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The role of GpsB in Staphylococcus aureus cell morphogenesis

2024-03-13Artigo científico Acesso aberto
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dc.contributor.authorCosta, Sara Francisco
dc.contributor.authorSaraiva, Bruno M.
dc.contributor.authorVeiga, Helena
dc.contributor.authorMarques, Leonor B.
dc.contributor.authorSchäper, Simon
dc.contributor.authorSporniak, Marta
dc.contributor.authorVega, Daniel E.
dc.contributor.authorJorge, Ana M.
dc.contributor.authorDuarte, Andreia M.
dc.contributor.authorBrito, A.
dc.contributor.authorTavares, Andreia C.
dc.contributor.authorReed, Patricia
dc.contributor.authorPinho, Mariana G.
dc.contributor.institutionInstituto de Tecnologia Química e Biológica António Xavier (ITQB)
dc.contributor.pblAmerican Society for Microbiology
dc.date.accessioned2025-05-07T21:17:20Z
dc.date.available2025-05-07T21:17:20Z
dc.date.issued2024-03-13
dc.descriptionFunding Information: This study was funded by the European Research Council through grant ERC-2017-CoG-771709 (to M.G.P.); by national funds from FCT–Fundação para a Ciência e a Tecnologia through PTDC/BIA-MIC/6982/2020 (to H.V.), MOSTMICRO-ITQB R&D Unit (UIDB/04612/2020, UIDP/04612/2020 to ITQB-NOVA), and LS4FUTURE Associated Laboratory (LA/P/0087/2020 to ITQB-NOVA); by contract 2022.03033.CEECIND (to S.S.), fellowships PD/BD/135480/2018 (to S.F.C.), COVID/BD/152499/2022 (to S.F.C.), SFRH/BD/ 147052/2019 (to B.M.S.), UI/BD/153384/2022 (to L.B.M.), SFRH/BD/143461/2019 (to A.M.D.), and 2021.06849.BD (to A.D.B.); and by the European Union’s Horizon 2020 research and innovation program under the Marie Sklodowska-Curie grant agreement no. 839596 (to S.S.). Publisher Copyright: © 2024 Costa et al.
dc.description.abstractFor decades, cells of the Gram-positive bacterial pathogen Staphylococcus aureus were thought to lack a dedicated elongation machinery. However, S. aureus cells were recently shown to elongate before division, in a process that requires a shape elongation division and sporulation (SEDS)/penicillin-binding protein (PBP) pair for peptidoglycan synthesis, consisting of the glycosyltransferase RodA and the transpeptidase PBP3. In ovococci and rod-shaped bacteria, the elongation machinery, or elongasome, is composed of various proteins besides a dedicated SEDS/PBP pair. To identify proteins required for S. aureus elongation, we screened the Nebraska Transposon Mutant Library, which contains transposon mutants in virtually all non-essential staphylococcal genes, for mutants with modified cell shape. We confirmed the roles of RodA/PBP3 in S. aureus elongation and identified GpsB, SsaA, and RodZ as additional proteins involved in this process. The gpsB mutant showed the strongest phenotype, mediated by the partial delocalization from the division septum of PBP2 and PBP4, two penicillin-binding proteins that synthesize and cross-link peptidoglycan. Increased levels of these PBPs at the cell periphery versus the septum result in higher levels of peptidoglycan insertion/crosslinking throughout the entire cell, possibly overriding the RodA/PBP3-mediated peptidoglycan synthesis at the outer edge of the septum and/or increasing stiffness of the peripheral wall, impairing elongation. Consequently, in the absence of GpsB, S. aureus cells become more spherical. We propose that GpsB has a role in the spatio-temporal regulation of PBP2 and PBP4 at the septum versus cell periphery, contributing to the maintenance of the correct cell morphology in S. aureus. IMPORTANCE Staphylococcus aureus is a Gram-positive clinical pathogen, which is currently the second cause of death by antibiotic-resistant infections worldwide. For decades, S. aureus cells were thought to be spherical and lack the ability to undergo elongation. However, super-resolution microscopy techniques allowed us to observe the minor morphological changes that occur during the cell cycle of this pathogen, including cell elongation. S. aureus elongation is not required for normal growth in laboratory conditions. However, it seems to be essential in the context of some infections, such as osteomyelitis, during which S. aureus cells apparently elongate to invade small channels in the bones. In this work, we uncovered new determinants required for S. aureus cell elongation. In particular, we show that GpsB has an important role in the spatio-temporal regulation of PBP2 and PBP4, two proteins involved in peptidoglycan synthesis, contributing to the maintenance of the correct cell morphology in S. aureus.en
dc.description.versionpublishersversion
dc.description.versionpublished
dc.format.extent3170382
dc.identifier.doi10.1128/mbio.03235-23
dc.identifier.issn2161-2129
dc.identifier.otherPURE: 90506962
dc.identifier.otherPURE UUID: 606ae01e-0d37-4439-920c-0a5c9c4dc8a8
dc.identifier.otherScopus: 85187711070
dc.identifier.otherPubMed: 38319093
dc.identifier.otherORCID: /0000-0002-4263-6993/work/183499556
dc.identifier.urihttp://hdl.handle.net/10362/182735
dc.identifier.urlhttps://www.scopus.com/pages/publications/85187711070
dc.language.isoeng
dc.peerreviewedyes
dc.subjectelongasome
dc.subjectGpsB
dc.subjectmorphogenesis
dc.subjectStaphylococcus aureus
dc.subjectMicrobiology
dc.subjectVirology
dc.titleThe role of GpsB in Staphylococcus aureus cell morphogenesisen
dc.typejournal article
degois.publication.issue3
degois.publication.titlemBio
degois.publication.volume15
dspace.entity.typePublication
rcaap.rightsopenAccess

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