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The bacterial cell envelope
Colin Kleanthous and Judith P. Armitage
rstb.royalsocietypublishing.org
Department of Biochemistry, University of Oxford, Oxford OX1 3QU, UK
JA, 0000-0003-4983-9731
Introduction
Cite this article: Kleanthous C, Armitage JP.
2015 The bacterial cell envelope. Phil. Trans.
R. Soc. B 370: 20150019.
http://dx.doi.org/10.1098/rstb.2015.0019
Accepted: 3 August 2015
One contribution of 12 to a theme issue
‘The bacterial cell envelope’.
Subject Areas:
cellular biology, microbiology, biochemistry
Author for correspondence:
Judith P. Armitage
e-mail: [email protected]
Antonie van Leeuwenhoek, a draper from Delft, using a tiny homemade microscope, first described microbes or ‘animalcules’ in a number of letters to the
Royal Society. The letters specifically describe ‘animalcules’ in pepper water in
1676 (published 1677). The famous drawing of a swimming animalcule from a
scraping of his teeth was in a letter of 1684 (reference [1] is the original letter
while reference [2] uses replica microscopes to interpret the letters and reference
[3] is a recent article concisely putting this early work in context). These ‘animalcules’ were identified as living because they moved, and some were almost
certainly bacteria because of their calculated size and swimming pattern ‘. . .
whereas an eel always swims head first, these animalcules swam as well backwards as forwards’. Notwithstanding the Royal Society’s initial scepticism,
including wondering whether van Leeuwenhoek was inebriated at the time of
his observations, subsequent verification by Robert Hooke unambiguously
proved the existence of living, microscopic organisms invisible to the naked eye.
van Leeuwenhoek was ingenious in his use of everyday objects (grains of sand,
hair of a flea) to guesstimate the size of his animalcules (approx. 3 mm), although
his fear at not being believed made him underestimate the number of such
organisms in a drop of water in his correspondence with the Royal Society.
van Leeuwenhoek’s use of his single lens microscope changed perceptions about
our world. In the intervening 350 years, our knowledge of these animalcules (bacteria) has similarly been transformed. In particular, major technical advances in
microscopy, and the advent of genetic, biophysical, biochemical and structural
approaches have brought us unparalleled insights into these microscopic organisms.
We now also have a far greater understanding of their central importance to human
health and disease and to the global environment. In this edition, we focus on a
region of bacteria, the cell envelope, that in most bacteria accounts for only 10% of
the cell volume but to which the organism typically devotes a quarter of its genome.
The cell envelope gives bacteria their shape, provides the means by which they
generate usable forms of energy for growth and division, protects the organism
from host immune responses, promotes pathogenesis, is integral to the horizontal
transfer of plasmids and other mobile elements and forms the conduit through
which bacteria interface with their surroundings. The essential nature of the cell
envelope makes it vulnerable to small molecules that bacteria deploy when competing for resources, which is the foundation of antibiotic therapy today. Moreover, the
cell envelope remains a popular target in the search for novel antibiotics to combat
the rise in multidrug resistance. All the complex functions carried out by bacteria
require a high degree of organization, and much of the recent excitement regarding
envelope biology stems from our newly formed appreciation of this organization.
The reviews published in this collection reflect some of the major advances in the
field in the past few years from leaders in their respective fields. While we have
endeavoured to capture all that is novel and innovative in bacterial cell envelope
biology, inevitably some areas are absent for which the editors apologize. There
is only so much you can do (or indeed beg for).
In general, the bacterial cell envelope comes in two types: that of Gramnegative bacteria which have two membranes, a cytoplasmic and outer
membrane separated by the periplasm in which is a thin cell wall made up of
peptidoglycan, and that of Gram-positive bacteria which have only a cytoplasmic
membrane surrounded by a much thicker peptidoglycan layer. The structures
and processes described in this theme issue emanate from the cytoplasmic
membrane and cover the entirety of the cell envelope, and include studies in
both Gram-positive and Gram-negative microorganisms.
& 2015 The Author(s) Published by the Royal Society. All rights reserved.
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Competing interests. We declare we have no competing interests.
Funding. We received no funding for this study.
AUTHOR PROFILES
Judith Armitage did her BSc and PhD degrees in Microbiology at University College London. After a
period as a Lister Institute Research Fellow, she moved to the Biochemistry Department at University
of Oxford as a University Lecturer, becoming a full professor in 1995. Her research centres on the
behaviour of swimming bacteria, in particular the photoheterotrophic alpha proteobacterium Rhodobacter sphaeroides. She is particularly interested in the structure and function of the rotary flagellar
motor and its control by the chemotaxis systems. She is a Member of EMBO and a Fellow of the
American Academy of Microbiology and of The Royal Society.
Colin Kleanthous did his BSc in Chemistry with Biochemistry and PhD in Biochemistry at the University of Leicester. Following postdocs at the University of California, Berkeley, and University of
Glasgow, he took up a lectureship in the School of Biological Sciences at the University of East
Anglia, moving subsequently to the Department of Biology at the University of York. He joined
the Department of Biochemistry at the University of Oxford in 2012 as the Iveagh Professor of
Microbial Biochemistry. His research centres on bacterial protein –protein interactions, in particular
how bacteriocins use such interactions to catalyse their translocation across the Gram-negative
cell envelope, which has led to an interest in the organization of outer membrane proteins. He
was chairman of the UK Biochemical Society 2011–2013.
