{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,19]],"date-time":"2026-06-19T05:08:51Z","timestamp":1781845731148,"version":"3.54.5"},"reference-count":53,"publisher":"Elsevier BV","issue":"2","license":[{"start":{"date-parts":[[2025,4,1]],"date-time":"2025-04-01T00:00:00Z","timestamp":1743465600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2025,4,1]],"date-time":"2025-04-01T00:00:00Z","timestamp":1743465600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/legal\/tdmrep-license"}],"funder":[{"DOI":"10.13039\/501100005285","name":"Foundation for Research Support of Goi\u00e1s State","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100005285","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003593","name":"National Council for Scientific and Technological Development","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100003593","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Fungal Biology"],"published-print":{"date-parts":[[2025,4]]},"DOI":"10.1016\/j.funbio.2025.101545","type":"journal-article","created":{"date-parts":[[2025,1,25]],"date-time":"2025-01-25T00:16:49Z","timestamp":1737764209000},"page":"101545","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":2,"title":["Propionate consumption activates mitochondrial activity, methylcitrate cycle and promotes changes in the cell wall of the human pathogen Histoplasma capsulatum"],"prefix":"10.1016","volume":"129","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-8751-7242","authenticated-orcid":false,"given":"Luiz Paulo Ara\u00fajo","family":"Santos","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dayane","family":"Moraes","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Leandro do Prado","family":"Assun\u00e7\u00e3o","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2774-1856","authenticated-orcid":false,"given":"Matthias","family":"Brock","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kassyo Lobato Potenciano","family":"da Silva","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andr\u00e9a Rodrigues","family":"Chaves","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7890-7305","authenticated-orcid":false,"given":"Rafael Oliveira","family":"Martins","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mirelle Garcia","family":"Silva-Bail\u00e3o","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"C\u00e9lia Maria de Almeida","family":"Soares","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7754-4047","authenticated-orcid":false,"given":"Alexandre Melo","family":"Bail\u00e3o","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.funbio.2025.101545_bib1","doi-asserted-by":"crossref","first-page":"1150","DOI":"10.1016\/S1473-3099(18)30354-2","article-title":"Burden of HIV-associated histoplasmosis compared with tuberculosis in Latin America: a modelling study","volume":"18","author":"Adenis","year":"2018","journal-title":"Lancet Infect. Dis."},{"key":"10.1016\/j.funbio.2025.101545_bib2","doi-asserted-by":"crossref","first-page":"1695","DOI":"10.1111\/j.1462-5822.2008.01160.x","article-title":"Vesicular transport in Histoplasma capsulatum: an effective mechanism for trans-cell wall transfer of proteins and lipids in ascomycetes","volume":"10","author":"Albuquerque","year":"2008","journal-title":"Cell Microbiol."},{"issue":"12","key":"10.1016\/j.funbio.2025.101545_bib3","article-title":"Comparative proteomic analysis of Histoplasma capsulatum yeast and mycelium reveals differential metabolic shifts and cell wall remodeling processes in the different morphotypes","volume":"11","author":"Almeida","year":"2021","journal-title":"Front. Microbiol."},{"key":"10.1016\/j.funbio.2025.101545_bib4","doi-asserted-by":"crossref","first-page":"425","DOI":"10.3201\/eid2403.171258","article-title":"Multistate epidemiology of histoplasmosis, estados unidos, 2011-2014","volume":"24","author":"Armstrong","year":"2018","journal-title":"Emerg. Infect. Dis."