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Manganese ions serve as cofactors to three mitochondrial enzymes: superoxide dismutase (Sod2), arginase and glutamine synthase, and to glycosyltransferases residing in the Golgi. In Drosophila melanogaster, manganese has also been implicated in the formation of ceramide phosphoethanolamine, the insect's sphingomyelin analogue, a structural component of cellular membranes. Manganese overload leads to neurodegeneration and toxicity in both humans and Drosophila. Here, we report specific absorption and accumulation of manganese during the first week of adulthood in flies, which correlates with an increase in Sod2 activity during the same period. To test the requirement of dietary manganese for this accumulation, we generated a Drosophila model of manganese deficiency. Due to the lack of manganese-specific chelators, we used chemically defined media to grow the flies and deplete them of the metal. Dietary manganese depletion reduced Sod2 activity. We then examined gene and protein expression changes in the intestines of manganese depleted flies. We found adaptive responses to the presumed loss of known manganese-dependent enzymatic activities: less glutamine synthase activity (amination of glutamate to glutamine) was compensated by 50% reduction in glutaminase (deamination of glutamine to glutamate); less glycosyltransferase activity, predicted to reduce protein glycosylation, was compensated by 30% reduction in lysosomal mannosidases (protein deglycosylating enzymes); less ceramide phosphoethanolamine synthase activity was compensated by 30% reduction in the Drosophila sphingomyeline phospodiesterase, which could catabolize ceramide phosphoethanolamine in flies. Reduced Sod2 activity, predicted to cause superoxide-dependent iron\u2013sulphur cluster damage, resulted in cellular iron misregulation.<\/jats:p>","DOI":"10.1039\/c9mt00218a","type":"journal-article","created":{"date-parts":[[2019,11,26]],"date-time":"2019-11-26T13:03:39Z","timestamp":1574773419000},"page":"218-240","update-policy":"https:\/\/doi.org\/10.1039\/rsc_crossmark_policy","source":"Crossref","is-referenced-by-count":23,"title":["Intestinal response to dietary manganese depletion in <i>Drosophila<\/i>"],"prefix":"10.1093","volume":"12","author":[{"given":"Johana","family":"V\u00e1squez-Procopio","sequence":"first","affiliation":[{"name":"Departamento de Fisiolog\u00eda, Biof\u00edsica y Neurociencias, Centro de Investigaci\u00f3n y de Estudios Avanzados, Av. IPN 2508, Mexico City, 07360, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Beatriz","family":"Osorio","sequence":"additional","affiliation":[{"name":"Departamento de Fisiolog\u00eda, Biof\u00edsica y Neurociencias, Centro de Investigaci\u00f3n y de Estudios Avanzados, Av. IPN 2508, Mexico City, 07360, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Leticia","family":"Cort\u00e9s-Mart\u00ednez","sequence":"additional","affiliation":[{"name":"Departamento de Infect\u00f3mica y Patog\u00e9nesis Molecular, Centro de Investigaci\u00f3n y de Estudios Avanzados, Av. IPN 2508, Mexico City, 07360, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7276-7513","authenticated-orcid":false,"given":"Fidel","family":"Hern\u00e1ndez-Hern\u00e1ndez","sequence":"additional","affiliation":[{"name":"Departamento de Infect\u00f3mica y Patog\u00e9nesis Molecular, Centro de Investigaci\u00f3n y de Estudios Avanzados, Av. IPN 2508, Mexico City, 07360, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4432-7780","authenticated-orcid":false,"given":"Oscar","family":"Medina-Contreras","sequence":"additional","affiliation":[{"name":"Laboratorio de Investigaci\u00f3n en Inmunolog\u00eda y Prote\u00f3mica, Hospital Infantil de M\u00e9xico Federico G\u00f3mez, Dr M\u00e1rquez 162, Mexico City, 06720, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7671-7943","authenticated-orcid":false,"given":"Emmanuel","family":"R\u00edos-Castro","sequence":"additional","affiliation":[{"name":"Unidad