A dual-chain assembly pathway generates the high structural diversity of cell-wall polysaccharides in Lactococcus lactis

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dc.contributor.authorTheodorou, Iliasen
dc.contributor.authorCourtin, Pascalen
dc.contributor.authorPalussière, Simonen
dc.contributor.authorKulakauskas, Sauliusen
dc.contributor.authorBidnenko, Elenaen
dc.contributor.authorPéchoux, Christineen
dc.contributor.authorFenaille, Françoisen
dc.contributor.authorPenno, Christopheen
dc.contributor.authorMahony, Jenniferen
dc.contributor.authorvan Sinderen, Douween
dc.contributor.authorChapot-Chartier, Marie-Pierreen
dc.contributor.funderScience Foundation Irelanden
dc.date.accessioned2023-11-29T13:14:43Z
dc.date.available2023-11-29T13:14:43Z
dc.date.issued2019en
dc.description.abstractIn Lactococcus lactis, cell-wall polysaccharides (CWPSs) act as receptors for many bacteriophages, and their structural diversity among strains explains, at least partially, the narrow host range of these viral predators. Previous studies have reported that lactococcal CWPS consists of two distinct components, a variable chain exposed at the bacterial surface, named polysaccharide pellicle (PSP), and a more conserved rhamnan chain anchored to, and embedded inside, peptidoglycan. These two chains appear to be covalently linked to form a large heteropolysaccharide. The molecular machinery for biosynthesis of both components is encoded by a large gene cluster, named cwps. In this study, using a CRISPR/Cas-based method, we performed a mutational analysis of the cwps genes. MALDI-TOF MS-based structural analysis of the mutant CWPS combined with sequence homology, transmission EM, and phage sensitivity analyses enabled us to infer a role for each protein encoded by the cwps cluster. We propose a comprehensive CWPS biosynthesis scheme in which the rhamnan and PSP chains are independently synthesized from two distinct lipid-sugar precursors and are joined at the extracellular side of the cytoplasmic membrane by a mechanism involving a membrane-embedded glycosyltransferase with a GT-C fold. The proposed scheme encompasses a system that allows extracytoplasmic modification of rhamnan by complex substituting oligo-/polysaccharides. It accounts for the extensive diversity of CWPS structures observed among lactococci and may also have relevance to the biosynthesis of complex rhamnose-containing CWPSs in other Gram-positive bacteria.en
dc.description.statusPeer revieweden
dc.description.versionPublished Versionen
dc.format.mimetypeapplication/pdfen
dc.identifier.citationTheodorou, I., Courtin, P., Palussière, S., Kulakauskas, S., Bidnenko, E., Péchoux, C., Fenaille, F., Penno, C., Mahony, J., Van Sinderen, D. and Chapot-Chartier, M.-P. (2019) ‘A dual-chain assembly pathway generates the high structural diversity of cell-wall polysaccharides in Lactococcus lactis’, Journal of Biological Chemistry, 294(46), pp. 17612–17625. doi: 10.1074/jbc.RA119.009957en
dc.identifier.doi10.1074/jbc.ra119.009957en
dc.identifier.endpage17625en
dc.identifier.issn0021-9258en
dc.identifier.issued46en
dc.identifier.journaltitleJournal of Biological Chemistryen
dc.identifier.startpage17612en
dc.identifier.urihttps://hdl.handle.net/10468/15275
dc.identifier.volume294en
dc.language.isoenen
dc.publisherAmerican Society for Biochemistry and Molecular Biology Inc.en
dc.relation.ispartofJournal of Biological Chemistryen
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.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.rights© 2019 Theodorou et al. Published under exclusive license by The American Society for Biochemistry and Molecular Biology, Inc. This is an Open Access article under the CC BY license.en
dc.rights.urihttps://creativecommons.org/licenses/by/4.0/en
dc.subjectGram-positive bacteriaen
dc.subjectPolysaccharideen
dc.subjectCell wallen
dc.subjectBiosynthesisen
dc.subjectBacteriophageen
dc.subjectGlycopolymeren
dc.subjectGlycosyltransferaseen
dc.subjectLactic acid bacteriaen
dc.subjectRhamnanen
dc.subjectRhamnoseen
dc.titleA dual-chain assembly pathway generates the high structural diversity of cell-wall polysaccharides in Lactococcus lactisen
dc.typeArticle (peer-reviewed)en
dc.typejournal-articleen
oaire.citation.issue46en
oaire.citation.volume294en
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