Structure and function of the spoIIIJ gene of Bacillus subtilis: a vegetatively expressed gene that is essential for  G activity at an intermediate stage of sporulation

Errington, Jeff; Appleby, Lara; Daniel, Richard A.; Goodfellow, Hugh R.; Partridge, Sally R.; Yudkin, M. D.

doi:10.1099/00221287-138-12-2609

Cited by 91 publications

(115 citation statements)

References 40 publications

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“…Moreover, each homolog can have multiple functions and reaction mechanisms (7,(36)(37)(38). We envision that the peculiarity of having a hydrophilic cavity in the membrane may be a common feature conserved in many of the family members.…”

Section: Discussionmentioning

confidence: 99%

Hydrophilic microenvironment required for the channel-independent insertase function of YidC protein

Shimokawa-Chiba

Kumazaki

Tsukazaki

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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The recently solved crystal structure of YidC protein suggests that it mediates membrane protein insertion by means of an intramembrane cavity rather than a transmembrane (TM) pore. This concept of protein translocation prompted us to characterize the native, membrane-integrated state of YidC with respect to the hydropathic nature of its TM region. Here, we show that the cavityforming region of the stage III sporulation protein J (SpoIIIJ), a YidC homolog, is indeed open to the aqueous milieu of the Bacillus subtilis cells and that the overall hydrophilicity of the cavity, along with the presence of an Arg residue on several alternative sites of the cavity surface, is functionally important. We propose that YidC functions as a proteinaceous amphiphile that interacts with newly synthesized membrane proteins and reduces energetic costs of their membrane traversal.

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Section: Discussionmentioning

confidence: 99%

Hydrophilic microenvironment required for the channel-independent insertase function of YidC protein

Shimokawa-Chiba

Kumazaki

Tsukazaki

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…Previous work has shown that G accumulates but is mostly inactive in spoIIIA or spoIIIJ mutants of B. subtilis (19,41), both of which show a morphological block just after completion of the engulfment process (6,30). This has led to the suggestion that both spoIIIA and spoIIIJ act after engulfment to promote the activation of G in the prespore.…”

Section: Discussionmentioning

confidence: 99%

“…Conclusion of the engulfment process is not sufficient for the activation of G , which further requires expression of several genes, including the eight cistrons of the spoIIIA operon and the spoIIIJ gene (6,19,34). G accumulates in spoIIIA or spoIIIJ mutant cells but is unable to activate transcription from its target promoters (19,41).…”

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confidence: 99%

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Role of the Anti-Sigma Factor SpoIIAB in Regulation of σ ^G during Bacillus subtilis Sporulation

et al. 2004

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RNA polymerase sigma factor F initiates the prespore-specific program of gene expression during Bacillus subtilis sporulation. F governs transcription of spoIIIG, encoding the late prespore-specific regulator G . However, transcription of spoIIIG is delayed relative to other genes under the control of F , and after synthesis, G is initially kept in an inactive form. Activation of G requires the complete engulfment of the prespore by the mother cell and expression of the spoIIIA and spoIIIJ loci. We screened for random mutations in spoIIIG that bypassed the requirement for spoIIIA for the activation of G . We found a mutation (spoIIIGE156K) that resulted in an amino acid substitution at position 156, which is adjacent to the position of a mutation (E155K) previously shown to prevent interaction of SpoIIAB with G . Comparative modelling techniques and in vivo studies suggested that the spoIIIGE156K mutation interferes with the interaction of SpoIIAB with G . The GE156K isoform restored G -directed gene expression to spoIIIA mutant cells. However, expression of sspElacZ in the spoIIIA spoIIIGE156K double mutant was delayed relative to completion of the engulfment process and was not confined to the prespore. Rather, ␤-galactosidase accumulated throughout the entire cell at late times in development. This suggests that the activity of GE156K is still regulated in the prespore of a spoIIIA mutant, but not by SpoIIAB. In agreement with this suggestion, we also found that expression of spoIIIGE156K from the promoter for the early prespore-specific gene spoIIQ still resulted in sspE-lacZ induction at the normal time during sporulation, coincidently with completion of the engulfment process. In contrast, transcription of spoIIIGE156K, but not of the wild-type spoIIIG gene, from the mother cell-specific spoIID promoter permitted the rapid induction of sspE-lacZ expression. Together, the results suggest that SpoIIAB is either redundant or has no role in the regulation of G in the prespore.Gene expression in the prespore and mother cell chambers of sporulating Bacillus subtilis is controlled by RNA polymerase sigma subunits whose activity is restricted to a specific cell type (22,31,37,46). The activation of the sporulation-specific sigma factors is tightly coupled to the completion of key morphological intermediates in the process and also relies on signaling pathways that operate between the two cell types and that keep the prespore and mother cell lines of gene expression in close register (22,31,37,46). Soon after the asymmetric division of the sporangial cell, an event that creates the prespore and the much larger mother cell, the first compartmentspecific sigma factor F becomes active in the prespore (22,31,37,46

