{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,28]],"date-time":"2026-02-28T08:50:56Z","timestamp":1772268656752,"version":"3.50.1"},"reference-count":68,"publisher":"Oxford University Press (OUP)","issue":"12","license":[{"start":{"date-parts":[[2020,12,1]],"date-time":"2020-12-01T00:00:00Z","timestamp":1606780800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"},{"start":{"date-parts":[[2021,11,23]],"date-time":"2021-11-23T00:00:00Z","timestamp":1637625600000},"content-version":"am","delay-in-days":357,"URL":"http:\/\/rsc.li\/journals-terms-of-use"}],"funder":[{"DOI":"10.13039\/501100004586","name":"Funda\u00e7\u00e3o Carlos Chagas Filho de Amparo \u00e0 Pesquisa do Estado do Rio de Janeiro","doi-asserted-by":"publisher","award":["E-26\/202.918\/2017"],"award-info":[{"award-number":["E-26\/202.918\/2017"]}],"id":[{"id":"10.13039\/501100004586","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003593","name":"Conselho Nacional de Desenvolvimento Cient\u00edfico e Tecnol\u00f3gico","doi-asserted-by":"publisher","award":["307547\/2017-5"],"award-info":[{"award-number":["307547\/2017-5"]}],"id":[{"id":"10.13039\/501100003593","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002322","name":"Coordena\u00e7\u00e3o de Aperfei\u00e7oamento de Pessoal de N\u00edvel Superior","doi-asserted-by":"publisher","award":["001"],"award-info":[{"award-number":["001"]}],"id":[{"id":"10.13039\/501100002322","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["rsc.org"],"crossmark-restriction":true},"short-container-title":[],"published-print":{"date-parts":[[2020,12,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Iron is an essential nutrient but is toxic in excess mainly under acidic conditions. Yeasts have emerged as low cost, highly efficient soil inoculants for the decontamination of metal-polluted areas, harnessing an increasing understanding of their metal tolerance mechanisms. Here, we investigated the effects of extracellular iron and acid pH stress on the dimorphism of Yarrowia lipolytica. Its growth was unaffected by 1 or 2 mM FeSO4, while a strong cellular iron accumulation was detected. However, the iron treatments decreased the hyphal length and number, mainly at 2 mM FeSO4 and pH 4.5. Inward cell membrane H+ fluxes were found at pH 4.5 and 6.0 correlated with a pH increase at the cell surface and a conspicuous yeast-to-hypha transition activity. Conversely, a remarkable H+ efflux was detected at pH 3.0, related to the extracellular microenvironment acidification and inhibition of yeast-to-hypha transition. Iron treatments intensified H+ influxes at pH 4.5 and 6.0 and inhibited H+ efflux at pH 3.0. Moreover, iron treatments inhibited the expression and activities of the plasma membrane H+-ATPase, with the H+ transport inhibited to a greater extent than the ATP hydrolysis, suggesting an iron-induced uncoupling of the pump. Our data indicate that Y. lipolytica adaptations to high iron and acidic environments occur at the expense of remodelling the yeast morphogenesis through a cellular pH modulation by H+-ATPases and H+ coupled transporters, highlighting the capacity of this non-conventional yeast to accumulate high amounts of iron and its potential application for bioremediation.<\/jats:p>","DOI":"10.1039\/d0mt00179a","type":"journal-article","created":{"date-parts":[[2020,11,23]],"date-time":"2020-11-23T22:13:01Z","timestamp":1606169581000},"page":"2174-2185","update-policy":"https:\/\/doi.org\/10.1039\/rsc_crossmark_policy","source":"Crossref","is-referenced-by-count":7,"title":["Plasma membrane H+ pump at a crossroads of acidic and iron stresses in yeast-to-hypha transition"],"prefix":"10.1093","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-1967-6898","authenticated-orcid":false,"given":"Ant\u00f4nio Jesus Dorighetto","family":"Cogo","sequence":"first","affiliation":[{"name":"Laborat\u00f3rio de Bioqu\u00edmica e Fisiologia de Microrganismos, Centro de Bioci\u00eancias e Biotecnologia, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Campos dos Goytacazes, RJ, Brazil"},{"name":"Laborat\u00f3rio de Biologia Celular e Tecidual, Centro de Bioci\u00eancias e Biotecnologia, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Campos dos Goytacazes, RJ, Brazil"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5641-6852","authenticated-orcid":false,"given":"Arnoldo Rocha","family":"Fa\u00e7anha","sequence":"additional","affiliation":[{"name":"Laborat\u00f3rio de Biologia