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Terrabacteria: redefining bacterial envelope diversity, biogenesis and evolution

Nature Reviews Microbiology (2024)Cite this article

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Abstract

The bacterial envelope is one of the oldest and most essential cellular components and has been traditionally divided into Gram-positive (monoderm) and Gram-negative (diderm). Recent landmark studies have challenged a major paradigm in microbiology by inferring that the last bacterial common ancestor had a diderm envelope and that the outer membrane (OM) was lost repeatedly in evolution to give rise to monoderms. Intriguingly, OM losses appear to have occurred exclusively in the Terrabacteria, one of the two major clades of bacteria. In this Review, we present current knowledge about the Terrabacteria. We describe their diversity and phylogeny and then highlight the vast phenotypic diversity of the Terrabacteria cell envelopes, which display large deviations from the textbook examples of diderms and monoderms, challenging the classical Gram-positive–Gram-negative divide. We highlight the striking differences in the systems involved in OM biogenesis in Terrabacteria with respect to the classical diderm experimental models and how they provide novel insights into the diversity and biogenesis of the bacterial cell envelope. We also discuss the potential evolutionary steps that might have led to the multiple losses of the OM and speculate on how the very first OM might have emerged before the last bacterial common ancestor.

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Fig. 1: Diderm and monoderm cell envelope architectures as described in model organisms.
Fig. 2: Historical and current view of Terrabacteria diversity and redefinition of envelope types.
Fig. 3: Diversity of cell envelopes in Terrabacteria challenges the Gram-positive–Gram-negative divide.
Fig. 4: Outer membrane biogenesis and transport systems in E. coli and diderm Terrabacteria.
Fig. 5: Evolutionary scenarios for emergence and loss of the outer membrane.

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Acknowledgements

This work was supported by the Bettencourt-Schueller Foundation programme Impulscience (ENVOL) to S.G., the French National Research Agency (OM-LipAsy-CE44-008) to S.G. and C.B. and the French government Investissement d’Avenir Program, Laboratoire d’Excellence ‘Integrative Biology of Emerging Infectious Diseases’ (grant no. ANR-10-LABX-62-IBEID). B.B.B.’s PhD fellowship is supported by MENESR (Ministère Français de l’Education Nationale, de l’Enseignement Supérieur et de la Recherche), the Fondation pour la Recherche Médicale (FRM) and ANR-10-LABX-62-IBEID. B.B.B. wishes to thank H. Voedts and all members of the EBMC Unit for fruitful discussions during the preparation of this Review.

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  1. Evolutionary Biology of the Microbial Cell Laboratory, Institut Pasteur, Université Paris Cité, Paris, France

    Basile Beaud Benyahia, Najwa Taib & Simonetta Gribaldo

  2. Bioinformatics and Biostatistics Hub, Institut Pasteur, Université Paris Cité, Paris, France

    Najwa Taib

  3. Genetics of Biofilms Laboratory, Institut Pasteur, Université Paris Cité, Paris, France

    Christophe Beloin

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B.B.B. and N.T. researched data for the article. C.B. contributed to discussion of the content. B.B.B., N.T. and S.G. wrote the article. All authors reviewed and/or edited the manuscript before submission.

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Beaud Benyahia, B., Taib, N., Beloin, C. et al. Terrabacteria: redefining bacterial envelope diversity, biogenesis and evolution. Nat Rev Microbiol (2024). https://doi.org/10.1038/s41579-024-01088-0

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