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Spore Peptidoglycan

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  • Authors: David L. Popham1, Casey B. Bernhards2
  • Editors: Patrick Eichenberger3, Adam Driks4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Biological Sciences, Life Sciences I, Virginia Tech, Blacksburg, VA 24061; 2: U.S. Army Edgewood Chemical Biological Center, Aberdeen Proving Ground, MD 21010; 3: New York University, New York, NY; 4: Loyola University Medical Center, Maywood, IL
  • Source: microbiolspec December 2015 vol. 3 no. 6 doi:10.1128/microbiolspec.TBS-0005-2012
  • Received 21 August 2012 Accepted 05 October 2015 Published 18 December 2015
  • David L. Popham, dpopham@vt.edu
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  • Abstract:

    Bacterial endospores possess multiple integument layers, one of which is the cortex peptidoglycan wall. The cortex is essential for the maintenance of spore core dehydration and dormancy and contains structural modifications that differentiate it from vegetative cell peptidoglycan and determine its fate during spore germination. Following the engulfment stage of sporulation, the cortex is synthesized within the intermembrane space surrounding the forespore. Proteins responsible for cortex synthesis are produced in both the forespore and mother cell compartments. While some of these proteins also contribute to vegetative cell wall synthesis, others are sporulation specific. In order for the bacterial endospore to germinate and resume metabolism, the cortex peptidoglycan must first be degraded through the action of germination-specific lytic enzymes. These enzymes are present, yet inactive, in the dormant spore and recognize the muramic-δ-lactam modification present in the cortex. Germination-specific lytic enzymes across and share this specificity determinant, which ensures that the spore cortex is hydrolyzed while the vegetative cell wall remains unharmed. species tend to possess two redundant enzymes, SleB and CwlJ, capable of sufficient cortex degradation, while the clostridia have only one, SleC. Additional enzymes are often present that cannot initiate the cortex degradation process, but which can increase the rate of release of small fragments into the medium. Between the two families, the enzymes also differ in the enzymatic activities they possess and the mechanisms acting to restrict their activation until germination has been initiated.

  • Citation: Popham D, Bernhards C. 2015. Spore Peptidoglycan. Microbiol Spectrum 3(6):TBS-0005-2012. doi:10.1128/microbiolspec.TBS-0005-2012.

Key Concept Ranking

High-Performance Liquid Chromatography
0.4604028
Integral Membrane Proteins
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Transmission Electron Microscopy
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/content/journal/microbiolspec/10.1128/microbiolspec.TBS-0005-2012
2015-12-18
2017-11-21

Abstract:

Bacterial endospores possess multiple integument layers, one of which is the cortex peptidoglycan wall. The cortex is essential for the maintenance of spore core dehydration and dormancy and contains structural modifications that differentiate it from vegetative cell peptidoglycan and determine its fate during spore germination. Following the engulfment stage of sporulation, the cortex is synthesized within the intermembrane space surrounding the forespore. Proteins responsible for cortex synthesis are produced in both the forespore and mother cell compartments. While some of these proteins also contribute to vegetative cell wall synthesis, others are sporulation specific. In order for the bacterial endospore to germinate and resume metabolism, the cortex peptidoglycan must first be degraded through the action of germination-specific lytic enzymes. These enzymes are present, yet inactive, in the dormant spore and recognize the muramic-δ-lactam modification present in the cortex. Germination-specific lytic enzymes across and share this specificity determinant, which ensures that the spore cortex is hydrolyzed while the vegetative cell wall remains unharmed. species tend to possess two redundant enzymes, SleB and CwlJ, capable of sufficient cortex degradation, while the clostridia have only one, SleC. Additional enzymes are often present that cannot initiate the cortex degradation process, but which can increase the rate of release of small fragments into the medium. Between the two families, the enzymes also differ in the enzymatic activities they possess and the mechanisms acting to restrict their activation until germination has been initiated.

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Figures

Image of FIGURE 1
FIGURE 1

Structural elements of dormant and germinating spores. The dormant spore (left) has a densely staining dehydrated core (Co), surrounded by the inner forespore membrane, the poorly staining cortex PG (Cx), and multiple coat layers (Ct). Within the expanded, rehydrated core of the partially germinated spore (right), the nucleoid material is visible. The cortex and coats have expanded, and the cortex now binds some stain, presumably because of reactive groups generated by cortex degradation. Both spores are photographed at the same magnification. Bar = 0.25 µm. doi:10.1128/microbiolspec.TBS-0005-2012.f1

Source: microbiolspec December 2015 vol. 3 no. 6 doi:10.1128/microbiolspec.TBS-0005-2012
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Image of FIGURE 2
FIGURE 2

Spore PG structure and modification. The spore PG strands are composed of -acetylglucosamine (NAG), muramic-δ-lactam (MδL), and -acetylmuramic acid (NAM). Each NAM residue initially has a pentapeptide side chain composed of -Ala, -Glu, diaminopimelic acid (Dpm), and two -Ala residues. The peptides can be cleaved to tetrapeptides by DacB or DacF, a reaction that regulates the degree of PG cross-linking. Many peptides in the germ cell wall are cleaved to tripeptides by DacA. LytH is an endopeptidase that produces single -Ala side chains. The combined actions of the amidase CwlD and the deacetylase PdaA lead to the production of muramic-δ-lactam. Transpeptidase activities carried by class A and class B PBPs produce peptide cross-links between the glycan strands. doi:10.1128/microbiolspec.TBS-0005-2012.f2

