Review Article | Published:

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

Nature Reviews Microbiology volume 11, pages 3344 (2013) | Download Citation

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.

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.

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References

  1. 1.

    & Prokaryotic Development (ASM Press, 2000).

  2. 2.

    Untersuchungen über Bacterien. IV. Beiträge zur Biologie der Bacillen. Beiträge Biol. Pflanzen 7, 249–276 (1877). Along with Koch (below), this paper contains the first (and highly prescient) description of sporulation.

  3. 3.

    Untersuchungen über Bacterien V: Die Aetiologie der Milzbrand-Krankheit, begründet auf die Entwicklungsgeschichte der Bacillus anthracis. Beiträge Biol. Pflanzen 7, 277–308 (1877).

  4. 4.

    , , , & Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol. Mol. Biol. Rev. 64, 548–572 (2000).

  5. 5.

    , & Preservation records of micro-organisms: evidence of the tenacity of life. Microbiology 140, 2513–2529 (1994).

  6. 6.

    Longevity of micro-organisms. Nature 195, 643–646 (1962).

  7. 7.

    & La longévité des spores de B. anthracis (premier vaccin de Pasteur). Ann. Inst. Pasteur 87, 215–217 (1954).

  8. 8.

    , & Hierarchical evolution of the bacterial sporulation network. Curr. Biol. 20, R735–R745 (2010).

  9. 9.

    et al. Genomic determinants of sporulation in Bacilli and Clostridia: towards the minimal set of sporulation-specific genes. Environ. Microbiol. 14, 2870–2890 (2012). A comprehensive study of sporulation gene conservation among endospore formers.

  10. 10.

    , & Ecology and genomics of Bacillus subtilis. Trends Microbiol. 16, 269–275 (2008).

  11. 11.

    et al. Life in hot carbon monoxide: the complete genome sequence of Carboxydothermus hydrogenoformans Z-2901. PLoS Genet. 1, e65 (2005).

  12. 12.

    et al. A constant flux of diverse thermophilic bacteria into the cold Arctic seabed. Science 325, 1541–1544 (2009).

  13. 13.

    et al. Diversity of the human intestinal microbial flora. Science 308, 1635–1638 (2005).

  14. 14.

    & Evidence that entry into sporulation in Bacillus subtilis is governed by a gradual increase in the level and activity of the master regulator Spo0A. Genes Dev. 19, 2236–2244 (2005).

  15. 15.

    et al. The Spo0A regulon of Bacillus subtilis. Mol. Microbiol. 50, 1683–1701 (2003).

  16. 16.

    Specialized peptidoglycan of the bacterial endospore: the inner wall of the lockbox. Cell. Mol. Life Sci. 59, 426–433 (2002).

  17. 17.

    & Structure, assembly, and function of the spore surface layers. Ann. Rev. Microbiol. 61, 555–588 (2007). A thorough review that includes a comprehensive list of coat proteins in B. subtilis and B. anthracis.

  18. 18.

    The Bacillus anthracis spore. Mol. Aspects Med. 30, 368–373 (2009).

  19. 19.

    , , , & Spore cortex formation in Bacillus subtilis is regulated by accumulation of peptidoglycan precursors under the control of sigma K. Mol. Microbiol. 65, 1582–1594 (2007).

  20. 20.

    & Bacillus subtilis homologs of MviN (MurJ), the putative Escherichia coli lipid II flippase, are not essential for growth. J. Bacteriol. 191, 6020–6028 (2009).

  21. 21.

    & Dynamics of spore coat morphogenesis in Bacillus subtilis. Mol. Microbiol. 83, 245–260 (2012). This study ties the phenomenon of spore encasement to the regulation of expression of individual spore coat genes.

  22. 22.

    & Structure and morphogenesis of the bacterial spore coat. Bacteriol. Rev. 40, 360–402 (1976).

  23. 23.

    , & The composition and structure of bacterial spores. J. Cell Biol. 16, 579–592 (1963).

  24. 24.

    et al. Peptidoglycan remodeling and conversion of an inner membrane into an outer membrane during sporulation. Cell 146, 799–812 (2011).

  25. 25.

    et al. A distance-weighted interaction map reveals a previously uncharacterized layer of the Bacillus subtilis spore coat. Curr. Biol. 20, 934–938 (2010).

  26. 26.

    , , & The ExsY protein is required for complete formation of the exosporium of Bacillus anthracis. J. Bacteriol. 188, 7440–7448 (2006).