Celular e Tecidual, Centro de Bioci\u00eancias e Biotecnologia, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Campos dos Goytacazes, RJ, Brazil"}]},{"given":"Layz Ribeiro","family":"da Silva Teixeira","sequence":"additional","affiliation":[{"name":"Laborat\u00f3rio de Bioqu\u00edmica e Fisiologia de Microrganismos, Centro de Bioci\u00eancias e Biotecnologia, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Campos dos Goytacazes, RJ, Brazil"}]},{"given":"S\u00e1vio Bastos","family":"de Souza","sequence":"additional","affiliation":[{"name":"Laborat\u00f3rio de Biologia Celular e Tecidual, Centro de Bioci\u00eancias e Biotecnologia, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Campos dos Goytacazes, RJ, Brazil"}]},{"given":"Jani\u00e9lio Gon\u00e7alves","family":"da Rocha","sequence":"additional","affiliation":[{"name":"Laborat\u00f3rio de Biologia Celular e Tecidual, Centro de Bioci\u00eancias e Biotecnologia, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Campos dos Goytacazes, RJ, Brazil"}]},{"given":"Frederico Firme","family":"Figueira","sequence":"additional","affiliation":[{"name":"Laborat\u00f3rio de Bioqu\u00edmica e Fisiologia de Microrganismos, Centro de Bioci\u00eancias e Biotecnologia, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Campos dos Goytacazes, RJ, Brazil"},{"name":"Laborat\u00f3rio de Biologia Celular e Tecidual, Centro de Bioci\u00eancias e Biotecnologia, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Campos dos Goytacazes, RJ, Brazil"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6393-4976","authenticated-orcid":false,"given":"Frederico Jacob","family":"Eutr\u00f3pio","sequence":"additional","affiliation":[{"name":"Instituto Capixaba de Ci\u00eancia e Administra\u00e7\u00e3o, Vit\u00f3ria, ES, Brazil"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8082-5501","authenticated-orcid":false,"given":"Amanda Azevedo","family":"Bertolazi","sequence":"additional","affiliation":[{"name":"Laborat\u00f3rio de Biologia Celular e Tecidual, Centro de Bioci\u00eancias e Biotecnologia, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Campos dos Goytacazes, RJ, Brazil"},{"name":"Laborat\u00f3rio de Microbiologia Ambiental e Biotecnologia, Universidade de Vila Velha, ES, Brazil"}]},{"given":"Carlos Eduardo","family":"de Rezende","sequence":"additional","affiliation":[{"name":"Laborat\u00f3rio de Ci\u00eancias Ambientais, Centro de Bioci\u00eancias e Biotecnologia, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Campos dos Goytacazes, RJ, Brazil"}]},{"given":"Cesar Abel","family":"Krohling","sequence":"additional","affiliation":[{"name":"Instituto Capixaba de Pesquisa, Assist\u00eancia T\u00e9cnica e Extens\u00e3o Rural, Marechal Floriano, ES, Brazil"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8469-0701","authenticated-orcid":false,"given":"Lev A","family":"Okorokov","sequence":"additional","affiliation":[{"name":"Laborat\u00f3rio de Bioqu\u00edmica e Fisiologia de Microrganismos, Centro de Bioci\u00eancias e Biotecnologia, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Campos dos Goytacazes, RJ, Brazil"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3100-463X","authenticated-orcid":false,"given":"Cristina","family":"Cruz","sequence":"additional","affiliation":[{"name":"Center for Ecology, Evolution and Environmental Changes, Faculdade de Ci\u00eancias, Universidade de Lisboa, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4082-0076","authenticated-orcid":false,"given":"Alessandro Coutinho","family":"Ramos","sequence":"additional","affiliation":[{"name":"Instituto Capixaba de Ci\u00eancia e Administra\u00e7\u00e3o, Vit\u00f3ria, ES, Brazil"},{"name":"Laborat\u00f3rio de Microbiologia Ambiental e Biotecnologia, Universidade de Vila Velha, ES, Brazil"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6856-7711","authenticated-orcid":false,"given":"Anna L","family":"Okorokova-Fa\u00e7anha","sequence":"additional","affiliation":[{"name":"Laborat\u00f3rio de Bioqu\u00edmica e Fisiologia de Microrganismos, Centro de Bioci\u00eancias e Biotecnologia, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Campos dos Goytacazes, RJ, Brazil"}]}],"member":"286","published-online":{"date-parts":[[2020,12,15]]},"reference":[{"key":"2021121004471456300_cit1","doi-asserted-by":"crossref","first-page":"815","DOI":"10.1104\/pp.104.3.815","article-title":"Iron: nutritious, noxious, and not readily available","volume":"104","author":"Guerinot","year":"1994","journal-title":"Plant Physiol."