YidC is involved in the biogenesis of the secreted autotransporter hemoglobin protease.
Autotransporters (ATs) constitute an important family of virulence factors secreted by Gram-negative bacteria. Following their translocation across the inner membrane (IM), ATs temporarily reside in the periplasmic space after which they are secreted into the extracellular environment. Previous studies have shown that the AT hemoglobin protease (Hbp) of Escherichia coli requires a functional signal recognition particle pathway and Sec translocon for optimal targeting to and translocation across the IM. Here, we analyzed the mode of IM translocation of Hbp in more detail. Using site-directed photocross-linking, we found that the Hbp signal peptide is adjacent to YidC early during biogenesis. Notably, YidC is in part associated with the Sec translocon but has until now primarily been implicated in the biogenesis of IM proteins. In vivo, YidC appeared critical for the biogenesis of the ATs Hbp and EspC. For Hbp, depletion of YidC resulted in the formation of secretion-incompetent intermediates that were sensitive to degradation by the periplasmic protease DegP, indicating that YidC activity affects Hbp biogenesis at a late stage, after translocation across the IM. This is the first demonstration of a role for YidC in the biogenesis of an extracellular protein. We propose that YidC is required for maintenance of the translocation-competent state of certain ATs in the periplasm. The large periplasmic domain of YidC is not critical for this novel functionality as it can be deleted without affecting Hbp biogenesis.
Section of Molecular Microbiology, Department of Molecular Cell Biology, VU University, De Boelelaan 1085, 1081 HV Amsterdam, The Netherlands.
Wouter S P
WS
Jong
Corinne M
CM
ten Hagen-Jongman
Eelco
E
Ruijter
Romano V A
RV
Orru
Pierre
P
Genevaux
Joen
J
Luirink
D000251:Adenosine Triphosphatases / Q000235:genetics / Q000378:metabolism; D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism; D002462:Cell Membrane / Q000235:genetics / Q000378:metabolism; D010450:Endopeptidases / Q000096:biosynthesis* / Q000235:genetics; D004926:Escherichia coli / Q000235:genetics / Q000378:metabolism*; D029968:Escherichia coli Proteins / Q000235:genetics / Q000378:metabolism*; D006360:Heat-Shock Proteins / Q000235:genetics / Q000378:metabolism; D026901:Membrane Transport Proteins / Q000235:genetics / Q000378:metabolism*; D019897:Periplasm / Q000235:genetics / Q000378:metabolism*; D033903:Periplasmic Proteins / Q000235:genetics / Q000378:metabolism; D021382:Protein Sorting Signals / Q000502:physiology*; D017434:Protein Structure, Tertiary; D000069816:SEC Translocation Channels; D000081416:SecA Proteins; D012697:Serine Endopeptidases / Q000235:genetics / Q000378:metabolism
D001426:Bacterial Proteins; D029968:Escherichia coli Proteins; D006360:Heat-Shock Proteins; D026901:Membrane Transport Proteins; D033903:Periplasmic Proteins; D021382:Protein Sorting Signals; D000069816:SEC Translocation Channels; C412443:YIDC protein, E coli; D010450:Endopeptidases; C061682:DegP protease; D012697:Serine Endopeptidases; C114676:hemoglobin protease Hbp; D000251:Adenosine Triphosphatases; D000081416:SecA Proteins