A phylum level perspective on bacterial cell envelope architecture

doi:10.1016/j.tim.2010.06.005

Trends in Microbiology

Volume 18, Issue 10, October 2010, Pages 464-470

https://doi.org/10.1016/j.tim.2010.06.005 Get rights and content

Improved understanding of the bacterial phylogenetic tree has allowed the distinction of at least 25 phyla with cultured representatives. This review surveys the diversity of cell envelope types present in these phyla and emphasises that it is important to define bacterial cell envelopes according to whether they have one (monoderm) or two (diderm) cellular membranes and, in the latter case, lipopolysaccharide as well. A comparative genomics approach, facilitated by the recent vast expansion in genome sequence information, is used here to survey the distribution of key lipopolysaccharide biosynthesis enzymes across the bacterial world and to consider alternative diderm cell envelope architectures. These data add to our understanding of microbial diversity and it is notable that the majority of phyla are likely to comprise diderm, lipopolysaccharide containing bacteria. This analysis and a critical review of the literature also suggest that members of the phylum Chloroflexi are typically monoderm.

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

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Trends in Microbiology

ReviewA phylum level perspective on bacterial cell envelope architecture

Section snippets

Clear definitions are needed when describing bacterial cell envelopes

A broader phylogenetic perspective reveals dominance of the diderm–LPS cell envelope architecture

Phyla with typically monoderm cell envelopes

Exceptions within the typically diderm–LPS phyla

Phyla with understudied or ambiguous cell envelope features

Concluding remarks

Acknowledgements

Glossary

Use of the Gram stain in microbiology

Biotech. Histochem.

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.

Secretion and subcellular localizations of bacterial proteins: a semantic awareness issue

Trends Microbiol.

Discovery of new biosynthetic pathways: the lipid A story

J. Lipid Res.

Transport of lipopolysaccharide across the cell envelope: the long road of discovery

Nat. Rev. Microbiol.

The lipopolysaccharide transport system of Gram-negative bacteria

Biochim. Biophys. Acta

Biogenesis of outer membranes in Gram-negative bacteria

Biosci. Biotechnol. Biochem.

Rooting the tree of life by transition analyses

Biol. Direct

Deep phylogeny, ancestral groups and the four ages of life

Philos. Trans. R. Soc. B Biol. Sci.

The uncultured microbial majority

Annu. Rev. Microbiol.

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

Review
A phylum level perspective on bacterial cell envelope architecture

The structure and biological characteristics of the Spirochaeta aurantia outer membrane glycolipid LGL_B