  27. 27.

    et al. Morphogenesis of the Bacillus anthracis spore. J. Bacteriol. 189, 691–705 (2007).

  28. 28.

    et al. Bacillus anthracis spores of the bclA mutant exhibit increased adherence to epithelial cells, fibroblasts, and endothelial cells but not to macrophages. Infect. Immun. 75, 4498–4505 (2007).

  29. 29.

    , , , & Bacillus anthracis and Bacillus subtilis spore surface properties and transport. Colloids Surf. B Biointerfaces 76, 512–518 (2010).

  30. 30.

    et al. Surface architecture of endospores of the Bacillus cereus/anthracis/thuringiensis family at the subnanometer scale. Proc. Natl Acad. Sci. USA 108, 16014–16019 (2011). This study provides a high-resolution characterization of the exosporium structure, revealing a crystalline layer made of a honeycomb-like array of cups.

  31. 31.

    et al. Surface layers of Clostridium difficile endospores. J. Bacteriol. 193, 6461–6470 (2011).

  32. 32.

    I will survive: DNA protection in bacterial spores. Trends Microbiol. 15, 172–180 (2007).

  33. 33.

    , , & CotA of Bacillus subtilis is a copper-dependent laccase. J. Bacteriol. 183, 5426–5430 (2001).

  34. 34.

    & Color me bad: microbial pigments as virulence factors. Trends Microbiol. 17, 406–413 (2009).

  35. 35.

    & Synthesis and assembly of fungal melanin. Appl. Microbiol. Biotechnol. 93, 931–940 (2012).

  36. 36.

    , & The Bacillus subtilis spore coat provides “eat resistance” during phagocytic predation by the protozoan Tetrahymena thermophila. Proc. Natl Acad. Sci. USA 103, 165–170 (2006).

  37. 37.

    & Role of spore coat proteins in the resistance of Bacillus subtilis spores to Caenorhabditis elegans predation. J. Bacteriol. 190, 6197–6203 (2008).

  38. 38.

    , , & Protozoal digestion of coat-defective Bacillus subtilis spores produces “rinds” composed of insoluble coat protein. Appl. Environ. Microbiol. 74, 5875–5881 (2008).

  39. 39.

    , & Germination of spores of Bacillales and Clostridiales species: mechanisms and proteins involved. Trends Microbiol. 19, 85–94 (2011).

  40. 40.

    , , & A eukaryotic-like Ser/Thr kinase signals bacteria to exit dormancy in response to peptidoglycan fragments. Cell 135, 486–496 (2008).

  41. 41.

    Bacillus subtilis spore coat. Microbiol. Mol. Biol. Rev. 63, 1–20 (1999).

  42. 42.

    & Studies on the spores of aerobic bacteria. I. The occurrence of alanine racemase. J. Bacteriol. 65, 160–166 (1953).

  43. 43.

    , , & Identification of the immunodominant protein and other proteins of the Bacillus anthracis exosporium. J. Bacteriol. 185, 1903–1910 (2003).

  44. 44.

    , , & Genes of Bacillus cereus and Bacillus anthracis encoding proteins of the exosporium. J. Bacteriol. 185, 3373–3378 (2003).

  45. 45.

    , , & The spore-specific alanine racemase of Bacillus anthracis and its role in suppressing germination during spore development. J. Bacteriol. 191, 1303–1310 (2009).

  46. 46.

    , & Gene cloning and characterization of a second alanine racemase from Bacillus subtilis encoded by yncD. FEMS Microbiol. Lett. 283, 69–74 (2008).

  47. 47.

    et al. Analysis of the effects of a gerP mutation on the germination of spores of Bacillus subtilis. J. Bacteriol. 194, 5749–5758 (2012).

  48. 48.

    , , , & Analysis of spore cortex lytic enzymes and related proteins in Bacillus subtilis endospore germination. Microbiology 148, 2383–2392 (2002).

  49. 49.

    & Localization of the cortex lytic enzyme CwlJ in spores of Bacillus subtilis. J. Bacteriol. 184, 1219–1224 (2002).

  50. 50.

    & The Bacillus anthracis SleL (YaaH) protein is an N-acetylglucosaminidase involved in spore cortex depolymerization. J. Bacteriol. 190, 7601–7607 (2008).

  51. 51.

    , , & Localization of proteins to different layers and regions of Bacillus subtilis spore coats. J. Bacteriol. 192, 518–524 (2010).

  52. 52.

    , , & LysM, a widely distributed protein motif for binding to (peptido)glycans. Mol. Microbiol. 68, 838–847 (2008).

