Trends in Microbiology
ReviewA phylum level perspective on bacterial cell envelope architecture
Section snippets
Clear definitions are needed when describing bacterial cell envelopes
The Gram stain has been a cornerstone of diagnostic microbiology and a fundamental laboratory method for over a century [1]. However, the easy distinction of Gram-positive and Gram-negative bacteria has led to oversimplifications concerning the diversity of bacterial cell envelope architecture. Thus, it is timely to review current knowledge of cell envelope architecture in the light of our growing appreciation of bacterial phylogeny, especially as the recent vast expansion in genome sequence
A broader phylogenetic perspective reveals dominance of the diderm–LPS cell envelope architecture
The revolution in bacterial phylogeny enabled by 16S rRNA gene sequencing has allowed the recognition that, aside from the three most intensively studied phyla (Actinobacteria, Firmicutes and Proteobacteria), there are more than 20 other phylum-level lineages of cultured bacteria 10, 11, 12. An excellent taxonomic overview of these is provided by J.P. Euzéby (http://www.bacterio.cict.fr/classifphyla.html). The sheer volume of studies on the Proteobacteria largely explains why the term
Phyla with typically monoderm cell envelopes
Perhaps surprisingly, only two well-defined bacterial phyla are predominantly composed of monoderm bacteria: Actinobacteria and Firmicutes. However, even within these two phyla there are notable lineages of diderm bacteria (see below). In addition to their typically thick-walled ultrastructure [14], a chemotaxonomic characteristic of the monoderm Actinobacteria and Firmicutes is evident: their peptidoglycan is typically intercalated with covalently attached polymers such as teichoic and
Exceptions within the typically diderm–LPS phyla
Although the diderm–LPS cell envelope architecture clearly predominates in the bacterial world, members of some lineages, notably within the phylum Spirochaetes, appear to have lost the ability to synthesise LPS but retain a diderm cell envelope architecture wherein alternative lipids apparently replace lipid A in the outer membrane 34, 35 (Table S1 in the supplementary material online). Even within the Proteobacteria there are examples of bacteria that lack LPS, as in Sphingomonas where the
Phyla with understudied or ambiguous cell envelope features
The phylum Chloroflexi (formerly the ‘Green non-Sulphur’ bacteria) is a robust lineage within the bacterial phylogenetic tree but its position remains unclear. Further studies are needed to define more precisely the unusual cell envelope features of this taxon and much heterogeneity is apparent, including variable/atypical peptidoglycan content and proteinaceous layers [53]. Unusual long chain diol lipids are present in some representatives 54, 55. Many Chloroflexi appear to have layered cell
Concluding remarks
The cell envelope is of vital importance as the interface between bacteria and their environments. Consequently, an understanding of cell envelope biology is fundamental to our understanding of the overall biology of bacteria. An appreciation of the variety of cell envelope archetypes thus needs to underpin our growing understanding of the vast extent of microbial diversity. This review has focused on membranes but there is also a growing awareness of the possible variety of ways in which the
Acknowledgements
This review is dedicated to Professor Mike Goodfellow (University of Newcastle upon Tyne, UK), my mentor in taxonomy, on the occasion of his retirement.
Glossary
- Diderm bacteria
- those with two cellular membranes, regardless of lipid composition [2].
- Eobacteria
- those with two cellular membranes that lack LPS. However, as defined by Cavalier-Smith [8,9], this grouping does not accommodate the diderm Thermotogae or Fibrobacteres. The hypothesis presented here that the Chloroflexi are monoderm is inconsistent with the inclusion of the ‘Chlorobacteria’ (Chloroflexi) in this taxon [9,10].
- Glycobacteria
- those with two cellular membranes that contain LPS as defined
References (80)
Use of the Gram stain in microbiology
Biotech. Histochem.
(2001)What are archaebacteria: life's third domain or monoderm prokaryotes related to Gram-positive bacteria? A new proposal for the classification of prokaryotic organisms
Mol. Microbiol.
(1998)Secretion and subcellular localizations of bacterial proteins: a semantic awareness issue
Trends Microbiol.
(2009)Discovery of new biosynthetic pathways: the lipid A story
J. Lipid Res.
(2009)Transport of lipopolysaccharide across the cell envelope: the long road of discovery
Nat. Rev. Microbiol.
(2009)The lipopolysaccharide transport system of Gram-negative bacteria
Biochim. Biophys. Acta
(2009)Biogenesis of outer membranes in Gram-negative bacteria
Biosci. Biotechnol. Biochem.
