Enterococcus faecalis uses a phosphotransferase system permease and a host colonization-related ABC transporter for maltodextrin uptake

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dc.citation.titleJournal of Bacteriology
dc.citation.volume199
dc.contributor.otherFernández, María: provide plasmid pAGEnt
dc.creatorSauvageot, Nicolas
dc.creatorMokhtari, Abdelhamid
dc.creatorJoyet, Philippe
dc.creatorBudin Verneuil, Aurélie
dc.creatorBlancato, Víctor Sebastián
dc.creatorRepizo, Guillermo Daniel
dc.creatorHenry, Céline
dc.creatorPikis, Andreas
dc.creatorThompson, John
dc.creatorMagni, Christian
dc.creatorHartke, Axel
dc.creatorDeutscher, Josef
dc.date.accessioned2024-11-26T11:56:31Z
dc.date.available2024-11-26T11:56:31Z
dc.date.issued2017-04-11
dc.description.abstractMaltodextrin is a mixture of maltooligosaccharides, which are produced by the degradation of starch or glycogen. They are mostly composed of α-1,4- and some α-1,6-linked glucose residues. Genes presumed to code for the Enterococcus faecalis maltodextrin transporter were induced during enterococcal infection. We therefore carried out a detailed study of maltodextrin transport in this organism. Depending on their length (3 to 7 glucose residues), E. faecalis takes up maltodextrins either via MalT, a maltose-specific permease of the phosphoenolpyruvate (PEP):carbohydrate phosphotransferase system (PTS), or the ATP binding cassette (ABC) transporter MdxEFG-MsmX. Maltotriose, the smallest maltodextrin, is primarily transported by the PTS permease. A malT mutant therefore exhibits significantly reduced growth on maltose and maltotriose. The residual uptake of the trisaccharide is catalyzed by the ABC transporter, because a malT mdxF double mutant no longer grows on maltotriose. The trisaccharide arrives as maltotriose-6″-P in the cell. MapP, which dephosphorylates maltose-6′-P, also releases Pi from maltotriose-6″-P. Maltotetraose and longer maltodextrins are mainly (or exclusively) taken up via the ABC transporter, because inactivation of the membrane protein MdxF prevents growth on maltotetraose and longer maltodextrins up to at least maltoheptaose. E. faecalis also utilizes panose and isopanose, and we show for the first time, to our knowledge, that in contrast to maltotriose, its two isomers are primarily transported via the ABC transporter. We confirm that maltodextrin utilization via MdxEFG-MsmX affects the colonization capacity of E. faecalis, because inactivation of mdxF significantly reduced enterococcal colonization and/or survival in kidneys and liver of mice after intraperitoneal infection. IMPORTANCE: Infections by enterococci, which are major health care-associated pathogens, are difficult to treat due to their increasing resistance to clinically relevant antibiotics, and new strategies are urgently needed. A largely unexplored aspect is how these pathogens proliferate and which substrates they use in order to grow inside infected hosts. The use of maltodextrins as a source of carbon and energy was studied in Enterococcus faecalis and linked to its virulence. Our results demonstrate that E. faecalis can efficiently use glycogen degradation products. We show here that depending on the length of the maltodextrins, one of two different transporters is used: the maltose-PTS transporter MalT, or the MdxEFG-MsmX ABC transporter. MdxEFG-MsmX takes up longer maltodextrins as well as complex molecules, such as panose and isopanose.
dc.description.filFil: Sauvageot, Nicolas. Université de Caen Normandie. Institut de Biologie Fondamentale et Appliquée (IBFA). L’équipe Stress-Virulence de l’Unité de Recherche Risques Microbiens (U2RM); France.
dc.description.filFil: Mokhtari, Abdelhamid. Université Paris-Saclay. AgroParisTech; France.
dc.description.filFil: Mokhtari, Abdelhamid. Institut National de la Recherche Agronomique (INRA); France.
dc.description.filFil: Mokhtari, Abdelhamid. Institut Micalis; France.
dc.description.filFil: Mokhtari, Abdelhamid. Université 8 Mai 1945 Guelma. Faculty of Nature and Life and Earth Sciences and the Universes. Department of Biology; Algeria.
dc.description.filFil: Joyet, Philippe. Université Paris-Saclay. AgroParisTech; France.
dc.description.filFil: Joyet, Philippe. Institut National de la Recherche Agronomique (INRA); France.
dc.description.filFil: Joyet, Philippe. Institut Micalis; France.
dc.description.filFil: Budin Verneuil, Aurélie. Université de Caen Normandie. Institut de Biologie Fondamentale et Appliquée (IBFA). L’équipe Stress-Virulence de l’Unité de Recherche Risques Microbiens (U2RM); France.
dc.description.filFil: Blancato, Víctor Sebastián. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario (IBR-CONICET); Argentina.
dc.description.filFil: Repizo, Guillermo Daniel. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario (IBR-CONICET); Argentina.
dc.description.filFil: Henry, Céline. Université Paris-Saclay. AgroParisTech; France.
dc.description.filFil: Henry, Céline. Institut National de la Recherche Agronomique (INRA); France.