},{"issue":"10","key":"10.1016\/j.funbio.2025.101545_bib5","article-title":"Insights into Histoplasma capsulatum behavior on zinc deprivation","volume":"30","author":"Assun\u00e7\u00e3o","year":"2020","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"10.1016\/j.funbio.2025.101545_bib6","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1007\/s40475-015-0044-0","article-title":"Histoplasmosis infections worldwide: thinking outside of the Ohio River valley","volume":"1","author":"Bahr","year":"2015","journal-title":"Curr Trop Med Rep"},{"key":"10.1016\/j.funbio.2025.101545_bib7","article-title":"Hemoglobin uptake by Paracoccidioides spp. is receptor-mediated","volume":"15","author":"Bail\u00e3o","year":"2014","journal-title":"PLoS Neglected Trop. Dis."},{"key":"10.1016\/j.funbio.2025.101545_bib8","doi-asserted-by":"crossref","first-page":"2686","DOI":"10.1016\/j.micinf.2006.07.019","article-title":"Differential gene expression by Paracoccidioides brasiliensis in host interaction conditions: representational difference analysis identifies candidate genes associated with fungal pathogenesis","volume":"8","author":"Bailao","year":"2006","journal-title":"Microb. Infect."},{"key":"10.1016\/j.funbio.2025.101545_bib9","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1111\/j.1574-695X.2007.00277.x","article-title":"The transcriptional profile of Paracoccidioides brasiliensis yeast cells is influenced by human plasma","volume":"51","author":"Bailao","year":"2007","journal-title":"FEMS Immunol. Med. Microbiol."},{"key":"10.1016\/j.funbio.2025.101545_bib10","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1146\/annurev.bi.57.070188.001401","article-title":"Carnitine","volume":"57","author":"Bieber","year":"1988","journal-title":"Annu. Rev. Biochem."},{"key":"10.1016\/j.funbio.2025.101545_bib11","article-title":"High-throughput real-time quantitative reverse transcription PCR","volume":"15","author":"Bookout","year":"2006","journal-title":"Curr. Protoc. Mol. Biol."},{"key":"10.1016\/j.funbio.2025.101545_bib12","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1016\/0003-2697(76)90527-3","article-title":"A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding","volume":"7","author":"Bradford","year":"1976","journal-title":"Anal. Biochem."},{"key":"10.1016\/j.funbio.2025.101545_bib13","doi-asserted-by":"crossref","first-page":"3227","DOI":"10.1111\/j.1432-1033.2004.04255.x","article-title":"On the mechanism of action of the antifungal agent propionate","volume":"271","author":"Brock","year":"2004","journal-title":"Eur. J. Biochem."},{"key":"10.1016\/j.funbio.2025.101545_bib14","doi-asserted-by":"crossref","first-page":"961","DOI":"10.1046\/j.1365-2958.2000.01737.x","article-title":"Methylcitrate synthase from Aspergillus nidulans: implications for propionate as an antifungal agent","volume":"35","author":"Brock","year":"2000","journal-title":"Mol. Microbiol."},{"key":"10.1016\/j.funbio.2025.101545_bib15","doi-asserted-by":"crossref","first-page":"6184","DOI":"10.1046\/j.1432-1033.2002.03336.x","article-title":"Oxidation of propionate to pyruvate in Escherichia coli. Involvement of methylcitrate dehydratase and aconitase","volume":"269","author":"Brock","year":"2002","journal-title":"Eur. J. Biochem."},{"key":"10.1016\/j.funbio.2025.101545_bib17","article-title":"Identification of membrane proteome of Paracoccidioides lutzii and its regulation by zinc","volume":"25","author":"De Curcio","year":"2017","journal-title":"Future Sci OA"},{"key":"10.1016\/j.funbio.2025.101545_bib18","doi-asserted-by":"crossref","first-page":"3903","DOI":"10.1099\/mic.0.031781-0","article-title":"Methylcitrate cycle activation during adaptation of Fusarium solani and Fusarium verticillioides to propionyl-CoA-generating carbon sources","volume":"155","author":"Domin","year":"2009","journal-title":"Microbiology (Read.)"},{"key":"10.1016\/j.funbio.2025.101545_bib19","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1139\/m60-009","article-title":"The micromorphology of the tuberculate spores of Histoplasma capsulatum","volume":"6","author":"Edwards","year":"1960","journal-title":"Can. J. Microbiol."