2021.08.002","article-title":"New insights into the acetate uptake transporter (AceTr) family: Unveiling amino acid residues critical for specificity and activity","volume":"19","author":"Alves","year":"2021","journal-title":"Comput. Struct. Biotechnol. J."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"foab033","DOI":"10.1093\/femsyr\/foab033","article-title":"Evolutionary engineering reveals amino acid substitutions in Ato2 and Ato3 that allow improved growth of Saccharomyces cerevisiae on lactic acid","volume":"21","author":"Baldi","year":"2021","journal-title":"FEMS Yeast Res."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0304-4157(98)00023-9","article-title":"Phylogenetic characterization of novel transport protein families revealed by genome analyses","volume":"1422","author":"Saier","year":"1999","journal-title":"Biochim. Biophys. Acta (BBA) Rev. Biomembr."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1069","DOI":"10.1039\/C6MD00005C","article-title":"SLC Transporters: Structure, Function, and Drug Discovery","volume":"7","author":"Colas","year":"2016","journal-title":"Medchemcomm"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1016\/j.apsb.2019.12.006","article-title":"Solute carrier transporters: The metabolic gatekeepers of immune cells","volume":"10","author":"Song","year":"2020","journal-title":"Acta Pharm. Sin. B"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"299","DOI":"10.1016\/j.mam.2012.12.001","article-title":"SLC13 family of Na+-coupled di-and tri-carboxylate\/sulfate transporters","volume":"34","author":"Bergeron","year":"2013","journal-title":"Mol. Asp. Med."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"105484","DOI":"10.1016\/j.pep.2019.105484","article-title":"Expression, purification and crystallization of an SLC16 monocarboxylate transporter family homologue specific for l-lactate","volume":"165","author":"Bonetti","year":"2020","journal-title":"Protein Expr. Purif."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"e61350","DOI":"10.7554\/eLife.61350","article-title":"Structural basis for the reaction cycle of DASS dicarboxylate transporters","volume":"9","author":"Sauer","year":"2020","journal-title":"Elife"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1177","DOI":"10.1007\/s00424-020-02433-x","article-title":"Sodium-coupled glucose transport, the SLC5 family, and therapeutically relevant inhibitors: From molecular discovery to clinical application","volume":"472","author":"Gyimesi","year":"2020","journal-title":"Pfl\u00fcgers Arch. Eur. J. Physiol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"3623","DOI":"10.1128\/aem.57.12.3623-3628.1991","article-title":"Low-and high-affinity transport systems for citric acid in the yeast Candida utilis","volume":"57","year":"1991","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1007\/BF00257039","article-title":"Transport of lactate and other short-chain monocarboxylates in the yeast Candida utilis","volume":"23","year":"1986","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"743","DOI":"10.1002\/yea.320090708","article-title":"A comparative study on the transport of L(-)malic acid and other short-chain carboxylic acids in the yeast Candida utilis: Evidence for a general organic acid permease","volume":"9","year":"1993","journal-title":"Yeast"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1016\/0005-2736(93)90276-6","article-title":"Quantitative analysis of proton movements associated with the uptake of weak carboxylic acids. The yeast Candida utilis as a model","volume":"1153","year":"1993","journal-title":"Biochim. Biophys. Acta (BBA) Biomembr."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"464","DOI":"10.1080\/09687680701342669","article-title":"The conserved sequence NXX [S\/T] HX [S\/T] QDXXXT of the lactate\/pyruvate: H+ symporter subfamily defines the function of the substrate translocation pathway","volume":"24","author":"Paiva","year":"2007","journal-title":"Mol. Membr. Biol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"fox085","DOI":"10.1093\/femsyr\/fox085","article-title":"A CRISPR\/Cas9-based exploration into the elusive mechanism for lactate export in Saccharomyces cerevisiae","volume":"17","author":"Mans","year":"2017","journal-title":"FEMS Yeast Res."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"619","DOI":"10.1016\/0092-8674(89)90584-9","article-title":"Elevated recombination rates in transcriptionally active DNA","volume":"56","author":"Thomas","year":"1989","journal-title":"Cell"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1016\/S0580-9517(06)36025-4","article-title":"25 yeast genetic strain and plasmid collections","volume":"36","author":"Entian","year":"2007","journal-title":"Methods Microbiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1337","DOI":"10.1111\/j.1365-2958.2009.07003.x","article-title":"Functional specialization and differential regulation of short-chain carboxylic acid transporters in the pathogen Candida albicans","volume":"75","author":"Vieira","year":"2010","journal-title":"Mol. Microbiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"781","DOI":"10.1042\/bj20031180","article-title":"Functional expression of the lactate permease Jen1p of Saccharomyces cerevisiae in Pichia pastoris","volume":"376","author":"Schuller","year":"2003","journal-title":"Biochem. J."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"fox005","DOI":"10.1093\/femsyr\/fox005","article-title":"Yeast as a tool to express sugar acid transporters with biotechnological interest","volume":"17","author":"Ribas","year":"2017","journal-title":"FEMS Yeast Res."