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A dynamic, ring-forming MucB / RseB-like protein influences spore shape in Bacillus subtilis

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Kearns, Daniel B., Luhur, Johana, Chan, Helena, Kachappilly, Benson, Mohamed, Ahmed, Morlot, Cécile, Awad, Milena, Lyras, Dena, Taib, Najwa, Gribaldo, Simonetta, Rudner, David Z. and Rodrigues, Christopher D.A. (2020) A dynamic, ring-forming MucB / RseB-like protein influences spore shape in Bacillus subtilis. PLoS Genetics, 16 (12). e1009246. doi:10.1371/journal.pgen.1009246

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Official URL: http://dx.doi.org/10.1371/journal.pgen.1009246

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Abstract

How organisms develop into specific shapes is a central question in biology. The maintenance of bacterial shape is connected to the assembly and remodelling of the cell envelope. In endospore-forming bacteria, the pre-spore compartment (the forespore) undergoes morphological changes that result in a spore of defined shape, with a complex, multi-layered cell envelope. However, the mechanisms that govern spore shape remain poorly understood. Here, using a combination of fluorescence microscopy, quantitative image analysis, molecular genetics and transmission electron microscopy, we show that SsdC (formerly YdcC), a poorly-characterized new member of the MucB / RseB family of proteins that bind lipopolysaccharide in diderm bacteria, influences spore shape in the monoderm Bacillus subtilis. Sporulating cells lacking SsdC fail to adopt the typical oblong shape of wild-type forespores and are instead rounder. 2D and 3D-fluorescence microscopy suggest that SsdC forms a discontinuous, dynamic ring-like structure in the peripheral membrane of the mother cell, near the mother cell proximal pole of the forespore. A synthetic sporulation screen identified genetic relationships between ssdC and genes involved in the assembly of the spore coat. Phenotypic characterization of these mutants revealed that spore shape, and SsdC localization, depend on the coat basement layer proteins SpoVM and SpoIVA, the encasement protein SpoVID and the inner coat protein SafA. Importantly, we found that the ΔssdC mutant produces spores with an abnormal-looking cortex, and abolishing cortex synthesis in the mutant largely suppresses its shape defects. Thus, SsdC appears to play a role in the proper assembly of the spore cortex, through connections to the spore coat. Collectively, our data suggest functional diversification of the MucB / RseB protein domain between diderm and monoderm bacteria and identify SsdC as an important factor in spore shape development.

Item Type: Journal Article
Subjects: Q Science > QH Natural history
Q Science > QP Physiology
Q Science > QR Microbiology
Divisions: Faculty of Science > Life Sciences (2010- )
Library of Congress Subject Headings (LCSH): Bacillus subtilis , Gram-negative bacteria, Bacterial spores, Germination, Membrane proteins, Cells -- Morphology
Journal or Publication Title: PLoS Genetics
Publisher: Public Library of Science
ISSN: 1553-7390
Official Date: 14 December 2020
Dates:
DateEvent
14 December 2020Published
3 November 2020Accepted
Volume: 16
Number: 12
Article Number: e1009246
DOI: 10.1371/journal.pgen.1009246
Status: Peer Reviewed
Publication Status: Published
Access rights to Published version: Open Access
RIOXX Funder/Project Grant:
Project/Grant IDRIOXX Funder NameFunder ID
DP190100793Australian Research Councilhttp://dx.doi.org/10.13039/501100000923

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