Three distinct glycosylation pathways are involved in the decoration of Lactococcus lactis cell wall glycopolymers

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dc.contributor.authorTheodorou, Ilias
dc.contributor.authorCourtin, Pascal
dc.contributor.authorSadovskaya, Irina
dc.contributor.authorPalussière, Simon
dc.contributor.authorFenaille, François
dc.contributor.authorMahony, Jennifer
dc.contributor.authorChapot-Chartier, Marie-Pierre
dc.contributor.authorvan Sinderen, Douwe
dc.contributor.funderScience Foundation Irelanden
dc.date.accessioned2020-03-18T10:44:25Z
dc.date.available2020-03-18T10:44:25Z
dc.date.issued2020-03-13
dc.description.abstractExtra-cytoplasmic sugar decoration of glycopolymer components of the bacterial cell wall contributes to their structural diversity. Typically, the molecular mechanism that underpins such a decoration process involves a three-component glycosylation system (TGS) represented by an undecaprenyl-phosphate (Und-P) sugar-activating glycosyltransferase (Und-P GT), a flippase, and a polytopic glycosyltransferase (PolM GT) dedicated to attaching sugar residues to a specific glycopolymer. Here, using bioinformatic analyses, CRISPR-assisted recombineering, structural analysis of cell wall-associated polysaccharides (CWPS) through Maldi-Tof MS and methylation analysis, we report on three such systems in the bacterium Lactococcus lactis. On the basis of sequence similarities, we first identified three gene pairs, csdAB, csdCD, and csdEF, each encoding an Und-P GT and a PolM GT, as potential TGS component candidates. Our experimental results show that csdAB and csdCD are involved in Glc side chain addition on the CWPS components rhamnan and polysaccharide pellicle (PSP), respectively, whereas csdEF plays a role in galactosylation of lipoteichoic acid (LTA). We also identified a potential flippase encoded in the L. lactis genome (llnz_02975, cflA) and confirmed that it participates in the glycosylation of the three cell wall glycopolymers rhamnan, PSP, and LTA, thus indicating that its function is shared by the three TGSs. Finally, we observed that glucosylation of both rhamnan and PSP can increase resistance to bacteriophage predation and that LTA galactosylation alters L. lactis resistance to bacteriocin.en
dc.description.statusPeer revieweden
dc.description.versionPublished Versionen
dc.format.mimetypeapplication/pdfen
dc.identifier.citationTheodorou, I., Courtin, P., Sadovskaya, I., Palussière, S., Fenaille, F., Mahony, J., Chapot-Chartier, M.P. and van Sinderen, D. (2020) ‘Three distinct glycosylation pathways are involved in the decoration of Lactococcus lactis cell wall glycopolymers’, Journal of Biological Chemistry. doi: 10.1074/jbc.RA119.010844en
dc.identifier.doi10.1074/jbc.RA119.010844en
dc.identifier.eissn1083-351X
dc.identifier.issn0021-9258
dc.identifier.journaltitleJournal of Biological Chemistryen
dc.identifier.urihttps://hdl.handle.net/10468/9769
dc.language.isoenen
dc.publisherAmerican Society for Biochemistry and Molecular Biologyen
dc.relation.projectinfo:eu-repo/grantAgreement/SFI/SFI Investigator Programme/13/IA/1953/IE/Functional analysis of the host adsorption and DNA injection processes of a lactococcal bacteriophage/en
dc.relation.projectinfo:eu-repo/grantAgreement/SFI/SFI Starting Investigator Research Grant (SIRG)/15/SIRG/3430/IE/Phage-host interactome of the dairy bacterium Streptococcus thermophilus (PHIST)/en
dc.rights© 2020, the Authors. Published under license by The American Society for Biochemistry and Molecular Biology, Inc. This is an Open Access article under the CC BY license. This research was originally published in the Journal of Biological Chemistry: Theodorou, I., Courtin, P., Sadovskaya, I., Palussière, S., Fenaille, F., Mahony, J., Chapot-Chartier, M.P. and van Sinderen, D. (2020) ‘Three distinct glycosylation pathways are involved in the decoration of Lactococcus lactis cell wall glycopolymers’, Journal of Biological Chemistry. doi: 10.1074/jbc.RA119.010844en
dc.rights.urihttps://creativecommons.org/licenses/by/4.0/
dc.subjectLactic acid bacteriaen
dc.subjectGlycopolymeren
dc.subjectPhage receptoren
dc.subjectLipoteichoic aciden
dc.subjectLTAen
dc.subjectFlippaseen
dc.subjectPeptidoglycanen
dc.subjectGlycosylationen
dc.subjectGenomicsen
dc.subjectGlycobiologyen
dc.subjectBacteriophageen
dc.subjectCell wallen
dc.subjectGlycosyltransferaseen
dc.titleThree distinct glycosylation pathways are involved in the decoration of Lactococcus lactis cell wall glycopolymersen
dc.typeArticle (peer-reviewed)en
dc.typeArticle (preprint)en
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