  53. 53.

    , , & Small proteins link coat and cortex assembly during sporulation in Bacillus subtilis. Mol. Microbiol. 84, 682–696 (2012).

  54. 54.

    & Ultrastructural analysis during germination and outgrowth of Bacillus subtilis spores. J. Bacteriol. 120, 475–481 (1974).

  55. 55.

    , & Non-uniform assembly of the Bacillus anthracis exosporium and a bottle cap model for spore germination and outgrowth. Mol. Microbiol. 64, 359–367 (2007). A description of the polarity of the spore envelope and a model for spore germination and outgrowth.

  56. 56.

    & Comparative ultrastructure of selected aerobic spore-forming bacteria: a freeze-etching study. Bacteriol. Rev. 33, 346–378 (1969).

  57. 57.

    et al. Do mycobacteria produce endospores? Proc. Natl Acad. Sci. USA 107, 878–881 (2010).

  58. 58.

    et al. Clostridium taeniosporum spore ribbon-like appendage structure, composition and genes. Mol. Microbiol. 63, 629–643 (2007).

  59. 59.

    et al. Role played by exosporium glycoproteins in the surface properties of Bacillus cereus spores and in their adhesion to stainless steel. Appl. Environ. Microbiol. 77, 4905–4911 (2011).

  60. 60.

    , , , & Decontamination of a hard surface contaminated with Bacillus anthracisΔSterne and B. anthracis Ames spores using electrochemically generated liquid-phase chlorine dioxide (eClO2). J. Appl. Microbiol. 111, 1057–1064 (2011).

  61. 61.

    , & Populations of spore-forming bacteria in an acid forest soil, with special reference to Bacillus subtilis. J. Gen. Microbiol. 8, 183–190 (1974).

  62. 62.

    Roles of Bacillus endospores in the environment. Cell. Mol. Life Sci. 59, 410–416 (2002).

  63. 63.

    , , & Genes encoding spore coat polypeptides from Bacillus subtilis. J. Mol. Biol. 196, 1–10 (1987).

  64. 64.

    , , & Cloning and characterization of a gene required for assembly of the Bacillus subtilis spore coat. J. Bacteriol. 175, 1705–1716 (1993).

  65. 65.

    , , & Gene encoding a morphogenic protein required in the assembly of the outer coat of the Bacillus subtilis endospore. Genes Dev. 2, 1047–1054 (1988).

  66. 66.

    et al. Proteomic analysis of the spore coats of Bacillus subtilis and Bacillus anthracis. J. Bacteriol. 185, 1443–1454 (2003).

  67. 67.

    et al. Proteomics characterization of novel spore proteins of Bacillus subtilis. Microbiology 148, 3971–3982 (2002).

  68. 68.

    et al. The program of gene transcription for a single differentiating cell type during sporulation in Bacillus subtilis. PLoS Biol. 2, e328 (2004).

  69. 69.

    et al. The Bacillus subtilis spore coat protein interaction network. Mol. Microbiol. 59, 487–502 (2006).

  70. 70.

    et al. Gel-free proteomic identification of the Bacillus subtilis insoluble spore coat protein fraction. Proteomics 11, 4541–4550 (2011).

  71. 71.

    , , & Use of green fluorescent protein for visualization of cell-specific gene expression and subcellular protein localization during sporulation in Bacillus subtilis. J. Bacteriol. 177, 5906–5911 (1995).

  72. 72.

    et al. The σE regulon and the identification of additional sporulation genes in Bacillus subtilis. J. Mol. Biol. 327, 945–972 (2003).

  73. 73.

    & Genetic aspects of bacterial endospore formation. Bacteriol. Rev. 40, 908–962 (1976).

  74. 74.

    et al. An unusually small gene required for sporulation by Bacillus subtilis. Mol. Microbiol. 9, 761–771 (1993).

  75. 75.

    , & Characterization of spoIVA, a sporulation gene involved in coat morphogenesis in Bacillus subtilis. J. Bacteriol. 174, 575–585 (1992).

  76. 76.

    , , & Characterization of the yrbA gene of Bacillus subtilis, involved in resistance and germination of spores. J. Bacteriol. 181, 4986–4994 (1999).

  77. 77.

    , , & Morphogenetic proteins SpoVID and SafA form a complex during assembly of the Bacillus subtilis spore coat. J. Bacteriol. 182, 1828–1833 (2000).

  78. 78.