de Gen\u00f3mica, Prote\u00f3mica y Metabol\u00f3mica, LaNSE, Centro de Investigaci\u00f3n y de Estudios Avanzados, Av. IPN 2508, Mexico City, 07360, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aram","family":"Comjean","sequence":"additional","affiliation":[{"name":"Department of Genetics, Harvard Medical School, Boston, Massachusetts 02115, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fangge","family":"Li","sequence":"additional","affiliation":[{"name":"Department of Genetics, Harvard Medical School, Boston, Massachusetts 02115, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yanhui","family":"Hu","sequence":"additional","affiliation":[{"name":"Department of Genetics, Harvard Medical School, Boston, Massachusetts 02115, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9639-7708","authenticated-orcid":false,"given":"Stephanie","family":"Mohr","sequence":"additional","affiliation":[{"name":"Department of Genetics, Harvard Medical School, Boston, Massachusetts 02115, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Norbert","family":"Perrimon","sequence":"additional","affiliation":[{"name":"Department of Genetics, Harvard Medical School, Boston, Massachusetts 02115, USA"},{"name":"Howard Hughes Medical Institute, Boston, Massachusetts 02115, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0467-8444","authenticated-orcid":false,"given":"Fanis","family":"Missirlis","sequence":"additional","affiliation":[{"name":"Departamento de Fisiolog\u00eda, Biof\u00edsica y Neurociencias, Centro de Investigaci\u00f3n y de Estudios Avanzados, Av. IPN 2508, Mexico City, 07360, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2019,11,26]]},"reference":[{"key":"2021121004323956300_cit1","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1002\/biof.5520100102","article-title":"Manganese deficiency and toxicity: are high or low dietary amounts of manganese cause for concern?","volume":"10","author":"Finley","year":"1999","journal-title":"BioFactors"},{"key":"2021121004323956300_cit2","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1146\/annurev-nutr-071714-034419","article-title":"Manganese Is Essential for Neuronal Health","volume":"35","author":"Horning","year":"2015","journal-title":"Annu. Rev. Nutr."},{"key":"2021121004323956300_cit3","doi-asserted-by":"crossref","first-page":"6176","DOI":"10.1016\/S0021-9258(18)62675-4","article-title":"Superoxide dismutase from escherichia coli B. A new manganese-containing enzyme","volume":"245","author":"Keele Jr.","year":"1970","journal-title":"J. Biol. Chem."},{"key":"2021121004323956300_cit4","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1016\/S0021-9258(18)62504-9","article-title":"Nuclear magnetic resonance studies of manganese binding of rat liver arginase","volume":"246","author":"Hirsch-Kolb","year":"1971","journal-title":"J. Biol. Chem."},{"key":"2021121004323956300_cit5","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1016\/j.jmb.2007.10.029","article-title":"Crystal structures of mammalian glutamine synthetases illustrate substrate-induced conformational changes and provide opportunities for drug and herbicide design","volume":"375","author":"Krajewski","year":"2008","journal-title":"J. Mol. Biol."},{"key":"2021121004323956300_cit6","doi-asserted-by":"crossref","first-page":"3977","DOI":"10.1016\/S0021-9258(18)62129-5","article-title":"Studies on galactosyltransferase. Kinetic investigations with N-acetylglucosamine as the galactosyl group acceptor","volume":"246","author":"Morrison","year":"1971","journal-title":"J. Biol. Chem."},{"key":"2021121004323956300_cit7","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1080\/07391102.2003.10506900","article-title":"Comparison of the closed conformation of the beta 1,4-galactosyltransferase-1 (beta 4Gal-T1) in the presence and absence of alpha-lactalbumin (LA)","volume":"21","author":"Ramakrishnan","year":"2003","journal-title":"J. Biomol. Struct. Dyn."