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Signal peptides direct surface proteins to two distinct envelope locations of Staphylococcus aureus.

ABSTRACT: Surface proteins of Gram-positive bacteria are covalently linked to the cell wall envelope by a mechanism requiring an N-terminal signal peptide and a C-terminal LPXTG motif sorting signal. We show here that surface proteins of Staphylococcus aureus arrive at two distinct destinations in the bacterial envelope, either distributed as a ring surrounding each cell or as discrete assembly sites. Proteins with ring-like distribution (clumping factor A (ClfA), Spa, fibronectin-binding protein B (FnbpB), serine-aspartate repeat protein C (SdrC) and SdrD) harbour signal peptides with a YSIRK/GS motif, whereas proteins directed to discrete assembly sites (S. aureus surface protein A (SasA), SasD, SasF and SasK) do not. Reciprocal exchange of signal peptides between surface proteins with (ClfA) or without the YSIRK/GS motif (SasF) directed recombinant products to the alternate destination, whereas mutations that altered only the YSIRK sequence had no effect. Our observations suggest that S. aureus distinguishes between signal peptides to address proteins to either the cell pole (signal peptides without YSIRK/GS) or the cross wall, the peptidoglycan layer that forms during cell division to separate new daughter cells (signal peptides with YISRK/GS motif).

SUBMITTER: DeDent A

PROVIDER: S-EPMC2572169 | biostudies-literature | 2008 Oct

REPOSITORIES: biostudies-literature

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Signal peptides direct surface proteins to two distinct envelope locations of Staphylococcus aureus.

DeDent Andrea A Bae Taeok T Missiakas Dominique M DM Schneewind Olaf O

The EMBO journal 20080918 20

Surface proteins of Gram-positive bacteria are covalently linked to the cell wall envelope by a mechanism requiring an N-terminal signal peptide and a C-terminal LPXTG motif sorting signal. We show here that surface proteins of Staphylococcus aureus arrive at two distinct destinations in the bacterial envelope, either distributed as a ring surrounding each cell or as discrete assembly sites. Proteins with ring-like distribution (clumping factor A (ClfA), Spa, fibronectin-binding protein B (FnbpB ...[more]

PMID: 18800056

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Project description:Protein secretion is essential, but how it is managed is poorly understood. In bacteria, most secreted proteins require release from the outer surface of the cytoplasmic membrane by type I signal peptidase (SPase), which cleaves the mature protein from its membrane-bound N-terminal signal peptide. As the first step that occurs outside the protected cytoplasmic environment and because insufficient activity can rapidly result in the toxic accumulation of preproteins, the activity of SPase is expected to be closely monitored and perhaps supplemented when insufficient. Indeed, we previously demonstrated that inhibition of SPase in Staphylococcus aureus results in derepression of the ayrRABC operon, which encodes an alternate mechanism to release proteins. However, in this case, the proteins are released with partially intact signal peptides, with the exception of IsaA, which is released with a virtually intact signal peptide. Here we show that mutation of AyrA [ayrA(R233K)] results in constitutive derepression of ayrRABC and that mutation of IsaA's signal peptide [isaA(K2Q)] results in hyperderepression upon SPase inhibition, which also requires AyrA. Further studies demonstrate that the inducing signal for ayrRABC derepression is accumulation of a subset of preproteins with signal peptides that are stable toward further processing and that the signal is critically amplified by the K2Q mutation and relayed to AyrR by AyrA. These results elucidate the mechanism by which S. aureus monitors and responds to secretion stress. The presence of ayrRA in other bacteria suggests that it may represent a general strategy linking membrane stress to appropriate transcriptional responses.IMPORTANCE Bacteria interact with their environment by secreting proteins that perform a myriad of functions, and the final step is the release of the mature protein from the cell surface via the activity of type I signal peptidase (SPase). While the bacterial response to many stresses is understood in some detail, almost nothing is known about how cells respond to secretion stress, such as insufficient SPase activity, which would eventually result in cell death. We previously demonstrated that the inhibition of SPase in Staphylococcus aureus results in the derepression of the ayrRABC operon, which can functionally replace SPase, but which is normally repressed by AyrR. We now demonstrate that the inducing signal for derepression is accumulation of a subset of preproteins with signal peptides that are stable to further processing and that the signal is relayed to AyrR via AyrA.

Dataset Information

Signal peptides direct surface proteins to two distinct envelope locations of Staphylococcus aureus.

Publications

Signal peptides direct surface proteins to two distinct envelope locations of Staphylococcus aureus.

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