title: Enterococcus faecalis Uses a Phosphotransferase System Permease and a Host Colonization-Related ABC Transporter for Maltodextrin Uptake.
abstract: Maltodextrin 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 theEnterococcus faecalismaltodextrin 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. faecalistakes 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. AmalTmutant therefore exhibits significantly reduced growth on maltose and maltotriose. The residual uptake of the trisaccharide is catalyzed by the ABC transporter, because amalT mdxFdouble mutant no longer grows on maltotriose. The trisaccharide arrives as maltotriose-6″-P in the cell. MapP, which dephosphorylates maltose-6'-P, also releases Pifrom 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. faecalisalso 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 ofE. faecalis, because inactivation ofmdxFsignificantly reduced enterococcal colonization and/or survival in kidneys and liver of mice after intraperitoneal infection.IMPORTANCEInfections 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 inEnterococcus faecalisand linked to its virulence. Our results demonstrate thatE. faecaliscan 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.
authors.affiliation: Normandy University, UNICAEN, U2RM Stress/Virulence, Caen, France.
authors.forename: Nicolas
authors.initials: N
authors.lastname: Sauvageot
authors.affiliation: Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay, Jouy-en-Josas, France.|Department of Biology, 8 May 1945 University, Guelma, Algeria.
authors.forename: Abdelhamid
authors.initials: A
authors.lastname: Mokhtari
authors.affiliation: Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay, Jouy-en-Josas, France.
authors.forename: Philippe
authors.initials: P
authors.lastname: Joyet
authors.affiliation: Normandy University, UNICAEN, U2RM Stress/Virulence, Caen, France.
authors.forename: Aurélie
authors.initials: A
authors.lastname: Budin-Verneuil
authors.affiliation: Instituto de Biología Molecular y Celular de Rosario (IBR-CONICET), Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario, Rosario, Argentina.
authors.forename: Víctor S
authors.initials: VS
authors.lastname: Blancato
authors.affiliation: Instituto de Biología Molecular y Celular de Rosario (IBR-CONICET), Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario, Rosario, Argentina.
authors.forename: Guillermo D
authors.initials: GD
authors.lastname: Repizo
authors.affiliation: Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay, Jouy-en-Josas, France.
authors.forename: Céline
authors.initials: C
authors.lastname: Henry
authors.affiliation: Center for Drug Evaluation and Research, Food and Drug Administration, Silver Spring, Maryland, USA.|Microbial Biochemistry and Genetics Unit, Laboratory of Cell and Developmental Biology, NIDCR, National Institutes of Health, Bethesda, Maryland, USA.
authors.forename: Andreas
authors.initials: A
authors.lastname: Pikis
authors.affiliation: Microbial Biochemistry and Genetics Unit, Laboratory of Cell and Developmental Biology, NIDCR, National Institutes of Health, Bethesda, Maryland, USA.
authors.forename: John
authors.initials: J
authors.lastname: Thompson
authors.affiliation: Instituto de Biología Molecular y Celular de Rosario (IBR-CONICET), Facultad de Ciencias Bioquímicas y Farmacéuticas, Universidad Nacional de Rosario, Rosario, Argentina.
authors.forename: Christian
authors.initials: C
authors.lastname: Magni
authors.affiliation: Normandy University, UNICAEN, U2RM Stress/Virulence, Caen, France axel.hartke@unicaen.fr Josef.Deutscher@grignon.inra.fr.
authors.forename: Axel
authors.initials: A
authors.lastname: Hartke
authors.affiliation: Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay, Jouy-en-Josas, France axel.hartke@unicaen.fr Josef.Deutscher@grignon.inra.fr.|Centre National de la Recherche Scientifique, UMR8261 (affiliated with the Université Paris Diderot, Sorbonne Paris Cité), Expression Génétique Microbienne, Institut de Biologie Physico-Chimique, Paris, France.
authors.forename: Josef
authors.initials: J
authors.lastname: Deutscher
mesh_terms: D018528:ATP-Binding Cassette Transporters / Q000235:genetics / Q000378:metabolism*; D000818:Animals; D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism; D001692:Biological Transport; D013293:Enterococcus faecalis / Q000201:enzymology* / Q000235:genetics / Q000254:growth & development / Q000378:metabolism*; D007668:Kidney / Q000382:microbiology; D008099:Liver / Q000382:microbiology; D008320:Maltose / Q000494:pharmacology; D026901:Membrane Transport Proteins / Q000235:genetics; D051379:Mice; D009154:Mutation; D009844:Oligosaccharides / Q000378:metabolism; D010731:Phosphoenolpyruvate Sugar Phosphotransferase System / Q000235:genetics / Q000378:metabolism*; D011134:Polysaccharides / Q000378:metabolism*; D014312:Trisaccharides / Q000494:pharmacology
chemical_list: D018528:ATP-Binding Cassette Transporters; D001426:Bacterial Proteins; D026901:Membrane Transport Proteins; D009844:Oligosaccharides; D011134:Polysaccharides; D014312:Trisaccharides; C021705:maltooligosaccharides; C008317:maltotriose; D008320:Maltose; C008315:maltodextrin; D010731:Phosphoenolpyruvate Sugar Phosphotransferase System
keywords: ABC transporter; enterococci; host colonization; maltodextrin; phosphotransferase system