},{"key":"2021121004323956300_cit8","doi-asserted-by":"crossref","first-page":"6148","DOI":"10.1021\/acs.jpcb.7b03714","article-title":"First-Principles Interaction Analysis Assessment of the Manganese Cation in the Catalytic Activity of Glycosyltransferases","volume":"121","author":"Sladek","year":"2017","journal-title":"J. Phys. Chem. B"},{"key":"2021121004323956300_cit9","doi-asserted-by":"crossref","first-page":"11520","DOI":"10.1074\/jbc.M113.460972","article-title":"Ceramide phosphoethanolamine biosynthesis in Drosophila is mediated by a unique ethanolamine phosphotransferase in the Golgi lumen","volume":"288","author":"Vacaru","year":"2013","journal-title":"J. Biol. Chem."},{"key":"2021121004323956300_cit10","doi-asserted-by":"crossref","first-page":"1284","DOI":"10.1016\/j.bbamem.2019.05.001","article-title":"Ceramide phosphoethanolamine, an enigmatic cellular membrane sphingolipid, Biochimica et biophysica acta","volume":"1861","author":"Panevska","year":"2019","journal-title":"Biomembranes"},{"key":"2021121004323956300_cit11","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1016\/S0021-9258(18)70986-1","article-title":"The partition of manganese among organs and intracellular organelles of the rat","volume":"214","author":"Maynard","year":"1955","journal-title":"J. Biol. Chem."},{"key":"2021121004323956300_cit12","doi-asserted-by":"crossref","first-page":"2498","DOI":"10.1093\/jn\/113.12.2498","article-title":"Superoxide dismutase activity and lipid peroxidation in the rat: developmental correlations affected by manganese deficiency","volume":"113","author":"Zidenberg-Cherr","year":"1983","journal-title":"J. Nutr."},{"key":"2021121004323956300_cit13","doi-asserted-by":"crossref","first-page":"340","DOI":"10.1093\/jn\/124.3.340","article-title":"Dietary manganese deficiency decreases rat hepatic arginase activity","volume":"124","author":"Brock","year":"1994","journal-title":"J. Nutr."},{"key":"2021121004323956300_cit14","doi-asserted-by":"crossref","first-page":"1140","DOI":"10.1039\/C8MT00348C","article-title":"Manganese influx and expression of ZIP8 is essential in primary myoblasts and contributes to activation of SOD2","volume":"11","author":"Gordon","year":"2019","journal-title":"Metallomics"},{"key":"2021121004323956300_cit15","doi-asserted-by":"crossref","first-page":"47556","DOI":"10.1074\/jbc.M108923200","article-title":"Manganese superoxide dismutase in Saccharomyces cerevisiae acquires its metal co-factor through a pathway involving the Nramp metal transporter, Smf2p","volume":"276","author":"Luk","year":"2001","journal-title":"J. Biol. Chem."},{"key":"2021121004323956300_cit16","doi-asserted-by":"crossref","first-page":"10353","DOI":"10.1073\/pnas.1632471100","article-title":"Manganese activation of superoxide dismutase 2 in Saccharomyces cerevisiae requires MTM1, a member of the mitochondrial carrier family","volume":"100","author":"Luk","year":"2003","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"2021121004323956300_cit17","doi-asserted-by":"crossref","first-page":"22715","DOI":"10.1074\/jbc.M504257200","article-title":"Manganese activation of superoxide dismutase 2 in the mitochondria of Saccharomyces cerevisiae","volume":"280","author":"Luk","year":"2005","journal-title":"J. Biol. Chem."},{"key":"2021121004323956300_cit18","doi-asserted-by":"crossref","first-page":"1775","DOI":"10.1038\/sj.emboj.7601064","article-title":"The effects of mitochondrial iron homeostasis on cofactor specificity of superoxide dismutase 2","volume":"25","author":"Yang","year":"2006","journal-title":"EMBO J."},{"key":"2021121004323956300_cit19","doi-asserted-by":"crossref","first-page":"12227","DOI":"10.1074\/jbc.M511649200","article-title":"Manganese is the link between frataxin and iron-sulfur deficiency in the yeast model of Friedreich ataxia","volume":"281","author":"Irazusta","year":"2006","journal-title":"J. Biol. Chem."