    , , , & Subcellular localization of proteins involved in the assembly of the spore coat of Bacillus subtilis. Genes Dev. 8, 234–244 (1994). This article proposes a seminal model for coat assembly.

  79. 79.

    , , & Proteins involved in formation of the outermost layer of Bacillus subtilis spores. J. Bacteriol. 193, 4075–4080 (2011).

  80. 80.

    , , , & Identification of proteins in the exosporium of Bacillus anthracis. Microbiology 150, 355–363 (2004).

  81. 81.

    , , , & Ruthenium red staining for ultrastructural visualization of a glycoprotein layer surrounding the spore of Bacillus anthracis and Bacillus subtilis. J. Microbiol. Methods 58, 23–30 (2004). This study introduces the use of ruthenium red staining to analyse the outermost layer of the spore.

  82. 82.

    et al. SpoVM, a small protein essential to development in Bacillus subtilis, interacts with the ATP-dependent protease FtsH. J. Bacteriol. 179, 5534–5542 (1997).

  83. 83.

    et al. The coat morphogenetic protein SpoVID is necessary for spore encasement in Bacillus subtilis. Mol. Microbiol. 74, 634–649 (2009).

  84. 84.

    , , & SpoVID guides SafA to the spore coat in Bacillus subtilis. J. Bacteriol. 183, 3041–3049 (2001).

  85. 85.

    , , & Interaction between coat morphogenetic proteins SafA and SpoVID. J. Bacteriol. 188, 7731–7741 (2006).

  86. 86.

    & A four-dimensional view of assembly of a morphogenetic protein during sporulation in Bacillus subtilis. J. Bacteriol. 181, 781–790 (1999).

  87. 87.

    , & Peptide anchoring spore coat assembly to the outer forespore membrane in Bacillus subtilis. Mol. Microbiol. 62, 1547–1557 (2006).

  88. 88.

    , & Dynamic patterns of subcellular protein localization during spore coat morphogenesis in Bacillus subtilis. J. Bacteriol. 186, 4441–4448 (2004).

  89. 89.

    , & Visualization of the subcellular location of sporulation proteins in Bacillus subtilis using immunofluorescence microscopy. Mol. Microbiol. 18, 459–470 (1995).

  90. 90.

    & Subcellular localization of a small sporulation protein in Bacillus subtilis. J. Bacteriol. 185, 1391–1398 (2003).

  91. 91.

    , & Interactions between Bacillus subtilis early spore coat morphogenetic proteins. FEMS Microbiol. Lett. 299, 74–85 (2009).

  92. 92.

    et al. Physical interaction between coat morphogenetic proteins SpoVID and CotE is necessary for spore encasement in Bacillus subtilis. J. Bacteriol. 194, 4941–4950 (2012).

  93. 93.

    & ATP-driven self-assembly of a morphogenetic protein in Bacillus subtilis. Mol. Cell 31, 406–414 (2008).

  94. 94.

    & Functional analysis of the Bacillus subtilis morphogenetic spore coat protein CotE. Mol. Microbiol. 42, 1107–1120 (2001).

  95. 95.

    , , , & Searching for protein-protein interactions within the Bacillus subtilis spore coat. J. Bacteriol. 191, 3212–3219 (2009).

  96. 96.

    , & Switch protein alters specificity of RNA polymerase containing a compartment-specific sigma factor. Science 243, 526–529 (1989).

  97. 97.

    , & Cloning and characterization of a cluster of genes encoding polypeptides present in the insoluble fraction of the spore coat of Bacillus subtilis. J. Bacteriol. 175, 3757–3766 (1993).

  98. 98.

    , , , & Regulation of the transcription of a cluster of Bacillus subtilis spore coat genes. J. Mol. Biol. 240, 405–415 (1994).

  99. 99.

    & Cascade regulation of spore coat gene expression in Bacillus subtilis. J. Mol. Biol. 212, 645–660 (1990).

  100. 100.

    & Transglutaminase-mediated cross-linking of GerQ in the coats of Bacillus subtilis spores. J. Bacteriol. 186, 5567–5575 (2004).

  101. 101.

    , , , & Bacillus subtilis spore coat assembly requires cotH gene expression. J. Bacteriol. 178, 4375–4380 (1996).

  102. 102.

    et al. Characterization of the Bacillus subtilis spore morphogenetic coat protein CotO. J. Bacteriol. 187, 8278–8290 (2005).

  103. 103.

    et al. Organization and evolution of the cotG and cotH genes of Bacillus subtilis. J. Bacteriol. 193, 6664–6673 (2011).