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1016\/0378-1119(95)00037-7","article-title":"Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds","volume":"156","author":"Mumberg","year":"1995","journal-title":"Gene"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"325","DOI":"10.2144\/000113672","article-title":"Extraction of genomic DNA from yeasts for PCR-based applications","volume":"50","author":"Kristjuhan","year":"2011","journal-title":"BioTechniques"},{"key":"ref_36","unstructured":"Sambrook, J., Fritsch, E., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1692","DOI":"10.1093\/nar\/gkl091","article-title":"M-Coffee: Combining multiple sequence alignment methods with T-Coffee","volume":"34","author":"Wallace","year":"2006","journal-title":"Nucleic Acids Res."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1021\/ci049714+","article-title":"ZINC\u2212 A free database of commercially available compounds for virtual screening","volume":"45","author":"Irwin","year":"2005","journal-title":"J. Chem. Inf. Modeling"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1605","DOI":"10.1002\/jcc.20084","article-title":"UCSF Chimera\u2014A visualization system for exploratory research and analysis","volume":"25","author":"Pettersen","year":"2004","journal-title":"J. Comput. Chem."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Dallakyan, S., and Olson, A. (2015). Small-molecule library screening by docking with PyRx. Chemical Biology, Springer.","DOI":"10.1007\/978-1-4939-2269-7_19"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"354","DOI":"10.1016\/S0263-7855(97)00009-X","article-title":"HOLE: A program for the analysis of the pore dimensions of ion channel structural models","volume":"14","author":"Smart","year":"1996","journal-title":"J. Mol. Graph."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1016\/0263-7855(96)00018-5","article-title":"VMD: Visual molecular dynamics","volume":"14","author":"Humphrey","year":"1996","journal-title":"J. Mol. Graph."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1160","DOI":"10.1093\/bib\/bbx108","article-title":"MAFFT online service: Multiple sequence alignment, interactive sequence choice and visualization","volume":"20","author":"Katoh","year":"2017","journal-title":"Brief. Bioinform."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1870","DOI":"10.1093\/molbev\/msw054","article-title":"MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets","volume":"33","author":"Kumar","year":"2016","journal-title":"Mol. Biol. Evol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"974","DOI":"10.1111\/j.1574-6976.2008.00128.x","article-title":"Transport of carboxylic acids in yeasts","volume":"32","author":"Casal","year":"2008","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"805","DOI":"10.1111\/j.1365-2958.2011.07729.x","article-title":"A substrate translocation trajectory in a cytoplasm-facing topological model of the monocarboxylate\/H+ symporter Jen1p","volume":"81","author":"Myrianthopoulos","year":"2011","journal-title":"Mol. Microbiol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1080\/09687860400011373","article-title":"The disruption of JEN1 from Candida albicans impairs the transport of lactate","volume":"21","author":"Paiva","year":"2004","journal-title":"Mol. Membr. Biol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1007\/s00294-006-0107-9","article-title":"Functional analysis of Kluyveromyces lactis carboxylic acids permeases: Heterologous expression of KlJEN1 and KlJEN2 genes","volume":"51","author":"Pereira","year":"2007","journal-title":"Curr. Genet."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1099\/mic.0.25917-0","article-title":"Characterization, localization and functional analysis of Gpr1p, a protein affecting sensitivity to acetic acid in the yeast Yarrowia lipolytica","volume":"149","author":"Augstein","year":"2003","journal-title":"Microbiology"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"4416","DOI":"10.1128\/IAI.00984-15","article-title":"The Candida albicans ATO gene family promotes neutralization of the macrophage phagolysosome","volume":"83","author":"Danhof","year":"2015","journal-title":"Infect. Immun."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"e00156-20","DOI":"10.1128\/mBio.00156-20","article-title":"Carboxylic Acid Transporters in Candida Pathogenesis","volume":"11","author":"Alves","year":"2020","journal-title":"MBio"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"3901","DOI":"10.1091\/mbc.e01-12-0149","article-title":"Ammonia pulses and metabolic oscillations guide yeast colony development","volume":"13","author":"Devaux","year":"2002","journal-title":"Mol. Biol. Cell"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"485","DOI":"10.1042\/BJ20080124","article-title":"AcpA, a member of the GPR1\/FUN34\/YaaH membrane protein family, is essential for acetate permease activity in the hyphal fungus Aspergillus nidulans","volume":"412","author":"Robellet","year":"2008","journal-title":"Biochem. J."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/j.fgb.2015.02.010","article-title":"Expression and specificity profile of the major acetate transporter AcpA in Aspergillus nidulans","volume":"76","author":"Amillis","year":"2015","journal-title":"Fungal Genet. Biol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1016\/j.fgb.2005.12.008","article-title":"Functional analysis of alcS, a gene of the alc cluster in Aspergillus nidulans","volume":"43","author":"Flipphi","year":"2006","journal-title":"Fungal Genet. Biol."