(2009)Rooting the tree of life by transition analyses
Biol. Direct
(2006)Deep phylogeny, ancestral groups and the four ages of life
Philos. Trans. R. Soc. B Biol. Sci.
(2010)- et al.
The uncultured microbial majority
Annu. Rev. Microbiol.
(2003)
A changing of the guard
Environ. Microbiol.
Mapping the tree of life: progress and prospects
Microbiol. Mol. Biol. Rev.
Bioinformatic analyses of Gram-negative bacterial OstA outer membrane assembly homologues
Curr. Genomics
Architecture of peptidoglycan: more data and more models
Trends Microbiol.
A continuum of anionic charge: structures and functions of D-alanyl-teichoic acids in Gram-positive bacteria
Microbiol. Mol. Biol. Rev.
Teichoic acids and related cell-wall glycopolymers in Gram-positive physiology and host interactions
Nat. Rev. Microbiol.
Lipoteichoic acid biosynthesis: two steps forwards, one step sideways?
Trends Microbiol.
Revised minimal standards for description of new species of the class Mollicutes (division Tenericutes)
Int. J. Syst. Evol. Microbiol.
A new lineage of halophilic, wall-less, contractile bacteria from a brine-filled deep of the Red Sea
J. Bacteriol.
New lineage of filamentous, spore-forming, Gram-positive bacteria from soil
Appl. Environ. Microbiol.
Thermosporothrix hazakensis gen. nov., sp. nov., isolated from compost and description of Thermosporotrichaceae fam. nov. within the class Ktedonobacteria Cavaletti et al. 2007 and emended description of the class Ktedonobacteria
Int. J. Syst. Evol. Microbiol.
Isolation of novel bacteria, including a candidate division, from geothermal soils in New Zealand
Environ. Microbiol.
Cultivation of uncultured Chloroflexi subphyla: significance and ecophysiology of formerly uncultured Chloroflexi ‘subphylum I’ with natural and biotechnological relevance
Microbes Environ.
Isolation and characterization of lipopolysaccharide from Centipeda periodontii ATCC 35019
Oral Microbiol. Immunol.
Lipopolysaccharides of anaerobic beer spoilage bacteria of the genus Pectinatus – lipopolysaccharides of a Gram-positive genus
FEMS Microbiol. Rev.
Molecular dissection of the Selenomonas ruminantium cell envelope and lysine decarboxylase involved in the biosynthesis of a polyamine covalently linked to the cell wall peptidoglycan layer
Biosci. Biotechnol. Biochem.
Genome analysis of the anaerobic thermohalophilic bacterium Halothermothrix orenii
PLOS One
Mycobacterial outer membranes: in search of proteins
Trends Microbiol.
Chemical principles in the organization of lipid components in the mycobacterial cell envelope
Res. Microbiol.
Disclosure of the mycobacterial outer membrane: cryo-electron tomography and vitreous sections reveal the lipid bilayer structure
Proc. Natl. Acad. Sci. U. S. A.
Direct visualization of the outer membrane of mycobacteria and corynebacteria in their native state
J. Bacteriol.
Comparative cell wall core biosynthesis in the mycolated pathogens, Mycobacterium tuberculosis and Corynebacterium diphtheriae
FEMS Microbiol. Rev.
Evidence for a new type of outer membrane lipid in oral spirochaete Treponema denticola. Functioning permeation barrier without lipopolysaccharide
J. Biol. Chem.
The structure and biological characteristics of the Spirochaeta aurantia outer membrane glycolipid LGLB
Eur. J. Biochem.
Structural analysis of a new glycosphingolipid from the lipopolysaccharide-lacking bacterium Sphingomonas adhaesiva
Carbohydr. Res.
Ehrlichia chaffeensis and Anaplasma phagocytophilum lack genes for Lipid A biosynthesis and incorporate cholesterol for their survival
Infect. Immun.
The Wolbachia genome of Brugia malayi: endosymbiont evolution within a human pathogenic nematode
PLOS Biol.
Genome of the extremely radiation-resistant bacterium Deinococcus radiodurans viewed from the perspective of comparative genomics
Microbiol. Mol. Biol. Rev.
Involvement of the S-layer proteins Hpi and SlpA in the maintenance of cell envelope integrity in Deinococcus radiodurans R1
Microbiology
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