  104. 104.

    et al. CotC-CotU heterodimerization during assembly of the Bacillus subtilis spore coat. J. Bacteriol. 190, 1267–1275 (2008).

  105. 105.

    , & Bacterial nanomachines: the flagellum and type III injectisome. Cold Spring Harb. Perspect. Biol. 2, a000299 (2010).

  106. 106.

    & Exosporium and spore coat formation in Bacillus cereus T. J. Bacteriol. 115, 1179–1190 (1973).

  107. 107.

    & Targeting of the BclA and BclB proteins to the Bacillus anthracis spore surface. Mol. Microbiol. 70, 421–434 (2008).

  108. 108.

    Alternatives to binary fission in bacteria. Nature Rev. Microbiol. 3, 214–224 (2005).

  109. 109.

    et al. Partial penetrance facilitates developmental evolution in bacteria. Nature 460, 510–514 (2009).

  110. 110.

    & Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium. Nature Rev. Microbiol. 7, 36–49 (2009).

  111. 111.

    & Comparative biology of prokaryotic resting cells. Adv. Microb. Physiol. 9, 153–224 (1973).

  112. 112.

    , , , & Spore formation in Myxococcus xanthus is tied to cytoskeleton functions and polysaccharide spore coat deposition. Mol. Microbiol. 83, 486–505 (2012).

  113. 113.

    , & Versatile microbial surface-display for environmental remediation and biofuels production. Trends Microbiol. 16, 181–188 (2008).

  114. 114.

    , , & Oral vaccine delivery by recombinant spore probiotics. Int. Rev. Immunol. 28, 487–505 (2009).

  115. 115.

    et al. Immunization with Bacillus spores expressing toxin A peptide repeats protects against infection with Clostridium difficile strains producing toxins A and B. Infect. Immun. 79, 2295–2302 (2011).

  116. 116.

    et al. Sublingual immunization with an engineered Bacillus subtilis strain expressing tetanus toxin fragment C induces systemic and mucosal immune responses in piglets. Microbes Infect. 14, 447–456 (2012).

  117. 117.

    et al. Adsorption of beta-galactosidase of Alicyclobacillus acidocaldarius on wild type and mutants spores of Bacillus subtilis. Microb. Cell Fact. 11, 100 (2012).

  118. 118.

    , , & Geometric cue for protein localization in a bacterium. Science 323, 1354–1357 (2009). This study reveals that the coat morphogenetic protein SpoVM has the ability to recognize positive membrane curvature.

  119. 119.

    & Macromolecules that prefer their membranes curvy. Mol. Microbiol. 76, 822–832 (2010).

  120. 120.

    & Conserved functions of membrane active GTPases in coated vesicle formation. Science 325, 1217–1220 (2009).

  121. 121.

    , & A unifying mechanism accounts for sensing of membrane curvature by BAR domains, amphipathic helices and membrane-anchored proteins. Semin. Cell Dev. Biol. 21, 381–390 (2010).

  122. 122.

    et al. A novel lipolytic enzyme, YcsK (LipC), located in the spore coat of Bacillus subtilis, is involved in spore germination. J. Bacteriol. 189, 2369–2375 (2007).

  123. 123.

    , & Structural and germination defects of Bacillus subtilis spores with altered contents of a spore coat protein. J. Bacteriol. 173, 6618–6625 (1991).

  124. 124.

    , , , & Assembly of an oxalate decarboxylase produced under σK control into the Bacillus subtilis spore coat. J. Bacteriol. 186, 1462–1474 (2004).

  125. 125.

    , & CotM of Bacillus subtilis, a member of the α-crystallin family of stress proteins, is induced during development and participates in spore outer coat formation. J. Bacteriol. 179, 1887–1897 (1997).

  126. 126.

    et al. A spore coat protein, CotS, of Bacillus subtilis is synthesized under the regulation of σK and GerE during development and is located in the inner coat layer of spores. J. Bacteriol. 180, 2968–2974 (1998).

  127. 127.

    et al. Genomics, evolution, and crystal structure of a new family of bacterial spore kinases. Proteins 78, 1470–1482 (2010).

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

    • Peter T. McKenney
    •  & Patrick Eichenberger
  2. Department of Microbiology and Immunology, Stritch School of Medicine, Loyola University Chicago, Maywood, Illinois 60153, USA.

    • Adam Driks

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The authors declare no competing financial interests.

Corresponding author

Correspondence to Patrick Eichenberger.

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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