Literature DB >> 28242718

Enterococcus faecalis Uses a Phosphotransferase System Permease and a Host Colonization-Related ABC Transporter for Maltodextrin Uptake.

Nicolas Sauvageot1, Abdelhamid Mokhtari2,3, Philippe Joyet2, Aurélie Budin-Verneuil1, Víctor S Blancato4, Guillermo D Repizo4, Céline Henry2, Andreas Pikis5,6, John Thompson6, Christian Magni4, Axel Hartke7, Josef Deutscher8,9.   

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 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.
Copyright © 2017 American Society for Microbiology.

Entities:  

Keywords:  ABC transporter; enterococci; host colonization; maltodextrin; phosphotransferase system

Mesh:

Substances:

Year:  2017        PMID: 28242718      PMCID: PMC5388810          DOI: 10.1128/JB.00878-16

Source DB:  PubMed          Journal:  J Bacteriol        ISSN: 0021-9193            Impact factor:   3.490


  40 in total

1.  Pattern of action of Bacillus stearothermophilus neopullulanase on pullulan.

Authors:  T Imanaka; T Kuriki
Journal:  J Bacteriol       Date:  1989-01       Impact factor: 3.490

2.  Phosphoenolpyruvate-dependent protein kinase enzyme I of Streptococcus faecalis: purification and properties of the enzyme and characterization of its active center.

Authors:  C A Alpert; R Frank; K Stüber; J Deutscher; W Hengstenberg
Journal:  Biochemistry       Date:  1985-02-12       Impact factor: 3.162

3.  Cloning and characterization of a gene encoding a cold-shock protein in Lactobacillus casei.

Authors:  Nicolas Sauvageot; Sophie Beaufils; Alain Mazé; Josef Deutscher; Axel Hartke
Journal:  FEMS Microbiol Lett       Date:  2006-01       Impact factor: 2.742

4.  A multitask ATPase serving different ABC-type sugar importers in Bacillus subtilis.

Authors:  Mário José Ferreira; Isabel de Sá-Nogueira
Journal:  J Bacteriol       Date:  2010-08-06       Impact factor: 3.490

5.  Metabolism of polysaccharides by the Streptococcus mutants dexB gene product.

Authors:  G C Whiting; I C Sutcliffe; R R Russell
Journal:  J Gen Microbiol       Date:  1993-09

6.  Molecular characterization of group A Streptococcus maltodextrin catabolism and its role in pharyngitis.

Authors:  Samuel A Shelburne; David B Keith; Michael T Davenport; Nicola Horstmann; Richard G Brennan; James M Musser
Journal:  Mol Microbiol       Date:  2008-07       Impact factor: 3.501

7.  The Intraperitoneal Transcriptome of the Opportunistic Pathogen Enterococcus faecalis in Mice.

Authors:  Cécile Muller; Margherita Cacaci; Nicolas Sauvageot; Maurizio Sanguinetti; Thomas Rattei; Thomas Eder; Jean-Christophe Giard; Jörn Kalinowski; Torsten Hain; Axel Hartke
Journal:  PLoS One       Date:  2015-05-15       Impact factor: 3.240

8.  Pheromone killing of multidrug-resistant Enterococcus faecalis V583 by native commensal strains.

Authors:  Michael S Gilmore; Marcus Rauch; Matthew M Ramsey; Paul R Himes; Sriram Varahan; Janet M Manson; Francois Lebreton; Lynn Ernest Hancock
Journal:  Proc Natl Acad Sci U S A       Date:  2015-05-26       Impact factor: 11.205

Review 9.  Molecular mechanism of the Escherichia coli maltose transporter.

Authors:  Jue Chen
Journal:  Curr Opin Struct Biol       Date:  2013-04-27       Impact factor: 6.809

10.  Carbohydrate availability regulates virulence gene expression in Streptococcus suis.

Authors:  M Laura Ferrando; Peter van Baarlen; Germano Orrù; Rosaria Piga; Roger S Bongers; Michiel Wels; Astrid De Greeff; Hilde E Smith; Jerry M Wells
Journal:  PLoS One       Date:  2014-03-18       Impact factor: 3.240

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  6 in total

1.  Enterococcus faecalis Maltodextrin Gene Regulation by Combined Action of Maltose Gene Regulator MalR and Pleiotropic Regulator CcpA.

Authors:  Maxime Grand; Eliette Riboulet-Bisson; Josef Deutscher; Axel Hartke; Nicolas Sauvageot
Journal:  Appl Environ Microbiol       Date:  2020-09-01       Impact factor: 4.792

2.  Enzymes Required for Maltodextrin Catabolism in Enterococcus faecalis Exhibit Novel Activities.

Authors:  Philippe Joyet; Abdelhamid Mokhtari; Eliette Riboulet-Bisson; Víctor S Blancato; Martin Espariz; Christian Magni; Axel Hartke; Josef Deutscher; Nicolas Sauvageot
Journal:  Appl Environ Microbiol       Date:  2017-06-16       Impact factor: 4.792

Review 3.  The Enterococcus: a Model of Adaptability to Its Environment.

Authors:  Mónica García-Solache; Louis B Rice
Journal:  Clin Microbiol Rev       Date:  2019-01-30       Impact factor: 26.132

4.  Exploratory Analysis of the Microbiological Potential for Efficient Utilization of Fiber Between Lantang and Duroc Pigs.

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Journal:  Front Microbiol       Date:  2018-06-22       Impact factor: 5.640

5.  The Role of Fur in the Transcriptional and Iron Homeostatic Response of Enterococcus faecalis.

Authors:  Mauricio Latorre; Daniela Quenti; Dante Travisany; Kavindra V Singh; Barbara E Murray; Alejandro Maass; Verónica Cambiazo
Journal:  Front Microbiol       Date:  2018-07-17       Impact factor: 5.640

Review 6.  Multidrug Resistance (MDR) and Collateral Sensitivity in Bacteria, with Special Attention to Genetic and Evolutionary Aspects and to the Perspectives of Antimicrobial Peptides-A Review.

Authors:  András Fodor; Birhan Addisie Abate; Péter Deák; László Fodor; Ervin Gyenge; Michael G Klein; Zsuzsanna Koncz; Josephat Muvevi; László Ötvös; Gyöngyi Székely; Dávid Vozik; László Makrai
Journal:  Pathogens       Date:  2020-06-29
  6 in total

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