},{"key":"2021121004323956300_cit20","doi-asserted-by":"crossref","first-page":"22633","DOI":"10.1074\/jbc.M109.026773","article-title":"The interaction of mitochondrial iron with manganese superoxide dismutase","volume":"284","author":"Naranuntarat","year":"2009","journal-title":"J. Biol. Chem."},{"key":"2021121004323956300_cit21","doi-asserted-by":"crossref","first-page":"1914","DOI":"10.1523\/JNEUROSCI.3432-15.2016","article-title":"Shawn, the Drosophila Homolog of SLC25A39\/40, Is a Mitochondrial Carrier That Promotes Neuronal Survival","volume":"36","author":"Slabbaert","year":"2016","journal-title":"J. Neurosci."},{"key":"2021121004323956300_cit22","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1016\/j.cmet.2009.06.012","article-title":"Discovery of genes essential for heme biosynthesis through large-scale gene expression analysis","volume":"10","author":"Nilsson","year":"2009","journal-title":"Cell Metab."},{"key":"2021121004323956300_cit23","doi-asserted-by":"crossref","first-page":"50","DOI":"10.3389\/fphys.2018.00050","article-title":"Iron Sulfur and Molybdenum Cofactor Enzymes Regulate the Drosophila Life Cycle by Controlling Cell Metabolism","volume":"9","author":"Marelja","year":"2018","journal-title":"Front. Physiol."},{"key":"2021121004323956300_cit24","doi-asserted-by":"crossref","first-page":"656","DOI":"10.1039\/c3mt00041a","article-title":"Insights into the iron-ome and manganese-ome of Deltamtm1 Saccharomyces cerevisiae mitochondria","volume":"5","author":"Park","year":"2013","journal-title":"Metallomics"},{"key":"2021121004323956300_cit25","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1007\/s40572-017-0136-1","article-title":"Relationships Between Essential Manganese Biology and Manganese Toxicity in Neurological Disease","volume":"4","author":"Pfalzer","year":"2017","journal-title":"Curr. Environ. Health Rep."},{"key":"2021121004323956300_cit26","doi-asserted-by":"crossref","first-page":"828","DOI":"10.1038\/201828a0","article-title":"Primordial Homeostasis in a Mammal as Shown by the Control of Manganese","volume":"201","author":"Cotzias","year":"1964","journal-title":"Nature"},{"key":"2021121004323956300_cit27","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1212\/WNL.17.2.128","article-title":"Chronic manganese poisoning. Clinical picture and manganese turnover","volume":"17","author":"Mena","year":"1967","journal-title":"Neurology"},{"key":"2021121004323956300_cit28","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1007\/978-3-319-60189-2_2","article-title":"Manganese and Developmental Neurotoxicity","volume":"18","author":"Lucchini","year":"2017","journal-title":"Adv. Neurobiol."},{"key":"2021121004323956300_cit29","doi-asserted-by":"crossref","first-page":"811","DOI":"10.1007\/s10534-011-9454-1","article-title":"Manganese accumulation in the CNS and associated pathologies","volume":"24","author":"Rivera-Mancia","year":"2011","journal-title":"Biometals"},{"key":"2021121004323956300_cit30","first-page":"405","article-title":"Contribution of experimental manganese encephalopathy to neurology and neuropathology","volume":"27","author":"Pentschew","year":"1964","journal-title":"Rev. Neuro-Psiquiatr."},{"key":"2021121004323956300_cit31","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1016\/0013-9351(78)90075-0","article-title":"Manganese encephalopathy in growing rats","volume":"15","author":"Chandra","year":"1978","journal-title":"Environ. Res."