Genome-Wide Analysis of Cell Type-Specific Gene Transcription during Spore Formation in Clostridium difficile

Saujet, Laure; Pereira, Fátima C.; Serrano, Mònica; Soutourina, Olga; Monot, Marc; Shelyakin, Pavel V.; Gelfand, Mikhail S.; Dupuy, Bruno; Henriques, Adriano O.; Martin‐Verstraete, Isabelle

doi:10.1371/journal.pgen.1003756

Cited by 143 publications

(370 citation statements)

References 97 publications

(294 reference statements)

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“…The P spoIIIA -SNAP Cd promoter fusion in C. difficile showed that E was confined to the mother cell, similar to what is seen for B. subtilis (94). Transcriptional profiling using microarray analysis showed that there are 97 genes under the control of E in C. difficile (95). As in B. subtilis, this makes the C. difficile E regulon the largest regulon among the four sporulation-specific sigma factors.…”

Section: E the First Mother Cell-specific Sigma Factor Is Involvedmentioning

confidence: 54%

“…Moreover, the transcription of sigK appeared to be confined to the mother cell, which is consistent with its role as a mother cellspecific sigma factor (94). Global transcription profiling revealed that there are 56 genes that are putatively under the control of K in C. difficile (95). These included genes that play a role in spore coat assembly, spore maturation, and mother cell lysis (95).…”

Section: K Has a Second Role Late In Sporulation As The Second Mothmentioning

confidence: 58%

“…Genomewide gene transcription analysis of the C. difficile sigF mutant revealed that 25 genes were downregulated in the C. difficile sigF mutant, indicating that they are potentially under F control (95). Unlike in C. acetobutylicum, it appears that gpr, spoIIR, and spoIIP are all under the control of F in C. difficile (95).…”

Section: Sporulation-specific Sigma Factors That Are Activated Downstmentioning

confidence: 99%

“…Using transcriptional SNAP Cd fusions to CD2470 (the ortholog of the B. subtilis gpr gene), which is predicted to be under the control of F , Pereira et al demonstrated that F is active exclusively in the forespore despite being transcribed in both the mother cell and forespore compartments (94). Genomewide gene transcription analysis of the C. difficile sigF mutant revealed that 25 genes were downregulated in the C. difficile sigF mutant, indicating that they are potentially under F control (95). Unlike in C. acetobutylicum, it appears that gpr, spoIIR, and spoIIP are all under the control of F in C. difficile (95).…”

Section: Sporulation-specific Sigma Factors That Are Activated Downstmentioning

confidence: 99%

“…Additionally, an electron-dense region was seen around the forespore, indicating deposition of spore coat proteins (94), which is not seen in the B. subtilis sigG mutant (104). Transcriptional profiling using microarray analysis showed that there are 50 genes under the control of G in C. difficile (95), including genes responsible for the import of dipicolinic acid, cell wall synthesis, and cortex formation (95). Expression of the promoter fusion P sigG -SNAP Cd was not detected in the C. difficile sigF mutant, indicating that F is necessary for sigG expression (94).…”

Section: E the First Mother Cell-specific Sigma Factor Is Involvedmentioning

confidence: 99%

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The Clostridium Sporulation Programs: Diversity and Preservation of Endospore Differentiation

Al-Hinai

Jones

Papoutsakis

2015

Microbiol Mol Biol Rev

156

190

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SUMMARY Bacillus and Clostridium organisms initiate the sporulation process when unfavorable conditions are detected. The sporulation process is a carefully orchestrated cascade of events at both the transcriptional and posttranslational levels involving a multitude of sigma factors, transcription factors, proteases, and phosphatases. Like Bacillus genomes, sequenced Clostridium genomes contain genes for all major sporulation-specific transcription and sigma factors ( spo0A , sigH , sigF , sigE , sigG , and sigK ) that orchestrate the sporulation program. However, recent studies have shown that there are substantial differences in the sporulation programs between the two genera as well as among different Clostridium species. First, in the absence of a Bacillus -like phosphorelay system, activation of Spo0A in Clostridium organisms is carried out by a number of orphan histidine kinases. Second, downstream of Spo0A, the transcriptional and posttranslational regulation of the canonical set of four sporulation-specific sigma factors (σ F , σ E , σ G , and σ K ) display different patterns, not only compared to Bacillus but also among Clostridium organisms. Finally, recent studies demonstrated that σ K , the last sigma factor to be activated according to the Bacillus subtilis model, is involved in the very early stages of sporulation in Clostridium acetobutylicum , C. perfringens , and C. botulinum as well as in the very late stages of spore maturation in C. acetobutylicum . Despite profound differences in initiation, propagation, and orchestration of expression of spore morphogenetic components, these findings demonstrate not only the robustness of the endospore sporulation program but also the plasticity of the program to generate different complex phenotypes, some apparently regulated at the epigenetic level.

