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Sporulation in Bacteria: Beyond the Standard Model

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  • Authors: Elizabeth A. Hutchison1, David A. Miller2, Esther R. Angert3
  • Editors: Patrick Eichenberger4, Adam Driks5
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Biology, SUNY Geneseo, Geneseo, NY 14454; 2: Department of Microbiology, Medical Instill Development, New Milford, CT 06776; 3: Department of Microbiology, Cornell University, Ithaca, NY 14853; 4: New York University, New York, NY; 5: Loyola University Medical Center, Maywood, IL
  • Source: microbiolspec October 2014 vol. 2 no. 5 doi:10.1128/microbiolspec.TBS-0013-2012
  • Received 13 November 2012 Accepted 27 August 2014 Published 03 October 2014
  • Esther R. Angert, era23@cornell.edu
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  • Abstract:

    Endospore formation follows a complex, highly regulated developmental pathway that occurs in a broad range of . Although has served as a powerful model system to study the morphological, biochemical, and genetic determinants of sporulation, fundamental aspects of the program remain mysterious for other genera. For example, it is entirely unknown how most lineages within the regulate entry into sporulation. Additionally, little is known about how the sporulation pathway has evolved novel spore forms and reproductive schemes. Here, we describe endospore and internal offspring development in diverse and outline progress in characterizing these programs. Moreover, comparative genomics studies are identifying highly conserved sporulation genes, and predictions of sporulation potential in new isolates and uncultured bacteria can be made from these data. One surprising outcome of these comparative studies is that core regulatory and some structural aspects of the program appear to be universally conserved. This suggests that a robust and sophisticated developmental framework was already in place in the last common ancestor of all extant that produce internal offspring or endospores. The study of sporulation in model systems beyond will continue to provide key information on the flexibility of the program and provide insights into how changes in this developmental course may confer advantages to cells in diverse environments.

  • Citation: Hutchison E, Miller D, Angert E. 2014. Sporulation in Bacteria: Beyond the Standard Model. Microbiol Spectrum 2(5):TBS-0013-2012. doi:10.1128/microbiolspec.TBS-0013-2012.

Key Concept Ranking

Programmed Cell Death
0.49050528
Peyer's Patches
0.48549184
Cellular Processes
0.416553
Genetic Elements
0.40671062
0.49050528

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/content/journal/microbiolspec/10.1128/microbiolspec.TBS-0013-2012
2014-10-03
2017-09-25

Abstract:

Endospore formation follows a complex, highly regulated developmental pathway that occurs in a broad range of . Although has served as a powerful model system to study the morphological, biochemical, and genetic determinants of sporulation, fundamental aspects of the program remain mysterious for other genera. For example, it is entirely unknown how most lineages within the regulate entry into sporulation. Additionally, little is known about how the sporulation pathway has evolved novel spore forms and reproductive schemes. Here, we describe endospore and internal offspring development in diverse and outline progress in characterizing these programs. Moreover, comparative genomics studies are identifying highly conserved sporulation genes, and predictions of sporulation potential in new isolates and uncultured bacteria can be made from these data. One surprising outcome of these comparative studies is that core regulatory and some structural aspects of the program appear to be universally conserved. This suggests that a robust and sophisticated developmental framework was already in place in the last common ancestor of all extant that produce internal offspring or endospores. The study of sporulation in model systems beyond will continue to provide key information on the flexibility of the program and provide insights into how changes in this developmental course may confer advantages to cells in diverse environments.