},{"key":"2021121004323956300_cit32","first-page":"75","article-title":"Alterations in brain dopamine and GABA following inorganic or organic manganese administration","volume":"3","author":"Gianutsos","year":"1982","journal-title":"Neurotoxicology"},{"key":"2021121004323956300_cit33","doi-asserted-by":"crossref","first-page":"1045","DOI":"10.1007\/s10534-011-9463-0","article-title":"Acute and chronic metal exposure impairs locomotion activity in Drosophila melanogaster: a model to study Parkinsonism","volume":"24","author":"Bonilla-Ramirez","year":"2011","journal-title":"Biometals"},{"key":"2021121004323956300_cit34","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1016\/j.tox.2012.01.016","article-title":"Minocycline increases the life span and motor activity and decreases lipid peroxidation in manganese treated Drosophila melanogaster","volume":"294","author":"Bonilla","year":"2012","journal-title":"Toxicology"},{"key":"2021121004323956300_cit35","doi-asserted-by":"crossref","first-page":"70","DOI":"10.3389\/fgene.2018.00070","article-title":"The Impact of Environmental Mn Exposure on Insect Biology","volume":"9","author":"Ben-Shahar","year":"2018","journal-title":"Front. Genet."},{"key":"2021121004323956300_cit36","doi-asserted-by":"crossref","first-page":"35758","DOI":"10.1074\/jbc.M109.051409","article-title":"The divalent metal transporter homologues SMF-1\/2 mediate dopamine neuron sensitivity in caenorhabditis elegans models of manganism and parkinson disease","volume":"284","author":"Settivari","year":"2009","journal-title":"J. Biol. Chem."},{"key":"2021121004323956300_cit37","doi-asserted-by":"crossref","first-page":"e1001084","DOI":"10.1371\/journal.pgen.1001084","article-title":"Extracellular dopamine potentiates mn-induced oxidative stress, lifespan reduction, and dopaminergic neurodegeneration in a BLI-3-dependent manner in Caenorhabditis elegans","volume":"6","author":"Benedetto","year":"2010","journal-title":"PLoS Genet."},{"key":"2021121004323956300_cit38","doi-asserted-by":"crossref","first-page":"1816","DOI":"10.1039\/C4MT00168K","article-title":"Manganese disturbs metal and protein homeostasis in Caenorhabditis elegans","volume":"6","author":"Angeli","year":"2014","journal-title":"Metallomics"},{"key":"2021121004323956300_cit39","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1016\/j.ajhg.2012.01.017","article-title":"Mutations in SLC30A10 cause parkinsonism and dystonia with hypermanganesemia, polycythemia, and chronic liver disease","volume":"90","author":"Quadri","year":"2012","journal-title":"Am. J. Hum. Genet."},{"key":"2021121004323956300_cit40","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1016\/j.ajhg.2012.01.018","article-title":"Syndrome of hepatic cirrhosis, dystonia, polycythemia, and hypermanganesemia caused by mutations in SLC30A10, a manganese transporter in man","volume":"90","author":"Tuschl","year":"2012","journal-title":"Am. J. Hum. Genet."},{"key":"2021121004323956300_cit41","doi-asserted-by":"crossref","first-page":"894","DOI":"10.1016\/j.ajhg.2015.11.003","article-title":"SLC39A8 Deficiency: A Disorder of Manganese Transport and Glycosylation","volume":"97","author":"Park","year":"2015","journal-title":"Am. J. Hum. Genet."},{"key":"2021121004323956300_cit42","doi-asserted-by":"crossref","first-page":"11601","DOI":"10.1038\/ncomms11601","article-title":"Mutations in SLC39A14 disrupt manganese homeostasis and cause childhood-onset parkinsonism-dystonia","volume":"7","author":"Tuschl","year":"2016","journal-title":"Nat. Commun."},{"key":"2021121004323956300_cit43","doi-asserted-by":"crossref","first-page":"E1769","DOI":"10.1073\/pnas.1720739115","article-title":"SLC39A14 deficiency alters manganese homeostasis and excretion resulting in brain manganese accumulation and motor deficits in mice","volume":"115","author":"Jenkitkasemwong","year":"2018","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"2021121004323956300_cit44","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1007\/s11910-019-0942-y","article-title":"Genetic Disorders of Manganese Metabolism","volume":"19","author":"Anagianni","year":"2019","journal-title":"Curr. Neurol. Neurosci."},{"key":"2021121004323956300_cit45","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1242\/jeb.201.1.115","article-title":"Metal ions suppress the abnormal taste behavior of the Drosophila mutant malvolio","volume":"201","author":"Orgad","year":"1998","journal-title":"J. Exp. 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