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Embedding a ribonuclease in the spore crust couples gene expression to spore development in Bacillus subtilis

ABSTRACT: Faced with nutritional stress, some bacteria form endospores that can survive extreme conditions for long periods of time; yet the function of many proteins expressed during sporulation remains a mystery. We show that one such protein, KapD, is a 3 prime exoribonuclease expressed under control of the mother cell-specific transcription factors SigE and SigK in B. subtilis. KapD assembles dynamically over the spore surface through a direct interaction with the major crust protein CotY. KapD catalytic activity is required for the normal adhesiveness of spore surface layers. We identify the sigK mRNA as a key substrate for KapD and show that its sequestration by CotY controls the stability of the sigK transcript. SigK is controlled through excision of a prophage-like element, transcriptional regulation, and removal of an inhibitory pro-sequence. We reveal a fourth, posttranscriptional layer of control of sigK expression that couples late-stage gene expression in the mother cell to spore morphogenesis.

INSTRUMENT(S): QExactive plus

ORGANISM(S): Bacillus Subtilis (ncbitaxon:1423)

SUBMITTER: Alexandre D'Halluin

PROVIDER: MSV000096627 | MassIVE | Tue Dec 10 01:21:00 GMT 2024

SECONDARY ACCESSION(S): PXD058725

REPOSITORIES: MassIVE

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Project description:Bacterial spores play an important role in disease initiation, transmission and persistence. The outermost spore layer, the exosporium, is important as it is the first point of contact between the spore and the environment and may be involved in spore adherence, protection and germination. Clostridium sordellii is a highly lethal, spore forming pathogen that causes soft-tissue infections, enteritis and toxic-shock syndrome. Despite the importance of C. sordellii spores in disease, spore proteins from this bacterium have not been defined or interrogated functionally. In this study, we identified the C. sordellii outer spore proteome and two of the identified proteins, CSA and CSB, were characterised using a genetic and phenotypic approach. Both proteins were essential for the correct formation and positioning of the C. sordellii spore coat and exosporium. The absence of CSA reduced sporulation levels and increased spore sensitivity to heat, sodium hydroxide and hydrochloric acid. By comparison, CSB was required for normal levels of spore adherence to cervical, but not vaginal, cells, with csb mutant spores having increased adherence properties. The establishment of a mouse infection model of the gastrointestinal tract for C. sordellii allowed the role of CSA and CSB to be interrogated in an infected host. Following the oral administration of spores to mice, the wild-type strain efficiently colonized the gastrointestinal tract, with the peak of bacterial numbers occurring at one day post-infection. Colonization was reduced by two logs at four days post-infection. By comparison, mice infected with the csb mutant did not show a reduction in bacterial numbers. The absence of CSB therefore allows the csb mutant to persist within the gastrointestinal tract. We conclude that C. sordellii outer spore proteins are important for the structural and functional integrity of spores, and for colonization and persistence during infection. Finally, Clostridium difficile, Bacillus cereus and Bacillus anthracis encode proteins with homology to CSA and CSB but these bacteria produce spores that are structurally dissimilar to those of C. sordellii, and the function of the proteins in these hosts is different to that in C. sordellii. These findings suggest that, despite their homology, spore proteins can have variable functions in different bacterial species which highlights the necessity of studying each spore protein in the cognate species from which it originates.

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Embedding a ribonuclease in the spore crust couples gene expression to spore development in Bacillus subtilis

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