Source: microbiolspec December 2015 vol. 3 no. 6 doi:10.1128/microbiolspec.TBS-0005-2012
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Image of FIGURE 3
FIGURE 3

Expression of spore PG synthesis and modifying enzymes. The PBPs 1, 2c, 4, and DacA are expressed during vegetative growth and some protein persists in the sporangium. PBPs 1, 2c, and 4 may participate in cortex PG polymerization. DacA certainly is involved in shortening spore PG peptide side chains to tripeptides. Following asymmetric septation and initiation of compartmentalized gene expression, σ and σ drive expression of PG-active proteins in the two cells. Upon completion of engulfment and activation of σ, additional genes are expressed, and germ cell wall synthesis dependent on PBPs 2c and 2d commences adjacent to the inner forespore membrane. Mother cell-expressed proteins commence cortex synthesis adjacent to the outer forespore membrane, and a σ-dependent increase in Mur activity provides precursors for continued synthesis. Solid arrows indicate a direct effect on gene expression by the sigma factor. A dashed arrow indicates potential indirect effects on protein abundance or activity. Black lines represent membranes, and gray lines represent PG structures. doi:10.1128/microbiolspec.TBS-0005-2012.f3

Source: microbiolspec December 2015 vol. 3 no. 6 doi:10.1128/microbiolspec.TBS-0005-2012
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Image of FIGURE 4
FIGURE 4

Domain architecture of GSLEs and interacting proteins. The proteins, along with the conserved domains and motifs shown, are drawn to scale. SleB and YpeB have signal sequences (SS) for export across the inner forespore membrane during sporulation. Both SleB and SleC have a PG-binding domain (PG-bind) (pfam01471), presumably to aid in protein localization or substrate affinity. The LysM domains (pfam01476) found in SleL/YaaH also recognize PG and are thought to play a similar role. The N-terminal pre- (N-pre) and pro- (N-pro), and C-terminal pro- (C-pro) sequences that are removed from SleC by Csp proteases during sporulation or germination are shown, as well as the N-terminal prosequence that is cleaved from Csp. YpeB contains three predicted PepSY domains (pfam03413), which play an unknown role; however, these domains have been involved in the inhibition of peptidase activity in PepSY-containing proteases. The C terminus of YwdL/GerQ is highly conserved, and a glutamine-rich (Q-rich) region is found toward the N terminus of the protein. The hydrolase family 2 (Hydrolase fam. 2) (pfam07486), glycosyl hydrolase family 18 (pfam00704), peptidase S8 family (pfam00082), and glycosyl hydrolase family 25 (pfam01183) domains contain the enzyme active sites. doi:10.1128/microbiolspec.TBS-0005-2012.f4

Source: microbiolspec December 2015 vol. 3 no. 6 doi:10.1128/microbiolspec.TBS-0005-2012
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Image of FIGURE 5
FIGURE 5

Localization of GSLEs and interacting proteins in dormant spores. SleB (B) and YpeB (Y) have been alternately demonstrated to be localized to the outer cortex/outer forespore membrane and the inner forespore membrane of dormant spores. The precise location of CwlJ (J) within the spore coat layers is unknown, but YwdL/GerQ (Q) is found within the inner coat. SleL/YaaH (L) has also been shown to be an inner coat protein. SleC (C), Csp proteases (P), and SleM (M) are located outside the cortex, either in the inner spore coat or outer forespore membrane. While these proteins are drawn within a single spore, in actuality, a spore only contains a subset of the proteins shown. B, Y, J, Q, and L are found in and likely a few , while C, P, and M are found only in certain . Colocalization is shown for B-Y, J-Q, and C-P due to the requirement of YpeB and YwdL/GerQ for stable incorporation of SleB and CwlJ, respectively, into the dormant spore, and the processing of pro-SleC to active SleC by Csp proteases. However, it should be noted that there is currently no evidence that B-Y or J-Q directly interact. doi:10.1128/microbiolspec.TBS-0005-2012.f5

Source: microbiolspec December 2015 vol. 3 no. 6 doi:10.1128/microbiolspec.TBS-0005-2012
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Image of FIGURE 6
FIGURE 6

GSLE cleavage of cortex PG. A single strand of cortex PG is shown at the top, and the cleavage sites for the GSLE enzyme classes are indicated by arrows. A peptide cross-link to another strand is shown, but the second glycan strand is omitted. The proposed -acetylmuramoyl--alanine amidase (A) activity of SleC can break peptide cross-links by cleaving a peptide from NAM. The cleavage sites and representative products (bottom) of -acetylglucosaminidase (G, SleL), -acetylmuramidase (M, SleM), and lytic transglycosylase (LT, SleB and SleC) are indicated. doi:10.1128/microbiolspec.TBS-0005-2012.f6

Source: microbiolspec December 2015 vol. 3 no. 6 doi:10.1128/microbiolspec.TBS-0005-2012
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Tables

Generic image for table
TABLE 1

Identities of orthologous genes potentially involved in synthesis of spore PG in species spanning the family

Source: microbiolspec December 2015 vol. 3 no. 6 doi:10.1128/microbiolspec.TBS-0005-2012
Generic image for table
TABLE 2

Identities of orthologous genes potentially involved in degradation of spore PG in a range of species spanning the family

Source: microbiolspec December 2015 vol. 3 no. 6 doi:10.1128/microbiolspec.TBS-0005-2012
Generic image for table
TABLE 3

Identities of orthologous genes potentially involved in degradation of spore PG in a range of species spanning the family

Source: microbiolspec December 2015 vol. 3 no. 6 doi:10.1128/microbiolspec.TBS-0005-2012

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