},{"key":"10.1016\/j.funbio.2025.101545_bib20","doi-asserted-by":"crossref","first-page":"1605","DOI":"10.1084\/jem.177.6.1605","article-title":"Histoplasma capsulatum modulates the acidification of phagolysosomes","volume":"1","author":"Eissenberg","year":"1993","journal-title":"J. Exp. Med."},{"key":"10.1016\/j.funbio.2025.101545_bib21","doi-asserted-by":"crossref","first-page":"619","DOI":"10.1111\/febs.13389","article-title":"Histoplasma capsulatum surmounts obstacles to intracellular pathogenesis","volume":"283","author":"Garfoot","year":"2016","journal-title":"FEBS J."},{"key":"10.1016\/j.funbio.2025.101545_bib22","doi-asserted-by":"crossref","first-page":"1683","DOI":"10.1002\/pmic.200800562","article-title":"The detection, correlation, and comparison of peptide precursor and product ions from data independent LC-MS with data dependant LC-MS\/MS","volume":"9","author":"Geromanos","year":"2009","journal-title":"Proteomics"},{"key":"10.1016\/j.funbio.2025.101545_bib23","doi-asserted-by":"crossref","first-page":"1929","DOI":"10.1021\/pr1011697","article-title":"Definition of the extracellular proteome of pathogenic-phase Histoplasma capsulatum","volume":"1","author":"Holbrook","year":"2011","journal-title":"J. Proteome Res."},{"key":"10.1016\/j.funbio.2025.101545_bib24","doi-asserted-by":"crossref","first-page":"2334","DOI":"10.1128\/IAI.00173-13","article-title":"Redundant catalases detoxify phagocyte reactive oxygen and facilitate Histoplasma capsulatum pathogenesis","volume":"81","author":"Holbrook","year":"2013","journal-title":"Infect. Immun."},{"key":"10.1016\/j.funbio.2025.101545_bib25","doi-asserted-by":"crossref","first-page":"5615","DOI":"10.1128\/JB.181.18.5615-5623.1999","article-title":"Salmonella typhimurium LT2 catabolizes propionate via the 2-methylcitric acid cycle","volume":"181","author":"Horswill","year":"1999","journal-title":"J. Bacteriol."},{"key":"10.1016\/j.funbio.2025.101545_bib27","first-page":"134","article-title":"Methylcitrate synthase from Aspergillus fumigatus is essential for manifestation of invasive aspergillosis","volume":"10","author":"Ibrahim-Granet","year":"2008","journal-title":"Cell Microbiol."},{"key":"10.1016\/j.funbio.2025.101545_bib28","doi-asserted-by":"crossref","first-page":"1492","DOI":"10.1271\/bbb.130139","article-title":"Gene identification and functional analysis of methylcitrate synthase in citric acid-producing Aspergillus niger Wu-2223L","volume":"77","author":"Kobayashi","year":"2013","journal-title":"Biosci. Biotechnol. Biochem."},{"key":"10.1016\/j.funbio.2025.101545_bib29","doi-asserted-by":"crossref","first-page":"488","DOI":"10.1111\/mmi.13894","article-title":"Acetate provokes mitochondrial stress and cell death in Ustilago maydis","volume":"107","author":"Kretschmer","year":"2018","journal-title":"Mol. Microbiol."},{"key":"10.1016\/j.funbio.2025.101545_bib30","doi-asserted-by":"crossref","first-page":"680","DOI":"10.1038\/227680a0","article-title":"Cleavage of structural proteins during the assembly of the head of bacteriophage T4","volume":"227","author":"Laemmli","year":"1970","journal-title":"Nature"},{"key":"10.1016\/j.funbio.2025.101545_bib31","doi-asserted-by":"crossref","first-page":"894","DOI":"10.1111\/mmi.12139","article-title":"The 2-methylcitrate cycle is implicated in the detoxification of propionate in Toxoplasma gondii","volume":"87","author":"Limenitakis","year":"2013","journal-title":"Mol. Microbiol."},{"key":"10.1016\/j.funbio.2025.101545_bib32","doi-asserted-by":"crossref","first-page":"3615","DOI":"10.1111\/j.1742-4658.2005.04784.x","article-title":"Methylcitrate synthase from Aspergillus fumigatus. Propionyl-CoA affects polyketide synthesis, growth and morphology of conidia","volume":"272","author":"Maerker","year":"2005","journal-title":"FEBS J."},{"key":"10.1016\/j.funbio.2025.101545_bib33","doi-asserted-by":"crossref","first-page":"1551","DOI":"10.1016\/j.funbio.2023.05.004","article-title":"High copper promotes cell wall remodeling and oxidative stress in Histoplasma capsulatum, as revealed by proteomics","volume":"127","author":"Moraes","year":"2023","journal-title":"Fungal Biol."