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Section: E the First Mother Cell-specific Sigma Factor Is Involvedmentioning

confidence: 54%

Section: K Has a Second Role Late In Sporulation As The Second Mothmentioning

confidence: 58%

Section: Sporulation-specific Sigma Factors That Are Activated Downstmentioning

confidence: 99%

Section: Sporulation-specific Sigma Factors That Are Activated Downstmentioning

confidence: 99%

Section: E the First Mother Cell-specific Sigma Factor Is Involvedmentioning

confidence: 99%

See 3 more Smart Citations

The Clostridium Sporulation Programs: Diversity and Preservation of Endospore Differentiation

Al-Hinai

Jones

Papoutsakis

2015

Microbiol Mol Biol Rev

156

190

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Oscillating behavior of Clostridium difficile Min proteins in Bacillus subtilis

et al. 2016

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In rod‐shaped bacteria, the proper placement of the division septum at the midcell relies, at least partially, on the proteins of the Min system as an inhibitor of cell division. The main principle of Min system function involves the formation of an inhibitor gradient along the cell axis; however, the establishment of this gradient differs between two well‐studied gram‐negative and gram‐positive bacteria. While in gram‐negative Escherichia coli, the Min system undergoes pole‐to‐pole oscillation, in gram‐positive Bacillus subtilis, proper spatial inhibition is achieved by the preferential attraction of the Min proteins to the cell poles. Nevertheless, when E.coli Min proteins are inserted into B.subtilis cells, they still oscillate, which negatively affects asymmetric septation during sporulation in this organism. Interestingly, homologs of both Min systems were found to be present in various combinations in the genomes of anaerobic and endospore‐forming Clostridia, including the pathogenic Clostridium difficile. Here, we have investigated the localization and behavior of C.difficile Min protein homologs and showed that MinDE proteins of C.difficile can oscillate when expressed together in B.subtilis cells. We have also investigated the effects of this oscillation on B.subtilis sporulation, and observed decreased sporulation efficiency in strains harboring the MinDE genes. Additionally, we have evaluated the effects of C.difficile Min protein expression on vegetative division in this heterologous host.

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"One‐Pot" Sample Processing Method for Proteome‐Wide Analysis of Microbial Cells and Spores

Swarge

Roseboom

Zheng

et al. 2018

Proteomics Clinical Apps

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PurposeBacterial endospores, the transmissible forms of pathogenic bacilli and clostridia, are heterogeneous multilayered structures composed of proteins. These proteins protect the spores against a variety of stresses, thus helping spore survival, and assist in germination, by interacting with the environment to form vegetative cells. Owing to the complexity, insolubility, and dynamic nature of spore proteins, it has been difficult to obtain their comprehensive protein profiles.Experimental designThe intact spores of Bacillus subtilis, Bacillus cereus, and Peptoclostridium difficile and their vegetative counterparts were disrupted by bead beating in 6 m urea under reductive conditions. The heterogeneous mixture was then double digested with LysC and trypsin. Next, the peptide mixture was pre‐fractionated with zwitterionic hydrophilic interaction liquid chromatography (ZIC‐HILIC) followed by reverse‐phase LC‐FT‐MS analysis of the fractions.Results"One‐pot" method is a simple, robust method that yields identification of >1000 proteins with high confidence, across all spore layers from B. subtilis, B. cereus, and P. difficile.Conclusions and medical relevanceThis method can be employed for proteome‐wide analysis of non‐spore‐forming as well as spore‐forming pathogens. Analysis of spore protein profile will help to understand the sporulation and germination processes and to distinguish immunogenic protein markers.

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Genome-Wide Analysis of Cell Type-Specific Gene Transcription during Spore Formation in Clostridium difficile

Cited by 143 publications

References 97 publications

The Clostridium Sporulation Programs: Diversity and Preservation of Endospore Differentiation

The Clostridium Sporulation Programs: Diversity and Preservation of Endospore Differentiation

Oscillating behavior of Clostridium difficile Min proteins in Bacillus subtilis

"One‐Pot" Sample Processing Method for Proteome‐Wide Analysis of Microbial Cells and Spores

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