Cleavage of an engulfment peptidoglycan hydrolase by a sporulation signature protease in Clostridioides difficile

In the model organism Bacillus subtilis, a signaling protease produced in the forespore, SpoIVB, is essential for the activation of the sigma factor σK, which is produced in the mother cell as an inactive pro‐protein, pro‐σK. SpoIVB has a second function essential to sporulation, most likely during...

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Published in:	Molecular microbiology Vol. 122; no. 2; pp. 213 - 229
Main Authors:	Martins, Diogo, Nerber, Hailee N., Roughton, Charlotte G., Fasquelle, Amaury, Barwinska‐Sendra, Anna, Vollmer, Daniela, Gray, Joe, Vollmer, Waldemar, Sorg, Joseph A., Salgado, Paula S., Henriques, Adriano O., Serrano, Mónica
Format:	Journal Article
Language:	English
Published:	England Blackwell Publishing Ltd 01-08-2024
Subjects:	Amidase Bacillus subtilis - enzymology Bacillus subtilis - genetics Bacillus subtilis - metabolism Bacterial Proteins - genetics Bacterial Proteins - metabolism Cell activation Cleavage Clostridioides difficile Clostridioides difficile - enzymology Clostridioides difficile - genetics Clostridioides difficile - metabolism Cortex Deletion mutant Dormancy Gene expression Gene Expression Regulation, Bacterial Heat resistance Inactivation Mutants N-Acetylmuramoyl-L-alanine Amidase - genetics N-Acetylmuramoyl-L-alanine Amidase - metabolism Nucleotide sequence Peptide Hydrolases - genetics Peptide Hydrolases - metabolism peptidoglycan Peptidoglycan - metabolism Peptidoglycan hydrolase Protease serine‐protease Sigma factor Sigma Factor - genetics Sigma Factor - metabolism SpoIIP SpoIVB Spores Spores, Bacterial - genetics Spores, Bacterial - metabolism Sporulation Substrates Synthesis Thermal resistance cortex peptidoglycan SpoIVB SpoIIP serine‐protease
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Summary:	In the model organism Bacillus subtilis, a signaling protease produced in the forespore, SpoIVB, is essential for the activation of the sigma factor σK, which is produced in the mother cell as an inactive pro‐protein, pro‐σK. SpoIVB has a second function essential to sporulation, most likely during cortex synthesis. The cortex is composed of peptidoglycan (PG) and is essential for the spore's heat resistance and dormancy. Surprisingly, the genome of the intestinal pathogen Clostridioides difficile, in which σK is produced without a pro‐sequence, encodes two SpoIVB paralogs, SpoIVB1 and SpoIVB2. Here, we show that spoIVB1 is dispensable for sporulation, while a spoIVB2 in‐frame deletion mutant fails to produce heat‐resistant spores. The spoIVB2 mutant enters sporulation, undergoes asymmetric division, and completes engulfment of the forespore by the mother cell but fails to synthesize the spore cortex. We show that SpoIIP, a PG hydrolase and part of the engulfasome, the machinery essential for engulfment, is cleaved by SpoIVB2 into an inactive form. Within the engulfasome, the SpoIIP amidase activity generates the substrates for the SpoIID lytic transglycosylase. Thus, following engulfment completion, the cleavage and inactivation of SpoIIP by SpoIVB2 curtails the engulfasome hydrolytic activity, at a time when synthesis of the spore cortex peptidoglycan begins. SpoIVB2 is also required for normal late gene expression in the forespore by a currently unknown mechanism. Together, these observations suggest a role for SpoIVB2 in coordinating late morphological and gene expression events between the forespore and the mother cell. Model for the cleavage of SpoIIP by SpoIVB2 during sporulation in Clostridioides difficile. Soon after engulfment completion, SpoIVB2 cleaves SpoIIP, part of the engulfasome complex, to generate the SpoIIPc form. The function of SpoIVB2 is required for synthesis of the cortex layer which takes place across the outer forespore membrane.
Bibliography:	Hailee N. Nerber and Charlotte G. Roughton contributed equally to this work. ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23
ISSN:	0950-382X 1365-2958 1365-2958
DOI:	10.1111/mmi.15291