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

Luhur, J; Chan, H; Kachappilly, B; Mohamed, A; Morlot, C; Awad, M; Lyras, D; Taib, N; Gribaldo, S; Rudner, DZ; Rodrigues, CDA

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

Luhur, J Chan, H

Kachappilly, B Mohamed, A Morlot, C Awad, M Lyras, D Taib, N Gribaldo, S Rudner, DZ Rodrigues, CDA

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Publisher:: Public Library of Science (PLoS)
Publication Type:: Journal Article
Citation:: PLoS Genet, 2020, 16, (12)
Issue Date:: 2020-12-14

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Field	Value	Language
dc.contributor.author	Luhur, J
dc.contributor.author	Chan, H https://orcid.org/0000-0002-5194-0006
dc.contributor.author	Kachappilly, B
dc.contributor.author	Mohamed, A
dc.contributor.author	Morlot, C
dc.contributor.author	Awad, M
dc.contributor.author	Lyras, D
dc.contributor.author	Taib, N
dc.contributor.author	Gribaldo, S
dc.contributor.author	Rudner, DZ
dc.contributor.author	Rodrigues, CDA
dc.date.accessioned	2020-12-18T00:36:20Z
dc.date.available	2020-11-03
dc.date.available	2020-12-18T00:36:20Z
dc.date.issued	2020-12-14
dc.identifier.citation	PLoS Genet, 2020, 16, (12)
dc.identifier.issn	1553-7390
dc.identifier.issn	1553-7404
dc.identifier.uri	http://hdl.handle.net/10453/144818
dc.description.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 supresses 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.
dc.language	eng
dc.publisher	Public Library of Science (PLoS)
dc.relation	http://purl.org/au-research/grants/arc/DP190100793
dc.relation.ispartof	PLoS Genet
dc.relation.isbasedon	10.1371/journal.pgen.1009246
dc.rights	info:eu-repo/semantics/openAccess
dc.subject	0604 Genetics
dc.subject.classification	Developmental Biology
dc.title	A dynamic, ring-forming MucB / RseB-like protein influences spore shape in Bacillus subtilis.
dc.type	Journal Article
utslib.citation.volume	16
utslib.location.activity	United States
utslib.for	0604 Genetics
pubs.organisational-group	/University of Technology Sydney/Faculty of Science
pubs.organisational-group	/University of Technology Sydney/Strength - ithree - Institute of Infection, Immunity and Innovation
pubs.organisational-group	/University of Technology Sydney
utslib.copyright.status	open_access	*
pubs.consider-herdc	false
dc.date.updated	2020-12-18T00:35:58Z
pubs.issue	12
pubs.publication-status	Published online
pubs.volume	16
utslib.citation.issue	12

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 supresses 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.

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http://hdl.handle.net/10453/144818