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Image of FIGURE 1

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FIGURE 1

Bacteria that produce endospores or intracellular offspring exhibit a wide variety of morphological phenotypes. Phase-contrast microscopy is often used to identify mature endospores (A to C and E) as these highly mineralized cells appear phase-bright. In this image of , the caret (>) indicates a cell that is not dividing or sporulating and the asterisk (*) indicates a cell undergoing binary fission. All other cells in the image contain a phase-bright endospore. frequently produces phase-bright endospores at both ends of the cell. Image courtesy of Avigdor Eldar and Michael Elowitz, California Institute of Technology. In this image of , the arrows indicate cells with seven endospores. The fluorescence micrograph of outlines cell membranes and spore coats stained with FM1-43. -like type C (cigar-shaped cell) and type J (elongated cells), each containing two phase-bright endospores. sp. type B with two internal daughter cells, stained with DAPI. Cellular DNA is located at the periphery of the cytoplasm in the mother cell and each offspring. Scanning electron micrograph (SEM) of the ileum lining from a rat reveals the epithelial surface densely populated with SFB. Arrow indicates a holdfast cell that has not yet elongated into a filament. Transmission electron micrograph (TEM) of a thin section through the gut wall reveals the structure of the SFB holdfast cell (indicated by an asterisk). TEMs illustrate the two possible fates for developing intracellular SFB: (I) two holdfast cells or (J) two endospores that are encased in a common coat (C), inner (I) and outer (O) cortex. Panel C reproduced from Siunov et al. ( 47 ) with permission from Society for General Microbiology. Panel E reproduced from Flint et al. ( 33 ) with permission from ASM Press. Panel F reproduced from Mendell et al. ( 93 ) with permission from the National Academy of Sciences, USA. Panels G and H reproduced from Erlandsen and Chase ( 69 ) with permission from the American Society for Nutrition. Panels I and J reproduced from Ferguson and Birch-Andersen ( 74 ) with permission from John Wiley and Sons. doi:10.1128/microbiolspec.TBS-0013-2012.f1

Source: microbiolspec October 2014 vol. 2 no. 5 doi:10.1128/microbiolspec.TBS-0013-2012
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FIGURE 2

Endospore development. In monosporic bacteria, complete division occurs at only one end of the developing sporangium , while bacteria that produce two endospores generally divide at both poles . In some lineages, such as the SFB and , engulfed forespores undergo division (not shown). Note that at least three chromosome copies are required to produce two viable endospores. Following endospore engulfment, cortex and coat layers develop, and upon endospore maturation, the mother cell lyses, releasing one (A) or two (B) endospores. doi:10.1128/microbiolspec.TBS-0013-2012.f2

Source: microbiolspec October 2014 vol. 2 no. 5 doi:10.1128/microbiolspec.TBS-0013-2012
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FIGURE 3

Life cycle of . Endospores germinate and, during outgrowth, a cell may undergo binary fission or immediately begin to sporulate by dividing at the poles . The forespores are engulfed , and the forespores may undergo binary fission to produce additional forespores . Forespores then elongate and develop into mature endospores . Figure reproduced from Ward and Angert ( 52 ) with permission from John Wiley and Sons. doi:10.1128/microbiolspec.TBS-0013-2012.f3

Source: microbiolspec October 2014 vol. 2 no. 5 doi:10.1128/microbiolspec.TBS-0013-2012
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FIGURE 4

Life cycle of SFB and sp. type B. (i) The SFB life cycle begins with a holdfast cell that is anchored to the intestinal epithelia (not shown). (ii) Holdfast cells elongate and divide into primary segments as the filament grows. (iii) At the start of development, cells in the filament divide again to produce secondary segments. (iv) Next, secondary segments divide asymmetrically, and then engulfment of the smaller cell (in grey) occurs, in a manner similar to that of other endosporeformers. Development progresses from the free end of the filament toward the holdfast. (v) Each engulfed offspring cell then forms into a crescent shape (vi) and then divides to either form two holdfast offspring cells per segment (inset, top) or develop into an endospore via formation of a spore cortex and coat (inset, bottom). (i) In sp. type B, twin offspring form by division at both cell poles. Engulfment occurs (ii to iii) and offspring cells elongate (iv). The offspring cells begin to produce their own offspring before they are released from the mother cell (v). doi:10.1128/microbiolspec.TBS-0013-2012.f4

Source: microbiolspec October 2014 vol. 2 no. 5 doi:10.1128/microbiolspec.TBS-0013-2012
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