dc.description.filFil: Henry, Céline. Institut Micalis; France.
dc.description.filFil: Pikis, Andreas. Food and Drug Administration (FDA). Center for Drug Evaluation and Research (CDER); United States.
dc.description.filFil: Pikis, Andreas. National Institute of Health (NIH). National Institute of Dental and Craniofacial Research (NIDCR). Microbial Biochemistry and Genetics Unit; United States.
dc.description.filFil: Pikis, Andreas. National Institute of Health (NIH). National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK). Laboratory of Cellular & Developmental Biology; United States.
dc.description.filFil: Thompson, John. National Institute of Health (NIH). National Institute of Dental and Craniofacial Research (NIDCR). Microbial Biochemistry and Genetics Unit; United States.
dc.description.filFil: Thompson, John. National Institute of Health (NIH). National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK). Laboratory of Cellular & Developmental Biology; United States.
dc.description.filFil: Magni, Christian. Universidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas. Instituto de Biología Molecular y Celular de Rosario (IBR-CONICET); Argentina.
dc.description.filFil: Hartke, Axel. Université de Caen Normandie. Institut de Biologie Fondamentale et Appliquée (IBFA). L’équipe Stress-Virulence de l’Unité de Recherche Risques Microbiens (U2RM); France.
dc.description.filFil: Deutscher, Josef. Université Paris-Saclay. AgroParisTech; France.
dc.description.filFil: Deutscher, Josef. Institut National de la Recherche Agronomique (INRA); France.
dc.description.filFil: Deutscher, Josef. Institut Micalis; France.
dc.description.filFil: Deutscher, Josef. Université Paris Cité. Centre national de la recherche scientifique (CNRS). Institut de Biologie Physico-Chimique (IBPC). Laboratoire de l'Expression Génétique Microbienne (UMR 8261); France.
dc.description.sponsorshipECOS-Sud Argentina-Francia program: action no. A09B03
dc.description.sponsorshipAgencia Nacional de Promoción de la Investigación, el Desarrollo Tecnológico y la Innovación (Agencia I+D+i): contracts 2014-1513 and 2014-3482
dc.description.sponsorshipNational Institutes of Health (NIH). Intramural Research Program of the NIDCR
dc.description.sponsorshipU.S. Department of Health and Human Services (HHS)
dc.description.sponsorshipInitiative d'Excellence program (IdEx): grant DYNAMO, ANR-11-LABX-0011
dc.description.sponsorshipRégion of Normandy
dc.description.sponsorshipEuropean Regional Development Fund (ERDF)
dc.description.sponsorshipAlgerian government fellowship
dc.description.sponsorshipConsejo Nacional de Investigaciones Científicas y Técnicas (CONICET)
dc.description.versionpeerreviewed
dc.format.extent1-17
dc.identifier.citationSauvageot, N., Mokhtari, A., Joyet, P., Budin Verneuil, A., Blancato, V.S., Repizo, G.D., Henry, C., Pikis, A., Thompson, J., Magni, C., Hartke, A. and Deutscher, J. (2017). Enterococcus faecalis uses a phosphotransferase system permease and a host colonization-related ABC transporter for maltodextrin uptake. Journal of Bacteriology, 199(9). https://doi.org/10.1128/jb.00878-16
dc.identifier.e-issn1098-5530
dc.identifier.issn0021-9193
dc.identifier.urihttps://hdl.handle.net/2133/28228
dc.language.isoen
dc.publisherAmerican Society for Microbiology
dc.relation.publisherversionhttps://doi.org/10.1128/jb.00878-16
dc.relation.publisherversionhttps://journals.asm.org/doi/10.1128/jb.00878-16
dc.rightsembargoedAccess
dc.rights.holderSauvageot, Nicolas
dc.rights.holderMokhtari, Abdelhamid
dc.rights.holderJoyet, Philippe
dc.rights.holderBudin Verneuil, Aurélie
dc.rights.holderBlancato, Víctor Sebastián
dc.rights.holderRepizo, Guillermo Daniel
dc.rights.holderHenry, Céline
dc.rights.holderPikis, Andreas
dc.rights.holderThompson, John
dc.rights.holderMagni, Christian
dc.rights.holderHartke, Axel
dc.rights.holderDeutscher, Josef
dc.rights.holderUniversidad Nacional de Rosario. Facultad de Ciencias Bioquímicas y Farmacéuticas
dc.rights.holderAmerican Society for Microbiology
dc.rights.textAttribution-NonCommercial-NoDerivatives 4.0 Internationalen
dc.rights.urihttp://creativecommons.org/licenses/by-nc-nd/4.0/
dc.subjectEnterococci
dc.subjectMaltodextrin
dc.subjectPhosphotransferase system
dc.subjectABC transporter
dc.subjectHost colonization
dc.subjectATP-binding cassette transporters
dc.subjectMembrane transport proteins
dc.subjectEnterococcus faecalis
dc.titleEnterococcus faecalis uses a phosphotransferase system permease and a host colonization-related ABC transporter for maltodextrin uptake
dc.typearticulo
dc.type.versionpublishedVersion

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