Cell-wall remodeling drives engulfment during Bacillus subtiliss porulation
File(s)Ojkic_eLife_2016.pdf (4.81 MB)
Published version
Author(s)
Ojkic, N
Lopez-Garrido, J
Pogliano, K
Endres, RG
Type
Journal Article
Abstract
When starved, the Gram-positive bacterium Bacillus subtilis forms durable spores for
survival. Sporulation initiates with an asymmetric cell division, creating a large mother cell and a
small forespore. Subsequently, the mother cell membrane engulfs the forespore in a phagocytosislike
process. However, the force generation mechanism for forward membrane movement remains
unknown. Here, we show that membrane migration is driven by cell wall remodeling at the leading
edge of the engulfing membrane, with peptidoglycan synthesis and degradation mediated by
penicillin binding proteins in the forespore and a cell wall degradation protein complex in the
mother cell. We propose a simple model for engulfment in which the junction between the septum
and the lateral cell wall moves around the forespore by a mechanism resembling the ‘template
model’. Hence, we establish a biophysical mechanism for the creation of a force for engulfment
based on the coordination between cell wall synthesis and degradation.
survival. Sporulation initiates with an asymmetric cell division, creating a large mother cell and a
small forespore. Subsequently, the mother cell membrane engulfs the forespore in a phagocytosislike
process. However, the force generation mechanism for forward membrane movement remains
unknown. Here, we show that membrane migration is driven by cell wall remodeling at the leading
edge of the engulfing membrane, with peptidoglycan synthesis and degradation mediated by
penicillin binding proteins in the forespore and a cell wall degradation protein complex in the
mother cell. We propose a simple model for engulfment in which the junction between the septum
and the lateral cell wall moves around the forespore by a mechanism resembling the ‘template
model’. Hence, we establish a biophysical mechanism for the creation of a force for engulfment
based on the coordination between cell wall synthesis and degradation.
Date Issued
2016-11-17
Date Acceptance
2016-11-14
Citation
eLife, 2016, 5
ISSN
2050-084X
Publisher
eLife Sciences Publications
Journal / Book Title
eLife
Volume
5
Copyright Statement
© 2016 Ojkic et al. This
article is distributed under the
terms of the Creative Commons
Attribution License (https://creativecommons.org/licenses/by/4.0/), which
permits unrestricted use and
redistribution provided that the
original author and source are
credited.
article is distributed under the
terms of the Creative Commons
Attribution License (https://creativecommons.org/licenses/by/4.0/), which
permits unrestricted use and
redistribution provided that the
original author and source are
credited.
Sponsor
Biotechnology and Biological Sciences Research Council (BBSRC)
Commission of the European Communities
Identifier
http://gateway.webofknowledge.com/gateway/Gateway.cgi?GWVersion=2&SrcApp=PARTNER_APP&SrcAuth=LinksAMR&KeyUT=WOS:000391440500001&DestLinkType=FullRecord&DestApp=ALL_WOS&UsrCustomerID=1ba7043ffcc86c417c072aa74d649202
Grant Number
BB/I019987/1
FP7-ERC-2011-STG-280492
Subjects
Science & Technology
Life Sciences & Biomedicine
Biology
Life Sciences & Biomedicine - Other Topics
PENICILLIN-BINDING PROTEINS
GENE-EXPRESSION
PEPTIDOGLYCAN ARCHITECTURE
FORESPORE ENGULFMENT
SPORE MORPHOGENESIS
MEMBRANE DYNAMICS
ESCHERICHIA-COLI
TEICHOIC-ACID
SPORULATION
LOCALIZATION
B. subtilis
cell wall
computational biology
infectious disease
microbiology
peptidoglycan remodeling
sporulation
systems biology
Publication Status
Published
Article Number
ARTN e18657