References
1.
Leewenhoeck A. 1677 Observation, communicated
to the publisher by Mr. Antonie van Leewenhoeck
in a Dutch letter of the 9 Octob. 1676 here
English’d: concerning little animals by him
observed in rain-well-sea and snow water; as
also in water wherein pepper had lain infused.
Phil. Trans. 12, 821–831. (doi:10.1098/rstl.
1677.0003)
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Ford BJ. 1991 The Leeuwenhoek legacy. Bristol and
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Lane N. 2015 The unseen world: reflections on
Leeuwenhoek (1677) ‘concerning little animals’.
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Rowlett VW, Margolin W. 2015 The bacterial
divisome: ready for its close-up. Phil. Trans.
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Collinson I, Corey RA, Allen WJ. 2015 Channel
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2
Phil. Trans. R. Soc. B 370: 20150019
[10,11]. The other major protein component in the outer
membrane is lipoprotein, which is dealt with in the next
review [12]. The authors highlight how lipoproteins can be
displayed on the surface of bacteria. Finally, we deal with
structures that span the cell envelope, including the rotary
motor of the bacterial flagellum and the related injectisome of
the type III secretion system [13], and the type VI secretion
system used by bacteria to kill each other during inter- and
intraspecies competition [14].
Given the rate of progress in understanding the bacterial
cell envelope since van Leeuwenhoek’s time, we can only
imagine what the next 350 years will bring. Already, single
ribosomes can be resolved almost at atomic resolution in bacteria! The forthcoming decades will undoubtedly furnish us
with ever more detailed knowledge of how the structures
of the cell envelope are built, maintained and regulated,
which will ultimately allow their exploitation as much
needed new targets for antibiotic therapy and biomaterials.
rstb.royalsocietypublishing.org
The edition begins with the key problem unicellular organisms face, that of identifying their middle at the right time to
ensure the even segregation of genetic and cellular material at
cell division [4]. The following article covers how proteins
move across the cytoplasmic membrane, so that the cell envelope can be built [5]. Peptidoglycan cell wall composition and
assembly are then dealt with in the two following reviews
[6,7]. The next five articles deal with the problems associated with building the outer membrane. In contrast to the
cytoplasmic membrane, the outer membrane is asymmetric,
composed of an inner leaflet of phospholipids and an outer leaflet of lipopolysaccharide (LPS). Another key difference is the
fact that the outer membrane is devoid of an energy source.
All these features mean that building and maintaining the
outer membrane has been until recently a puzzle. The five
reviews within the theme issue reflect the huge advances
that have been made and tackle complementary aspects of
this problem: these include building LPS at the cytoplasmic
membrane, and transporting it across the periplasm and then
inserting it into the outer membrane [8,9]; the following
two articles deal with the folding and insertion of the major
proteins in the outer membrane, which are almost all b-barrels
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8.
9.
Phil. Trans. R. Soc. B 370, 20150026. (doi:10.1098/
rstb.2015.0026)
12. Konovalova A, Silhavy TJ. 2015 Outer membrane
lipoprotein biogenesis: Lol is not the end. Phil.
Trans. R. Soc. B 370, 20150030. (doi:10.1098/rstb.
2015.0030)
13. Diepold A, Armitage JP. 2015 Type III secretion
systems: the bacterial flagellum and the
injectisome. Phil. Trans. R. Soc. B 370, 20150020.
(doi:10.1098/rstb.2015.0020)
14. Basler M. 2015 Type VI secretion system: secretion
by a contractile nanomachine. Phil. Trans. R. Soc. B
370, 20150021. (doi:10.1098/rstb.2015.0021)
3
Phil. Trans. R. Soc. B 370: 20150019
May JM, Sherman DJ, Simpson BW, Ruiz N,
Kahne D. 2015 Lipopolysaccharide transport
to the cell surface: periplasmic transport and
assembly into the outer membrane. Phil.
Trans. R. Soc. B 370, 20150027. (doi:10.1098/
rstb.2015.0027)
10. Rollauer SE, Sooreshjani MA, Noinaj N, Buchanan SK.
2015 Outer membrane protein biogenesis in
Gram-negative bacteria. Phil. Trans. R. Soc. B 370,
20150023. (doi:10.1098/rstb.2015.0023)
11. Fleming KG. 2015 A combined kinetic push and
thermodynamic pull as driving forces for outer
membrane protein sorting and folding in bacteria.
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7.
of peptidoglycan synthases. Phil. Trans. R.
Soc. B 370, 20150031. (doi:10.1098/rstb.
2015.0031)
Romaniuk JAH, Cegelski L. 2015 Bacterial cell
wall composition and the influence of antibiotics
by cell-wall and whole-cell NMR. Phil. Trans.
R. Soc. B 370, 20150024. (doi:10.1098/rstb.
2015.0024)
Simpson BW, May JM, Sherman DJ, Kahne D, Ruiz
N. 2015 Lipopolysaccharide transport to the cell
surface: biosynthesis and extraction from the inner
membrane. Phil. Trans. R. Soc. B 370, 20150029.
(doi:10.1098/rstb.2015.0029)