YidC1 and YidC2 are functionally distinct proteins involved in protein secretion, biofilm formation and cariogenicity of Streptococcus mutans

Palmer, Sam; Crowley, Paula J.; Oli, Monika W.; Ruelf, M. Adam; Michalek, Suzanne M.; Brady, L. Jeannine

doi:10.1099/mic.0.059139-0

Cited by 43 publications

(87 citation statements)

References 42 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The observation that both YidC1 and YidC2 can actively insert the small membrane protein F o c and bind ribosomes is in agree- ment with their (partial) overlapping function in the native host (14,16,28). Such overlapping function has also been observed with the YidC homologs of Bacillus subtilis (8,10).…”

Section: Discussionsupporting

confidence: 59%

“…The latter concerns impaired biofilm formation, decreased ATPase activity, and growth defects under acid, osmotic, and oxidative stress conditions (12). Interestingly, the stress tolerance and ATPase activity defects of the ⌬yidC2 mutant are complemented by a chimeric YidC1 protein that bears the C terminus of YidC2 (14). Therefore, the C terminus appears to play a key role in the specific YidC function.…”

mentioning

confidence: 99%

See 1 more Smart Citation

Interaction of Streptococcus mutans YidC1 and YidC2 with Translating and Nontranslating Ribosomes

Keyzer

Berrelkamp-Lahpor

et al. 2013

J Bacteriol

View full text Add to dashboard Cite

The YidC/OxaI/Alb3 family of membrane proteins is involved in the biogenesis of integral membrane proteins in bacteria, mitochondria, and chloroplasts. Gram-positive bacteria often contain multiple YidC paralogs that can be subdivided into two major classes, namely, YidC1 and YidC2. The Streptococcus mutans YidC1 and YidC2 proteins possess C-terminal tails that differ in charges (؉9 and ؉ 14) and lengths (33 and 61 amino acids). The longer YidC2 C terminus bears a resemblance to the C-terminal ribosome-binding domain of the mitochondrial OxaI protein and, in contrast to the shorter YidC1 C terminus, can mediate the interaction with mitochondrial ribosomes. These observations have led to the suggestion that YidC1 and YidC2 differ in their abilities to interact with ribosomes. However, the interaction with bacterial translating ribosomes has never been addressed. Here we demonstrate that Escherichia coli ribosomes are able to interact with both YidC1 and YidC2. The interaction is stimulated by the presence of a nascent membrane protein substrate and abolished upon deletion of the C-terminal tail, which also abrogates the YidC-dependent membrane insertion of subunit c of the F 1 F 0 -ATPase into the membrane. It is concluded that both YidC1 and YidC2 interact with ribosomes, suggesting that the modes of membrane insertion by these membrane insertases are similar.

show abstract

Section: Discussionsupporting

confidence: 59%

mentioning

confidence: 99%

Interaction of Streptococcus mutans YidC1 and YidC2 with Translating and Nontranslating Ribosomes

Keyzer

Berrelkamp-Lahpor

et al. 2013

J Bacteriol

View full text Add to dashboard Cite

show abstract

“…The respective substrates of the SRP pathway and YidC2 and YidC1 are largely unknown in S. mutans, although these systems likely overlap and appear to work in concert (72). The integral membrane proteins YidC1 and YidC2 would be expected to mediate membrane protein insertion, but they have also been found to influence the amount and functional maturation of cell surface-localized proteins, including adhesin P1 (71). In the current study, S. mutans mutants lacking Ffh, YidC2, and, to a lesser extent, YidC1 all demonstrated less eDNA than the parental strain.…”

Section: Discussionmentioning

confidence: 99%

“…Ffh (for SRP54) and scRNA are core elements of the bacterial signal recognition particle (SRP) cotranslational protein translocation pathway, and FtsY is the membrane-bound SRP receptor (70). YidC1 and YidC2 are paralogues of the ubiquitous YidC/OxaI/Alb3 family of membraneintegral chaperones and insertases (71,78). Loss of any of the S. mutans SRP pathway components Ffh, scRNA, and FtsY, as well as YidC2, results in severe acid, osmotic, and oxidative stress sensitivity with decreased membrane-associated F-ATPase activity by the mutant strains (70).…”