},{"key":"2021121004471456300_cit2","doi-asserted-by":"crossref","first-page":"944","DOI":"10.1126\/science.1083545","article-title":"The biogeochemical cycles of trace metals in the oceans","volume":"300","author":"Morel","year":"2003","journal-title":"Science"},{"key":"2021121004471456300_cit3","doi-asserted-by":"crossref","first-page":"1477","DOI":"10.1021\/cb300323q","article-title":"The ubiquity of iron","volume":"7","author":"Frey","year":"2012","journal-title":"ACS Chem. Biol."},{"key":"2021121004471456300_cit4","article-title":"Environmental Inorganic Chemistry: Properties, Processes, and Estimation Methods","volume-title":"SETAC Special Publication Series","author":"Walton","year":"1988"},{"key":"2021121004471456300_cit5","doi-asserted-by":"crossref","first-page":"558","DOI":"10.1002\/jpln.200520504","article-title":"Iron toxicity in rice \u2013 conditions and management concepts","volume":"168","author":"Becker","year":"2005","journal-title":"J. Plant Nutr. Soil Sci."},{"key":"2021121004471456300_cit6","doi-asserted-by":"crossref","first-page":"750","DOI":"10.1007\/s13238-014-0083-7","article-title":"Essential functions of iron-requiring proteins in DNA replication, repair and cell cycle control","volume":"5","author":"Zhang","year":"2014","journal-title":"Protein Cell"},{"key":"2021121004471456300_cit7","doi-asserted-by":"crossref","first-page":"1107","DOI":"10.1039\/C4MT00031E","article-title":"Heme in the marine environment: from cells to the iron cycle","volume":"6","author":"Hogle","year":"2014","journal-title":"Metallomics"},{"key":"2021121004471456300_cit8","doi-asserted-by":"crossref","first-page":"1483","DOI":"10.1039\/C7MT00116A","article-title":"The elemental role of iron in DNA synthesis and repair","volume":"9","author":"Puig","year":"2017","journal-title":"Metallomics"},{"key":"2021121004471456300_cit9","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1146\/annurev-arplant-042811-105522","article-title":"Iron uptake, translocation, and regulation in higher plants","volume":"63","author":"Kobayashi","year":"2012","journal-title":"Annu. Rev. Plant Biol."},{"key":"2021121004471456300_cit10","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1039\/C6MT00301J","article-title":"Iron acquisition in fungal pathogens of humans","volume":"9","author":"Bairwa","year":"2017","journal-title":"Metallomics"},{"key":"2021121004471456300_cit11","doi-asserted-by":"crossref","first-page":"1906","DOI":"10.1128\/AEM.03464-15","article-title":"Responses of Saccharomyces cerevisiae strains from different origins to elevated iron concentrations","volume":"82","author":"Mart\u00ednez-Garay","year":"2016","journal-title":"Appl. Environ. Microbiol."},{"key":"2021121004471456300_cit12","doi-asserted-by":"crossref","first-page":"602","DOI":"10.1101\/gad.314674.118","article-title":"Regulation of lipid peroxidation and ferroptosis in diverse species","volume":"32","author":"Conrad","year":"2018","journal-title":"Genes Dev."},{"key":"2021121004471456300_cit13","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1016\/j.cmet.2012.06.004","article-title":"Sphingolipid signaling mediates iron toxicity","volume":"16","author":"Lee","year":"2012","journal-title":"Cell Metab."},{"key":"2021121004471456300_cit14","doi-asserted-by":"crossref","first-page":"384","DOI":"10.4172\/1948-5948.1000243","article-title":"Heavy metal contaminants removal from wastewater using the potential filamentous fungi biomass: A review","volume":"7","author":"Siddique","year":"2015","journal-title":"J. Microb. Biochem. Technol."},{"key":"2021121004471456300_cit15","doi-asserted-by":"crossref","first-page":"269","DOI":"10.5772\/intechopen.70559","article-title":"Yeast Biomass: An alternative for bioremediation of heavy metals","volume-title":"Yeast-Industrial Applications","author":"Bahafid","year":"2017"},{"key":"2021121004471456300_cit16","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1016\/j.envint.2003.08.001","article-title":"Metal bioremediation through growing cells","volume":"30","author":"Malik","year":"2004","journal-title":"Environ. Int."},{"key":"2021121004471456300_cit17","doi-asserted-by":"crossref","first-page":"4080","DOI":"10.1038\/s41467-019-12085-w","article-title":"Comparative genomics reveals the origin of fungal hyphae and multicellularity","volume":"10","author":"Kiss","year":"2019","journal-title":"Nat. Commun."