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  • Review Article
  • Published:

The Bacillus subtilis endospore: assembly and functions of the multilayered coat

Nature Reviews Microbiology volume 11, pages 33–44 (2013)Cite this article

Subjects

Key Points

  • The Bacillus subtilis spore coat is a multilayered protective structure composed of more than 70 different proteins.

  • In addition to its protective role, the spore coat influences the process of spore germination and defines the type of interactions that spores can establish with various surfaces in the environment.

  • Fluorescence microscopy in combination with high-resolution image analysis has produced a spatially scaled coat protein interaction network indicating that the coat is organized into four distinct layers. These studies led to the discovery of the outermost layer of the coat in B. subtilis, referred to as the spore crust.

  • Time course analyses of spore coat assembly have revealed that two main steps can be distinguished in coat morphogenesis: the initial recruitment of proteins to the spore surface as a scaffold cap, followed by spore encasement in a series of successive waves.

  • Coat assembly is regulated at the transcriptional level by the sequential expression of individual coat genes and at the protein level by a small group of coat morphogenetic proteins that coordinate both the recruitment of coat proteins to specific coat layers and spore encasement.

Abstract

Sporulation in Bacillus subtilis involves an asymmetric cell division followed by differentiation into two cell types, the endospore and the mother cell. The endospore coat is a multilayered shell that protects the bacterial genome during stress conditions and is composed of dozens of proteins. Recently, fluorescence microscopy coupled with high-resolution image analysis has been applied to the dynamic process of coat assembly and has shown that the coat is organized into at least four distinct layers. In this Review, we provide a brief summary of B. subtilis sporulation, describe the function of the spore surface layers and discuss the recent progress that has improved our understanding of the structure of the endospore coat and the mechanisms of coat assembly.

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Figure 1: The sporulation and germination cycle in Bacillus subtilis.
Figure 2: Spore ultrastructure.
Figure 3: The coat genetic interaction network.
Figure 4: A model for coat morphogenesis: successive waves of spore encasement.

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Acknowledgements

We apologize to colleagues whose work could not be cited in full owing to space limitations. Work in P.E.'s laboratory is supported by grant GM081571 from the US National Institutes of Health (NIH). Work in A.D.'s laboratory is supported by NIH grants R21AI097934 and R01AI093493, and HDTRA1-11-1-0051 from the US Department of Defense.

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  1. Department of Biology, Center for Genomics and Systems Biology, New York University, New York, 10003, New York, USA

    Peter T. McKenney & Patrick Eichenberger

  2. Department of Microbiology and Immunology, Stritch School of Medicine, Loyola University Chicago, Maywood, 60153, Illinois, USA

    Adam Driks

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Glossary

Sporulation

The developmental process of spore formation.

Endospores

Metabolically dormant cells composed of a partially dehydrated central core (containing the genome) surrounded by several concentrically arranged protective layers. An endospore develops inside a mother cell.

Mother cell

The larger of the two compartments formed by asymmetric division of the sporulating cell, it synthesizes most of the building blocks required to assemble the endospore protective structures and lyses at the end of sporulation, releasing the spore into the environment.

Forespore

The smaller of the two compartments that are formed by asymmetric division of the sporulating cell. It matures into an endospore.

Coat

A spore protective structure, which is made up of dozens of proteins. It is usually multilayered, consisting of inner and outer layers.

Sporangium

A vessel in which spores are formed. In endospore formation it refers to a cell that has entered sporulation by dividing asymmetrically.

Engulfment

The morphological transition in sporulation during which the mother cell swallows the forespore in a phagocytosis-like process involving membrane migration. After engulfment is complete, the forespore becomes a cell within the mother cell cytoplasm.

Cortex

A spore protective structure composed of peptidoglycan. It is assembled between the inner and outer forespore membranes.

Crust

The outermost layer of the coat in Bacillus subtilis. It closely follows the contours of the outer coat.

Exosporium

The outermost structure of the spore in several species. It is a protein (and, in at least some cases, a glycoprotein) layer separated from the outer coat by a large gap of irregular width referred to as the interspace.

Bacteriovores

Free-living heterotrophs that feed on bacteria.

Lamellae

The characteristic alternating dark and light rings of the inner coat that are visible by electron microscopy.

Encasement

The morphological transition in spore coat assembly from a cap of coat proteins on the mother cell proximal pole of the forespore to a symmetric distribution around the circumference of the spore.

Injectisomes

In Gram-negative bacteria, a family of secretion systems that have a molecular architecture homologous to flagella.

Natto

A Japanese dish of cooked soy beans fermented by a strain of Bacillus subtilis. It has a pungent aroma and a unique texture.

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McKenney, P., Driks, A. & Eichenberger, P. The Bacillus subtilis endospore: assembly and functions of the multilayered coat. Nat Rev Microbiol 11, 33–44 (2013). https://doi.org/10.1038/nrmicro2921

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