},{"key":"ref_56","first-page":"fov094","article-title":"The Debaryomyces hansenii carboxylate transporters Jen1 homologues are functional in Saccharomyces cerevisiae","volume":"15","author":"Ribas","year":"2015","journal-title":"FEMS Yeast Res."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1002\/mbo3.225","article-title":"The evolution of Jen3 proteins and their role in dicarboxylic acid transport in Yarrowia","volume":"4","author":"Dulermo","year":"2015","journal-title":"Microbiologyopen"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"1130","DOI":"10.1111\/1751-7915.13781","article-title":"Characterization of JEN family carboxylate transporters from the acid-tolerant yeast Pichia kudriavzevii and their applications in succinic acid production","volume":"14","author":"Xi","year":"2021","journal-title":"Microb. Biotechnol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"foz029","DOI":"10.1093\/femsyr\/foz029","article-title":"The Cryptococcus neoformans monocarboxylate transporter Jen4 is responsible for increased 3-bromopyruvate sensitivity","volume":"19","author":"Ribas","year":"2019","journal-title":"FEMS Yeast Res."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"646","DOI":"10.1111\/j.1567-1364.2007.00245.x","article-title":"Evolution of the carboxylate Jen transporters in fungi","volume":"7","author":"Lodi","year":"2007","journal-title":"FEMS Yeast Res."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"644","DOI":"10.1139\/g91-098","article-title":"Sequence and structure of mtr, an amino acid transport gene of Neurospora crassa","volume":"34","author":"Koo","year":"1991","journal-title":"Genome"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1016\/j.bbamem.2004.09.014","article-title":"PcMtr, an aromatic and neutral aliphatic amino acid permease of Penicillium chrysogenum","volume":"1667","author":"Trip","year":"2004","journal-title":"Biochim. Biophys. Acta (BBA) Biomembr."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"585","DOI":"10.1042\/BJ20130412","article-title":"SATP (YaaH), a succinate\u2013acetate transporter protein in Escherichia coli","volume":"454","author":"Paiva","year":"2013","journal-title":"Biochem. J."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1042\/bj3500219","article-title":"The low-affinity monocarboxylate transporter MCT4 is adapted to the export of lactate in highly glycolytic cells","volume":"350","author":"Dimmer","year":"2000","journal-title":"Biochem. J."},{"key":"ref_65","first-page":"1","article-title":"Identification and application of keto acids transporters in Yarrowia lipolytica","volume":"5","author":"Guo","year":"2015","journal-title":"Sci. Rep."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"597","DOI":"10.1007\/s00424-005-1487-2","article-title":"Molecular properties of the SLC13 family of dicarboxylate and sulfate transporters","volume":"451","author":"Pajor","year":"2006","journal-title":"Pfl\u00fcgers Arch. Eur. J. Physiol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1007\/s00424-013-1369-y","article-title":"Sodium-coupled dicarboxylate and citrate transporters from the SLC13 family","volume":"466","author":"Pajor","year":"2014","journal-title":"Pfl\u00fcgers Arch. Eur. J. Physiol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"fnz071","DOI":"10.1093\/femsle\/fnz071","article-title":"Aspergillus niger citrate exporter revealed by comparison of two alternative citrate producing conditions","volume":"366","author":"Odoni","year":"2019","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"224","DOI":"10.1016\/j.ymben.2018.12.004","article-title":"Engineering of the citrate exporter protein enables high citric acid production in Aspergillus niger","volume":"52","author":"Steiger","year":"2019","journal-title":"Metab. Eng."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"foaa055","DOI":"10.1093\/femsyr\/foaa055","article-title":"Identification of the citrate exporter Cex1 of Yarrowia lipolytica","volume":"20","author":"Erian","year":"2020","journal-title":"FEMS Yeast Res."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"4144","DOI":"10.1128\/AEM.67.9.4144-4151.2001","article-title":"Characterization of Schizosaccharomyces pombe malate permease by expression in Saccharomyces cerevisiae","volume":"67","author":"Camarasa","year":"2001","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"15920","DOI":"10.1074\/jbc.273.26.15920","article-title":"Lactic acid efflux from white skeletal muscle is catalyzed by the monocarboxylate transporter isoform MCT3","volume":"273","author":"Wilson","year":"1998","journal-title":"J. Biol. Chem."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1016\/j.gene.2004.06.019","article-title":"Carboxylic acids permeases in yeast: Two genes in Kluyveromyces lactis","volume":"339","author":"Lodi","year":"2004","journal-title":"Gene"}],"container-title":["Journal of Fungi"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2309-608X\/8\/1\/51\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,13]],"date-time":"2025-10-13T13:36:23Z","timestamp":1760362583000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2309-608X\/8\/1\/51"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,1,5]]},"references-count":73,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2022,1]]}},"alternative-id":["jof8010051"],"URL":"https:\/\/doi.org\/10.3390\/jof8010051","relation":{},"ISSN":["2309-608X"],"issn-type":[{"value":"2309-608X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,1,5]]}}}