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Genetic screens identify additional genes implicated in envelope remodeling during the engulfment stage of bacillus subtilis sporulation
Australian Institute for Microbiology and Infection, University of Technology Sydneygrid.117476.2 (UTS), Sydney, Australia.
Department of Microbiology, Unit Evolutionary Biology of the Microbial Cell, Paris, France; Hub Bioinformatics and Biostatistics, Department of Computational Biology, USR 3756 CNRS, Paris, France.
Umeå University, Faculty of Medicine, Molecular Infection Medicine Sweden (MIMS). Umeå University, Faculty of Medicine, Department of Molecular Biology (Faculty of Medicine).ORCID iD: 0000-0002-6848-5134
Australian Institute for Microbiology and Infection, University of Technology Sydneygrid.117476.2 (UTS), Sydney, Australia.
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2022 (English)In: mBio, ISSN 2161-2129, E-ISSN 2150-7511, Vol. 13, no 5, article id e0173222Article in journal (Refereed) Published
Abstract [en]

During bacterial endospore formation, the developing spore is internalized into the mother cell through a phagocytic-like process called engulfment, which involves synthesis and hydrolysis of peptidoglycan. Engulfment peptidoglycan hydrolysis requires the widely conserved and well-characterized DMP complex, composed of SpoIID, SpoIIM, and SpoIIP. In contrast, although peptidoglycan synthesis has been implicated in engulfment, the protein players involved are less well defined. The widely conserved SpoIIIAH-SpoIIQ interaction is also required for engulfment efficiency, functioning like a ratchet to promote membrane migration around the forespore. Here, we screened for additional factors required for engulfment using transposon sequencing in Bacillus subtilis mutants with mild engulfment defects. We discovered that YrvJ, a peptidoglycan hydrolase, and the MurA paralog MurAB, involved in peptidoglycan precursor synthesis, are required for efficient engulfment. Cytological analyses suggest that both factors are important for engulfment when the DMP complex is compromised and that MurAB is additionally required when the SpoIIIAH-SpoIIQ ratchet is abolished. Interestingly, despite the importance of MurAB for sporulation in B. subtilis, phylogenetic analyses of MurA paralogs indicate that there is no correlation between sporulation and the number of MurA paralogs and further reveal the existence of a third MurA paralog, MurAC, within the Firmicutes. Collectively, our studies identify two new factors that are required for efficient envelop remodeling during sporulation and highlight the importance of peptidoglycan precursor synthesis for efficient engulfment in B. subtilis and likely other endospore-forming bacteria. IMPORTANCE In bacteria, cell envelope remodeling is critical for cell growth and division. This is also the case during the development of bacteria into highly resistant endospores (spores), known as sporulation. During sporulation, the developing spore becomes internalized inside the mother cell through a phagocytic-like process called engulfment, which is essential to form the cell envelope of the spore. Engulfment involves both the synthesis and hydrolysis of peptidoglycan and the stabilization of migrating membranes around the developing spore. Importantly, although peptidoglycan synthesis has been implicated during engulfment, the specific genes that contribute to this molecular element of engulfment have remained unclear. Our study identifies two new factors that are required for efficient envelope remodeling during engulfment and emphasizes the importance of peptidoglycan precursor synthesis for efficient engulfment in the model organism Bacillus subtilis and likely other endospore-forming bacteria. Finally, our work highlights the power of synthetic screens to reveal additional genes that contribute to essential processes during sporulation.

Place, publisher, year, edition, pages
American Society for Microbiology , 2022. Vol. 13, no 5, article id e0173222
Keywords [en]
cell envelope, engulfment, morphogenesis, peptidoglycan, peptidoglycan remodeling, spores, sporulation
National Category
Microbiology
Identifiers
URN: urn:nbn:se:umu:diva-200878DOI: 10.1128/mbio.01732-22ISI: 000853834000001PubMedID: 36066101Scopus ID: 2-s2.0-85140856044OAI: oai:DiVA.org:umu-200878DiVA, id: diva2:1710504
Funder
Knut and Alice Wallenberg FoundationSwedish Research CouncilThe Kempe FoundationsAvailable from: 2022-11-14 Created: 2022-11-14 Last updated: 2023-11-10Bibliographically approved

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Gilmore, Michael C.Cava, Felipe

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