},{"key":"10.1016\/j.funbio.2025.101545_bib34","doi-asserted-by":"crossref","first-page":"1109","DOI":"10.1111\/j.1365-2958.2006.05155.x","article-title":"Role of the methylcitrate cycle in Mycobacterium tuberculosis metabolism, intracellular growth, and virulence","volume":"60","author":"Mu\u00f1oz-El\u00edas","year":"2006","journal-title":"Mol. Microbiol."},{"key":"10.1016\/j.funbio.2025.101545_bib35","doi-asserted-by":"crossref","first-page":"2618","DOI":"10.1002\/jssc.201100238","article-title":"Detection and expression analysis of recombinant proteins in plant-derived complex mixtures using nanoUPLC-MS(E)","volume":"34","author":"Murad","year":"2011","journal-title":"J. Separ. Sci."},{"key":"10.1016\/j.funbio.2025.101545_bib36","doi-asserted-by":"crossref","DOI":"10.1016\/j.micres.2021.126730","article-title":"iTRAQ-based proteomic analysis of Paracoccidioides brasiliensis in response to hypoxia","volume":"247","author":"Oliveira","year":"2021","journal-title":"Microbiol. Res."},{"key":"10.1016\/j.funbio.2025.101545_bib37","doi-asserted-by":"crossref","first-page":"8151","DOI":"10.1074\/jbc.M113.517672","article-title":"Candida albicans utilizes a modified \u03b2-oxidation pathway for the degradation of toxic propionyl-CoA","volume":"21","author":"Otzen","year":"2014","journal-title":"J. Biol. Chem."},{"key":"10.1016\/j.funbio.2025.101545_bib38","doi-asserted-by":"crossref","first-page":"486","DOI":"10.1590\/S0074-02762009000300015","article-title":"Preferential transcription of Paracoccidioides brasiliensis genes: host niche and time-dependent expression","volume":"104","author":"Pereira","year":"2009","journal-title":"Mem. Inst. Oswaldo Cruz"},{"key":"10.1016\/j.funbio.2025.101545_bib39","doi-asserted-by":"crossref","first-page":"1834","DOI":"10.3389\/fmicb.2020.01834","article-title":"Metabolic adaptation of Paracoccidioides brasiliensis in response to in vitro copper deprivation","volume":"10","author":"Petito","year":"2020","journal-title":"Front. Microbiol."},{"key":"10.1016\/j.funbio.2025.101545_bib40","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1128\/jcm.12.2.279-281.1980","article-title":"Growth of Paracoccidioides brasiliensis yeast phase in a chemically defined culture medium","volume":"12","author":"Restrepo","year":"1980","journal-title":"J. Clin. Microbiol."},{"key":"10.1016\/j.funbio.2025.101545_bib41","doi-asserted-by":"crossref","first-page":"108","DOI":"10.3390\/jof9010108","article-title":"New methylcitrate synthase inhibitor induces proteolysis, lipid degradation and pyruvate excretion in Paracoccidioides brasiliensis","volume":"13","author":"Rocha","year":"2023","journal-title":"J Fungi (Basel)"},{"key":"10.1016\/j.funbio.2025.101545_bib42","first-page":"79","article-title":"Histoplasmosis and epizootic lymphangitis","volume":"16","author":"Rocha-Lima","year":"1912","journal-title":"Arch Schiffs Tropenhyg"},{"key":"10.1016\/j.funbio.2025.101545_bib43","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1186\/s43008-020-00029-9","article-title":"Propionate metabolism in a human pathogenic fungus: proteomic and biochemical analyses","volume":"5","author":"Santos","year":"2020","journal-title":"IMA Fungus"},{"key":"10.1016\/j.funbio.2025.101545_bib44","doi-asserted-by":"crossref","first-page":"3886","DOI":"10.1128\/JB.01767-07","article-title":"Functional characterization of a vitamin B12-dependent methylmalonyl pathway in Mycobacterium tuberculosis: implications for propionate metabolism during growth on fatty acids","volume":"190","author":"Savvi","year":"2008","journal-title":"J. Bacteriol."},{"key":"10.1016\/j.funbio.2025.101545_bib55","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1016\/S0006-3495(99)77214-0","article-title":"Measurement of mitochondrial membrane potential using fluorescent rhodamine derivatives","volume":"6","author":"Scaduto","year":"1999","journal-title":"Biophys. J."