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Sporulation, bacterial cell envelopes and the origin of life

Abstract

Electron cryotomography (ECT) enables the 3D reconstruction of intact cells in a near-native state. Images produced by ECT have led to the proposal that an ancient sporulation-like event gave rise to the second membrane in diderm bacteria. Tomograms of sporulating monoderm and diderm bacterial cells show how sporulation can lead to the generation of diderm cells. Tomograms of Gram-negative and Gram-positive cell walls and purified sacculi suggest that they are more closely related than previously thought and support the hypothesis that they share a common origin. 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. One explanation for this model is that during the cataclysmic transitions of the early Earth, cellular evolution may have gone through a bottleneck in which only spores survived, which implies that the last bacterial common ancestor was a spore.

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Figure 1: Sporulation in Gram-positive and Gram-negative bacteria.
Figure 2: Model for how the outer membrane arose as a byproduct of sporulation and how losses then led to the diversity of modern bacterial cell plans.
Figure 3: Peptidoglycan remodelling during sporulation.
Figure 4: Rooted phylogenetic trees that represent relationships between bacterial phyla.

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Acknowledgements

Cryotomography in the Jensen laboratory is supported, in part, by the US National Institutes of Health (including grant RO1 GM101425), the Howard Hughes Medical institute (HHMI) and the Beckman Institute at California Institute of Technology (Caltech), Pasadena, USA. Further support for this publication came from the John Templeton Foundation. The opinions expressed in this publication are those of the authors and do not necessarily reflect the views of the John Templeton Foundation. The authors thank C. Cleland, T. Nordheim, L. Brengman, K. Willford and J. Eisen for helpful discussions about the early Earth and possible roots of the tree of life.

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Tocheva, E., Ortega, D. & Jensen, G. Sporulation, bacterial cell envelopes and the origin of life. Nat Rev Microbiol 14, 535–542 (2016). https://doi.org/10.1038/nrmicro.2016.85

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