Independent gene duplications of the YidC/Oxa/Alb3 family enabled a specialized cotranslational function.
YidC/Oxa/Alb3 family proteins catalyze the insertion of integral membrane proteins in bacteria, mitochondria, and chloroplasts, respectively. Unlike gram-negative organisms, gram-positive bacteria express 2 paralogs of this family, YidC1/SpoIIIJ and YidC2/YgjG. In Streptococcus mutans, deletion of yidC2 results in a stress-sensitive phenotype similar to that of mutants lacking the signal recognition particle (SRP) protein translocation pathway, while deletion of yidC1 has a less severe phenotype. In contrast to eukaryotes and gram-negative bacteria, SRP-deficient mutants are viable in S. mutans; however, double SRP-yidC2 mutants are severely compromised. Thus, YidC2 may enable loss of the SRP by playing an independent but overlapping role in cotranslational protein insertion into the membrane. This is reminiscent of the situation in mitochondria that lack an SRP pathway and where Oxa1 facilitates cotranslational membrane protein insertion by binding directly to translation-active ribosomes. Here, we show that OXA1 complements a lack of yidC2 in S. mutans. YidC2 also functions reciprocally in oxa1-deficient Saccharomyces cerevisiae mutants and mediates the cotranslational insertion of mitochondrial translation products into the inner membrane. YidC2, like Oxa1, contains a positively charged C-terminal extension and associates with translating ribosomes. Our results are consistent with a gene-duplication event in gram-positive bacteria that enabled the specialization of a YidC isoform that mediates cotranslational activity independent of an SRP pathway.
Gene Center, Department of Chemistry and Biochemistry, University of Munich, Feodor-Lynen Strasse 25, 81377 Munich, Germany.
Soledad
S
Funes
Adnan
A
Hasona
Heike
H
Bauerschmitt
Caroline
C
Grubbauer
Frank
F
Kauff
Ryan
R
Collins
Paula J
PJ
Crowley
Sara R
SR
Palmer
L Jeannine
LJ
Brady
Johannes M
JM
Herrmann
D001426:Bacterial Proteins / Q000235:genetics*; D003576:Electron Transport Complex IV / Q000235:genetics*; D020440:Gene Duplication; D005816:Genetic Complementation Test; D008928:Mitochondria / Q000378:metabolism; D024101:Mitochondrial Proteins / Q000235:genetics*; D008957:Models, Genetic; D009154:Mutation / Q000235:genetics; D009687:Nuclear Proteins / Q000235:genetics*; D010802:Phylogeny; D011485:Protein Binding; D014176:Protein Biosynthesis; D012270:Ribosomes / Q000378:metabolism; D012441:Saccharomyces cerevisiae / Q000166:cytology / Q000235:genetics*; D013295:Streptococcus mutans / Q000235:genetics*; D013997:Time Factors
D001426:Bacterial Proteins; D024101:Mitochondrial Proteins; D009687:Nuclear Proteins; C090858:OXA1 protein; D003576:Electron Transport Complex IV