},{"key":"10.1016\/j.funbio.2025.101545_bib45","first-page":"e02712","article-title":"Metabolism of gluconeogenic substrates by an intracellular fungal pathogen circumvents nutritional limitations within macrophages","volume":"7","author":"Shen","year":"2020","journal-title":"mBio"},{"key":"10.1016\/j.funbio.2025.101545_bib46","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1016\/j.mib.2019.10.011","article-title":"Molecular regulation of Histoplasma dimorphism","volume":"52","author":"Sil","year":"2019","journal-title":"Curr. Opin. Microbiol."},{"key":"10.1016\/j.funbio.2025.101545_bib47","article-title":"Considerations about the geographic distribution of Histoplasma species","volume":"12","author":"Taylor","year":"2022","journal-title":"Appl. Environ. Microbiol."},{"key":"10.1016\/j.funbio.2025.101545_bib48","first-page":"1411","article-title":"Properties of methylcitrate synthase from Candida lipolytica","volume":"40","author":"Uchiyama","year":"1976","journal-title":"Agric. Biol. Chem."},{"key":"10.1016\/j.funbio.2025.101545_bib49","doi-asserted-by":"crossref","first-page":"1947","DOI":"10.1073\/pnas.0605728104","article-title":"A gene cluster encoding cholesterol catabolism in a soil actinomycete provides insight into Mycobacterium tuberculosis survival in macrophages","volume":"6","author":"Van der Geize","year":"2007","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"10.1016\/j.funbio.2025.101545_bib50","doi-asserted-by":"crossref","first-page":"28953","DOI":"10.1074\/jbc.271.46.28953","article-title":"The two acetyl-coenzyme A synthetases of Saccharomyces cerevisiae differ with respect to kinetic properties and transcriptional regulation","volume":"15","author":"Van den Berg","year":"1996","journal-title":"J. Biol. Chem."},{"key":"10.1016\/j.funbio.2025.101545_bib51","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0052470","article-title":"Analysis of the secretomes of Paracoccidioides mycelia and yeast cells","volume":"7","author":"Weber","year":"2012","journal-title":"PLoS One"},{"key":"10.1016\/j.funbio.2025.101545_bib52","doi-asserted-by":"crossref","first-page":"3819","DOI":"10.1021\/bi9005418","article-title":"Cholesterol metabolism increases the metabolic pool of propionate in Mycobacterium tuberculosis","volume":"12","author":"Yang","year":"2009","journal-title":"Biochemistry"},{"key":"10.1016\/j.funbio.2025.101545_bib53","doi-asserted-by":"crossref","DOI":"10.1371\/journal.ppat.1002713","article-title":"Extracellular superoxide dismutase protects Histoplasma yeast cells from host-derived oxidative stress","volume":"8","author":"Youseff","year":"2012","journal-title":"PLoS Pathog."},{"key":"10.1016\/j.funbio.2025.101545_bib54","doi-asserted-by":"crossref","DOI":"10.1093\/femsyr\/fow089","article-title":"A novel fungal killing mechanism of propionic acid","volume":"16","author":"Yun","year":"2016","journal-title":"FEMS Yeast Res."}],"container-title":["Fungal Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S187861462500011X?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S187861462500011X?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2025,2,27]],"date-time":"2025-02-27T23:59:26Z","timestamp":1740700766000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S187861462500011X"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,4]]},"references-count":53,"journal-issue":{"issue":"2","published-print":{"date-parts":[[2025,4]]}},"alternative-id":["S187861462500011X"],"URL":"https:\/\/doi.org\/10.1016\/j.funbio.2025.101545","relation":{},"ISSN":["1878-6146"],"issn-type":[{"value":"1878-6146","type":"print"}],"subject":[],"published":{"date-parts":[[2025,4]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Propionate consumption activates mitochondrial activity, methylcitrate cycle and promotes changes in the cell wall of the human pathogen Histoplasma capsulatum","name":"articletitle","label":"Article Title"},{"value":"Fungal Biology","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.funbio.2025.101545","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2025 British Mycological Society. Published by Elsevier Ltd. All rights are reserved, including those for text and data mining, AI training, and similar technologies.","name":"copyright","label":"Copyright"}],"article-number":"101545"}}