One or two membranes? Diderm Firmicutes challenge the Gram‐positive/Gram‐negative divide

@article{Megrian2020OneOT,
  title={One or two membranes? Diderm Firmicutes challenge the Gram‐positive/Gram‐negative divide},
  author={Daniela Megrian and Najwa Taib and Jerzy Witwinowski and Christophe Beloin and Simonetta Gribaldo},
  journal={Molecular Microbiology},
  year={2020},
  volume={113},
  pages={659 - 671}
}
How, when and why the transition between cell envelopes with one membrane (Gram‐positives or monoderms) and two (Gram‐negative or diderms) occurred in Bacteria is a key unanswered question in evolutionary biology. Different hypotheses have been put forward, suggesting that either the monoderm or the diderm phenotype is ancestral. The existence of diderm members in the classically monoderm Firmicutes challenges the Gram‐positive/Gram‐negative divide and provides a great opportunity to tackle the… 
View on Wiley
onlinelibrary.wiley.com
28 Citations
Highly Influential Citations
2
Background Citations
8
Methods Citations
1
Results Citations
2

28 Citations

Citation Type

Citation Type

Genome-wide analysis of the Firmicutes illuminates the diderm/monoderm transition.
TLDR
A third and deep branching diderm clade, the Limnochordia, is highlighted, strengthening the hypothesis of a diderm ancestor and the occurrence of independent transitions leading to the monoderm phenotype, and mapping the presence/absence of OM markers onto the tree of Bacteria shows the overwhelming presence of diderm phyla and the non-monophyly of monoderman ones.
An ancient divide in outer membrane tethering systems in Bacteria
TLDR
An evolutionary scenario is proposed whereby the last common bacterial ancestor used a system based on OmpM, which was later replaced by one based on the lipoprotein Pal concomitantly to the emergence of the Lol machinery to address lipoproteins to the OM, with OmpA as a possible transition state.
An ancient divide in outer membrane tethering systems in bacteria suggests a mechanism for the diderm-to-monoderm transition.
TLDR
An in-depth analysis of the four known main OM-tethering systems across the Tree of Bacteria shows that the presence of such systems follows the ToB with a bimodal distribution matching the deepest phylogenetic divergence between Terrabacteria and Gracilicutes, and suggests a mechanism for OM loss and the multiple emergences of the monoderm phenotype from diderm ancestors.
Was the Last Bacterial Common Ancestor a Monoderm after All?
TLDR
It is suggested that all cultivated and characterized bacteria might have evolved from a common ancestor with a monoderm cell-wall architecture, which would indicate that the appearance of the outer membrane was not a unique event and that selective forces have led to the repeated adoption of such an architecture.
Autotransporters drive biofilm formation and auto-aggregation in the diderm Firmicute Veillonella parvula
TLDR
Type V secreted autotransporters -typically found in diderm bacteria-are the main determinants of V. parvula auto-aggregation and biofilm formation, and inactivation of the gene coding for a poorly characterized metal-dependent phosphohydrolase HD domain protein conserved in the Firmicutes and their closely related diderm phyla inhibits autOTransporter-mediated biofilm Formation.
Autotransporters Drive Biofilm Formation and Autoaggregation in the Diderm Firmicute Veillonella parvula
TLDR
It is shown that type V secreted autotransporters, typically found in diderm bacteria, are the main determinants of V. parvula biofilm formation capacity and inactivation of the gene coding for a poorly characterized metal-dependent phosphohydrolase HD domain protein conserved in the Firmicutes and their closely related diderm phyla inhibits autOTransporter-mediated biofilm Formation.
A dynamic, ring-forming MucB / RseB-like protein influences spore shape in Bacillus subtilis
TLDR
Functional diversification of the MucB / RseB protein domain between diderm and monoderm bacteria is suggested and SsdC appears to play a role in the proper assembly of the spore cortex, through connections to thespore coat.
Direct Observation of Conversion From Walled Cells to Wall-Deficient L-Form and Vice Versa in Escherichia coli Indicates the Essentiality of the Outer Membrane for Proliferation of L-Form Cells
TLDR
Results strongly suggest that wall-deficient E. coli cells require a rigid outer membrane to survive, but not too rigid to prevent them from changing cell shape.
Conservation and evolution of the sporulation gene set in diverse members of the Firmicutes
TLDR
It is shown that the core set of sporulation genes, defined previously through genome comparisons of several bacilli and clostridia, is conserved in a wide variety of spore-formers from several distinct lineages of Firmicutes.
A rooted phylogeny resolves early bacterial evolution
TLDR
A phylogenetic analysis models the evolution of 11,272 protein families in bacteria and identifies the likely evolutionary root, suggesting that the diversification of the Firmicutes, CPR, Acidobacteriota, and Proteobacteria is the oldest among extant bacterial phyla.
...
1
2
3
...

References

SHOWING 1-10 OF 82 REFERENCES
Phylogenomic analysis supports the ancestral presence of LPS-outer membranes in the Firmicutes
TLDR
The hypothesis that the LPS-OMs of Negativicutes and Halanaerobiales are remnants of an ancient diderm cell envelope that was present in the ancestor of the Firmicutes is supported, and that the monoderm phenotype in this phylum is a derived character that arose multiple times independently through OM loss.
Origin of diderm (Gram-negative) bacteria: antibiotic selection pressure rather than endosymbiosis likely led to the evolution of bacterial cells with two membranes
TLDR
There is no reliable evidence to support the endosymbiotic origin of double membrane bacteria, and many observations suggest that antibiotic selection pressure was an important selective force in prokaryotic evolution and that it likely played a central role in the evolution of diderm (Gram-negative) bacteria.
The Mycobacterial Cell Envelope: A Relict From the Past or the Result of Recent Evolution?
TLDR
A novel alternative hypothesis is proposed whereby the stepwise acquisition of core enzymatic functions may have allowed the sequential remodeling of the external cell membrane during the evolution of Actinobacteria and has led to the unique mycomembrane of slow-growing mycobacteria as the authors know it today.
Outer Membrane Proteome of Veillonella parvula: A Diderm Firmicute of the Human Microbiome
TLDR
The first experimental proteomic characterization of the cell envelope of a diderm Firmicute, producing an OM proteome of V. parvula, and provides important information on the role of OM components in the lifestyle of Veillonella, such as a possible gene cluster for O-antigen synthesis and a large number of adhesins.
A phylum level perspective on bacterial cell envelope architecture.
Sporulation, bacterial cell envelopes and the origin of life
TLDR
Mapping the distribution of cell envelope architectures onto a recent phylogenetic tree of life indicates that the diderm cell plan, and therefore the sporulation-like event that gave rise to it, must be very ancient.
Peptidoglycan Remodeling and Conversion of an Inner Membrane into an Outer Membrane during Sporulation
Cell envelope architecture in the Chloroflexi: a shifting frontline in a phylogenetic turf war.
TLDR
This Correspondence summarizes the compelling evidence that the Chloroflexi are in fact monoderm, i.e. have only a single cellular membrane.
Structure-functional analysis of the Dictyoglomus cell envelope.
A genomic update on clostridial phylogeny: Gram-negative spore formers and other misplaced clostridia.
TLDR
It is reaffirmed that 16S rRNA and ribosomal protein sequences are better indicators of evolutionary proximity than phenotypic traits, even such key ones as the structure of the cell envelope and Gram-staining pattern.
...
1
2
3
4
5
...