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“…Thus two homologues (Spy0247 and Spy0351) were identified of B. subtilis SpoIIIJ (Errington et al, 1992), a probable Lpp that has recently been suggested to be associated with the export and processing of integral membrane proteins (Tjalsma et al, 2000 ;Luirink et al, 2001 ;Yen et al, 2001). Both Spy0247 and Spy0351 are predicted to encode proteins with multiple MSDs in addition to the predicted Nterminal lipid anchor, as in SpoIIIJ (Luirink et al, 2001 ;Yen et al, 2001).…”

Section: Summary Featuresmentioning

confidence: 99%

Pattern searches for the identification of putative lipoprotein genes in Gram-positive bacterial genomes

2002

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INTRODUCTIONThe bacterial cell envelope is of major significance as the focal point for interaction between the bacterium and its environment, notably the host in the case of bacterial pathogens. Bacterial cell envelope proteins thus carry out numerous important functions including roles in adhesion, nutrient acquisition and a variety of interactions with host defences. In Gram-positive bacteria the matrix of peptidoglycan and other wall polymers surrounding the cell is not an efficient barrier to the passage of small macromolecules, due both to its inherent structural permeability and to its turnover during normal cell growth. Indeed, peptidoglycan may be sufficiently permeable as to allow the passage of globular proteins of up to "50 kDa in size (Demchick & Koch, 1996 ;Dijkstra & Keck, 1996). Consequently, in the absence of a retentive outer membrane, Grampositive bacteria have evolved distinct mechanisms for retaining proteins within their cell envelopes, including covalent linkage to the peptidoglycan and non-covalent binding to teichoic acids and other cell envelope polymers (Navarre & Schneewind, 1999 ;Cossart & Jonquieres, 2000 ;Janulczyk & Rasmussen, 2001). Also significant among these mechanisms is membraneanchoring of bacterial lipoproteins (Lpps) by covalent N-terminal lipidation (Braun & Wu, 1994 ; Sutcliffe & Russell, 1995). Lpps in Gram-positive bacteria perform important roles as substrate-binding proteins (SBPs) in ABC transporter systems ; in antibiotic resistance ; in cell signalling ; in protein export and folding ; in sporulation and germination ; in conjugation and various other functions (Sutcliffe & Russell, 1995 valent to those carried out by periplasmic proteins of Gram-negative bacteria.The archetypal bacterial Lpp is the murein lipoprotein of Escherichia coli characterized by Braun and coworkers (reviewed in Braun & Wu, 1994). Structural studies revealed that a diacylglycerol moiety is thioether linked to an N-terminal cysteine of this Lpp and that this lipid group serves to orientate the protein by anchoring it to the inner leaflet of the outer membrane. Chemically identical lipid modifications have since been proposed, primarily on the basis of protein sequence analysis (see below), for a great many proteins in both Gram-positive and Gram-negative bacteria, although relatively few have received extensive biochemical characterization.Biosynthesis of bacterial lipoprotein of the ' Braun ' type proceeds via a well conserved pathway that is apparently unique to prokaryotes (Fig. 1). Following signal-peptidedirected export of the prolipoprotein (proLpp), the enzyme prolipoprotein diacylglycerol transferase (Lgt) uses phospholipid substrates and catalyses the addition of a diacylglycerol lipid unit onto the thiol of a crucial conserved cysteine which is located within a ' lipobox ' motif at the cleavage region of the proLpp signal peptide (Sankaran et al., 1995 ; Qi et al., 1995). Subsequently, the signal peptide is removed by a specific lipoprotein signal peptidase II (Lsp) enzyme which ...

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Structure and function of the spoIIIJ gene of Bacillus subtilis: a vegetatively expressed gene that is essential for G activity at an intermediate stage of sporulation

Cited by 91 publications

References 40 publications

Hydrophilic microenvironment required for the channel-independent insertase function of YidC protein

Hydrophilic microenvironment required for the channel-independent insertase function of YidC protein

Role of the Anti-Sigma Factor SpoIIAB in Regulation of σ ^G during Bacillus subtilis Sporulation

Pattern searches for the identification of putative lipoprotein genes in Gram-positive bacterial genomes

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Structure and function of the spoIIIJ gene of Bacillus subtilis: a vegetatively expressed gene that is essential for G activity at an intermediate stage of sporulation

Cited by 91 publications

References 40 publications

Hydrophilic microenvironment required for the channel-independent insertase function of YidC protein

Hydrophilic microenvironment required for the channel-independent insertase function of YidC protein

Role of the Anti-Sigma Factor SpoIIAB in Regulation of σ G during Bacillus subtilis Sporulation

Pattern searches for the identification of putative lipoprotein genes in Gram-positive bacterial genomes

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Product

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Role of the Anti-Sigma Factor SpoIIAB in Regulation of σ ^G during Bacillus subtilis Sporulation