Communication across the bacterial cell envelope depends on the size of the periplasm
Author(s)
Type
Journal Article
Abstract
The
cell
envelope
of gram-negative
bacteria,
a structure
comprising
an
outer
(OM)
and
an
inner
(IM)
membrane,
is essential
for
life.
The
OM
and
the
IM
are
separated
by
the
peri-
plasm,
a compartment
that
contains
the
peptidoglycan
. The
OM
is tethered
to the
peptido-
glycan
via
the
lipoprotein,
Lpp.
However,
the
importance
of the
envelope’s
multilayered
architecture
remains
unknown.
Here,
when
we
removed
physical
coupling
between
the
OM
and
the
peptidoglycan,
cells
lost
the
ability
to sense
defects
in envelope
integrity.
Further
experiments
revealed
that
the
critical
parameter
for
the
transmission
of stress
signals
from
the
envelope
to the
cytoplasm
, where
cellular
behaviour
is controlled,
is the
IM-to-OM
dis-
tance.
Augmenting
this
distance
by
increasing
the
length
of the
lipoprotein
Lpp
destroyed
signalling,
whereas
simultaneously
increasing
the
length
of the
stress-sensing
lipoprotein
RcsF
restored
signalling.
Our
results
demonstrate
the
physiologica
l importance
of the
size
of the
periplasm.
They
also
reveal
that
strict
control
over
the
IM-to-OM
distance
is required
for
effective
envelope
surveillance
and
protection,
suggesting
that
cellular
architecture
and
the
structure
of transenvelope
protein
complexes
have
been
evolutionarily
co-optimised
for
correct
function.
Similar
strategies
are
likely
at play
in cellular
compartments
surrounded
by
2 concentric
membranes,
such
as
chloroplasts
and
mitochondria.
cell
envelope
of gram-negative
bacteria,
a structure
comprising
an
outer
(OM)
and
an
inner
(IM)
membrane,
is essential
for
life.
The
OM
and
the
IM
are
separated
by
the
peri-
plasm,
a compartment
that
contains
the
peptidoglycan
. The
OM
is tethered
to the
peptido-
glycan
via
the
lipoprotein,
Lpp.
However,
the
importance
of the
envelope’s
multilayered
architecture
remains
unknown.
Here,
when
we
removed
physical
coupling
between
the
OM
and
the
peptidoglycan,
cells
lost
the
ability
to sense
defects
in envelope
integrity.
Further
experiments
revealed
that
the
critical
parameter
for
the
transmission
of stress
signals
from
the
envelope
to the
cytoplasm
, where
cellular
behaviour
is controlled,
is the
IM-to-OM
dis-
tance.
Augmenting
this
distance
by
increasing
the
length
of the
lipoprotein
Lpp
destroyed
signalling,
whereas
simultaneously
increasing
the
length
of the
stress-sensing
lipoprotein
RcsF
restored
signalling.
Our
results
demonstrate
the
physiologica
l importance
of the
size
of the
periplasm.
They
also
reveal
that
strict
control
over
the
IM-to-OM
distance
is required
for
effective
envelope
surveillance
and
protection,
suggesting
that
cellular
architecture
and
the
structure
of transenvelope
protein
complexes
have
been
evolutionarily
co-optimised
for
correct
function.
Similar
strategies
are
likely
at play
in cellular
compartments
surrounded
by
2 concentric
membranes,
such
as
chloroplasts
and
mitochondria.
Date Issued
2017-12-19
Date Acceptance
2017-11-10
Citation
PLOS BIOLOGY, 2017, 15 (12)
ISSN
1545-7885
Publisher
PUBLIC LIBRARY OF SCIENCE
Journal / Book Title
PLOS BIOLOGY
Volume
15
Issue
12
Copyright Statement
©
2017
Asmar
et al. This is an open
access
article
distributed
under
the terms
of the
Creative
Commons
Attribution
License (https://creativecommons.org/licenses/by/4.0/),
which
permits
unrestricte
d use, distribu
tion, and
reproduction
in any medium,
provided
the original
author
and source
are credited.
2017
Asmar
et al. This is an open
access
article
distributed
under
the terms
of the
Creative
Commons
Attribution
License (https://creativecommons.org/licenses/by/4.0/),
which
permits
unrestricte
d use, distribu
tion, and
reproduction
in any medium,
provided
the original
author
and source
are credited.
Sponsor
Commission of the European Communities
Identifier
http://gateway.webofknowledge.com/gateway/Gateway.cgi?GWVersion=2&SrcApp=PARTNER_APP&SrcAuth=LinksAMR&KeyUT=WOS:000418943900022&DestLinkType=FullRecord&DestApp=ALL_WOS&UsrCustomerID=1ba7043ffcc86c417c072aa74d649202
Grant Number
630988
Subjects
Science & Technology
Life Sciences & Biomedicine
Biochemistry & Molecular Biology
Biology
Life Sciences & Biomedicine - Other Topics
OUTER-MEMBRANE LIPOPROTEIN
ESCHERICHIA-COLI
RCS PHOSPHORELAY
MUREIN-LIPOPROTEIN
PROTEIN RCSF
BINDING
STRESS
WALL
VISUALIZATION
ATTACHMENT
Bacterial Outer Membrane Proteins
Cell Membrane
Cell Wall
Cytoplasm
Escherichia coli
Escherichia coli Proteins
Gram-Negative Bacteria
Lipoproteins
Membrane Proteins
Peptidoglycan
Periplasm
06 Biological Sciences
11 Medical And Health Sciences
07 Agricultural And Veterinary Sciences
Developmental Biology
Publication Status
Published
Article Number
ARTN e2004303