Section: Discussionmentioning

confidence: 99%

Streptococcus mutans Extracellular DNA Is Upregulated during Growth in Biofilms, Actively Released via Membrane Vesicles, and Influenced by Components of the Protein Secretion Machinery

et al. 2014

Self Cite

View full text Add to dashboard Cite

f Streptococcus mutans, a major etiological agent of human dental caries, lives primarily on the tooth surface in biofilms. Limited information is available concerning the extracellular DNA (eDNA) as a scaffolding matrix in S. mutans biofilms. This study demonstrates that S. mutans produces eDNA by multiple avenues, including lysis-independent membrane vesicles. Unlike eDNAs from cell lysis that were abundant and mainly concentrated around broken cells or cell debris with floating open ends, eDNAs produced via the lysis-independent pathway appeared scattered but in a structured network under scanning electron microscopy. Compared to eDNA production of planktonic cultures, eDNA production in 5-and 24-h biofilms was increased by >3-and >1.6-fold, respectively. The addition of DNase I to growth medium significantly reduced biofilm formation. In an in vitro adherence assay, added chromosomal DNA alone had a limited effect on S. mutans adherence to saliva-coated hydroxylapatite beads, but in conjunction with glucans synthesized using purified glucosyltransferase B, the adherence was significantly enhanced. Deletion of sortase A, the transpeptidase that covalently couples multiple surface-associated proteins to the cell wall peptidoglycan, significantly reduced eDNA in both planktonic and biofilm cultures. Sortase A deficiency did not have a significant effect on membrane vesicle production; however, the protein profile of the mutant membrane vesicles was significantly altered, including reduction of adhesin P1 and glucan-binding proteins B and C. Relative to the wild type, deficiency of protein secretion and membrane protein insertion machinery components, including Ffh, YidC1, and YidC2, also caused significant reductions in eDNA.

show abstract

“…Full-length YidC2, but not YidC1 or YidC2, lacking the C-terminal tail, supports cotranslational insertion into the mitochondrial inner membrane of oxa1 -deficient S. cerevisiae mutants (Funes et al , 2009 ). Appending YidC1 with the YidC2 C terminus allows YidC1 to complement the stress sensitivity of a Δ yidC2 strain (Palmer et al , 2012 ). However, in the case of the B. subtilis SpoIIIJ and YqjG, the C termini are both very short ( ∼ 15 amino acids), and such a classification seems not apparent.…”

Section: Protein Targetingmentioning

confidence: 99%

The YidC/Oxa1/Alb3 protein family: common principles and distinct features

Saller

Keyzer

et al. 2012

Biological Chemistry

View full text Add to dashboard Cite

The members of the YidC/Oxa1/Alb3 protein family are evolutionary conserved in all three domains of life. They facilitate the insertion of membrane proteins into bacterial, mitochondrial, and thylakoid membranes and have been implicated in membrane protein folding and complex formation. The major classes of substrates are small hydrophobic subunits of large energy-transducing complexes involved in respiration and light capturing. All YidC-like proteins share a conserved membrane region, whereas the N- and C-terminal regions are diverse and fulfill accessory functions in protein targeting.

show abstract

YidC1 and YidC2 are functionally distinct proteins involved in protein secretion, biofilm formation and cariogenicity of Streptococcus mutans

Cited by 43 publications

References 42 publications

Interaction of Streptococcus mutans YidC1 and YidC2 with Translating and Nontranslating Ribosomes

Interaction of Streptococcus mutans YidC1 and YidC2 with Translating and Nontranslating Ribosomes

Streptococcus mutans Extracellular DNA Is Upregulated during Growth in Biofilms, Actively Released via Membrane Vesicles, and Influenced by Components of the Protein Secretion Machinery

The YidC/Oxa1/Alb3 protein family: common principles and distinct features

Contact Info

Product

Resources

About