},{"key":"2021121004471456300_cit18","doi-asserted-by":"crossref","first-page":"847","DOI":"10.1007\/s00253-009-2156-8","article-title":"Environmental and industrial applications of Yarrowia lipolytica","volume":"84","author":"Bankar","year":"2009","journal-title":"Appl. Microbiol. Biotechnol."},{"key":"2021121004471456300_cit19","doi-asserted-by":"crossref","first-page":"920","DOI":"10.1016\/j.biotechadv.2014.04.008","article-title":"Yarrowia lipolytica and pollutants: Interactions and applications","volume":"32","author":"Zinjarde","year":"2014","journal-title":"Biotechnol. Adv."},{"key":"2021121004471456300_cit20","doi-asserted-by":"crossref","first-page":"449","DOI":"10.1016\/j.chemosphere.2004.04.003","article-title":"Improvement of soil characteristics and growth of Dorycnium pentaphyllum by amendment with agrowastes and inoculation with AM fungi and\/or the yeast Yarrowia lipolytica","volume":"56","author":"Medina","year":"2004","journal-title":"Chemosphere"},{"key":"2021121004471456300_cit21","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1002\/yea.2921","article-title":"Yarrowia lipolytica","volume":"29","author":"Nicaud","year":"2012","journal-title":"Yeast"},{"key":"2021121004471456300_cit22","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1007\/978-3-319-06437-6_2","article-title":"Yarrowia lipolytica in biotechnological applications","volume-title":"Biotechnological Application of the Yeast Yarrowia lipolytica","author":"Harzevili","year":"2014"},{"key":"2021121004471456300_cit23","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1016\/j.plipres.2015.12.001","article-title":"Yarrowia lipolytica as a biotechnological chassis to produce usual and unusual fatty acids","volume":"61","author":"Ledesma-Amaro","year":"2016","journal-title":"Prog. Lipid Res."},{"key":"2021121004471456300_cit24","doi-asserted-by":"crossref","first-page":"2150","DOI":"10.1016\/j.biotechadv.2018.10.004","article-title":"Synthetic biology tools for engineering Yarrowia lipolytica","volume":"36","author":"Larroude","year":"2018","journal-title":"Biotechnol. Adv."},{"key":"2021121004471456300_cit25","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1159\/000060349","article-title":"Yarrowia lipolytica: an organism amenable to genetic manipulation as a model for analysing dimorphism in fungi","volume":"5","author":"Dominguez","year":"2000","journal-title":"Contrib. Microbiol."},{"key":"2021121004471456300_cit26","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1007\/s00203-002-0478-3","article-title":"Different effectors of dimorphism in Yarrowia lipolytica","volume":"178","author":"Ruiz-Herrera","year":"2002","journal-title":"Arch. 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Lett."},{"key":"2021121004471456300_cit29","doi-asserted-by":"crossref","first-page":"617","DOI":"10.1007\/s00792-018-1022-y","article-title":"Heavy metal tolerance in marine strains of Yarrowia lipolytica","volume":"22","author":"Bankar","year":"2018","journal-title":"Extremophiles"},{"key":"2021121004471456300_cit30","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1016\/S0079-6603(03)01014-6","article-title":"The yeast and plant plasma membrane H+ pump ATPase: divergent regulation for the same function","volume":"74","author":"Lefebvre","year":"2003","journal-title":"Prog. Nucleic Acid Res."},{"key":"2021121004471456300_cit31","doi-asserted-by":"crossref","first-page":"3230","DOI":"10.1016\/j.molp.2015.11.002","article-title":"Plasma membrane H(+)-ATPase regulation in the center of plant physiology","volume":"9","author":"Falhof","year":"2016","journal-title":"Mol. 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Rev Microbiol."},{"key":"2021121004471456300_cit40","volume-title":"Wisconsin procedures for soil testing, plant analysis and feed e forage analysis: plant analysis","author":"Peters","year":"2005"},{"key":"2021121004471456300_cit41","doi-asserted-by":"crossref","first-page":"bio029660","DOI":"10.1242\/bio.029660","article-title":"Spermine modulates fungal morphogenesis and activates plasma membrane H+-ATPase during yeast to hyphae transition","volume":"7","author":"Cogo","year":"2018","journal-title":"Biol. Open"},{"key":"2021121004471456300_cit42","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1016\/0003-2697(76)90527-3","article-title":"Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding","volume":"72","author":"Bradford","year":"1976","journal-title":"Anal. 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