PG0026 Is the C-terminal Signal Peptidase of a Novel Secretion System of Porphyromonas gingivalis

Glew, Michelle D.; Veith, Paul D.; Peng, Bo; Chen, Yu‐Yen; Gorasia, Dhana G.; Yang, Qiaohui; Slakeski, Nada; Chen, Dina; Moore, Caroline B.; Crawford, Simon; Reynolds, Eric C.

doi:10.1074/jbc.m112.369223

Cited by 129 publications

(236 citation statements)

References 43 publications

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“…Targeting of these proteins to the PorSS may involve conserved C-terminal domains (CTDs) that are found on proteins known to be secreted by PorSSs (14,(57)(58)(59)(60)(61). Consistent with this, each of the genomes of the organisms predicted to have PorSSs encoded many proteins with conserved PorSS-type CTDs identified by the TIGRFAMs, TIGR04131 and TIGR04183, whereas all but two of the remaining bacteria had few, if any, genes encoding proteins with these conserved domains.…”

Section: Resultsmentioning

confidence: 69%

Gliding Motility and Por Secretion System Genes Are Widespread among Members of the Phylum Bacteroidetes

2013

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The phylum Bacteroidetes is large and diverse, with rapid gliding motility and the ability to digest macromolecules associated with many genera and species. Recently, a novel protein secretion system, the Por secretion system (PorSS), was identified in two members of the phylum, the gliding bacterium Flavobacterium johnsoniae and the nonmotile oral pathogen Porphyromonas gingivalis. The components of the PorSS are not similar in sequence to those of other well-studied bacterial secretion systems. The F. johnsoniae PorSS genes are a subset of the gliding motility genes, suggesting a role for the secretion system in motility. The F. johnsoniae PorSS is needed for assembly of the gliding motility apparatus and for secretion of a chitinase, and the P. gingivalis PorSS is involved in secretion of gingipain protease virulence factors. Comparative analysis of 37 genomes of members of the phylum Bacteroidetes revealed the widespread occurrence of gliding motility genes and PorSS genes. Genes associated with other bacterial protein secretion systems were less common. The results suggest that gliding motility is more common than previously reported. Microscopic observations confirmed that organisms previously described as nonmotile, including Croceibacter atlanticus, "Gramella forsetii," Paludibacter propionicigenes, Riemerella anatipestifer, and Robiginitalea biformata, exhibit gliding motility. Three genes (gldA, gldF, and gldG) that encode an apparent ATP-binding cassette transporter required for F. johnsoniae gliding were absent from two related gliding bacteria, suggesting that the transporter may not be central to gliding motility.

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Section: Resultsmentioning

confidence: 69%

Gliding Motility and Por Secretion System Genes Are Widespread among Members of the Phylum Bacteroidetes

2013

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“…As the first corresponds to the calculated molecular mass of 134 kDa, the second appears to be partially modified after morphogenesis. Notably, CTD proteins are extensively modified with anionic lipopolysaccharide (A-LPS) after T9SS-dependent translocation and therefore migrate as diffuse bands in SDS-PAGE with molecular masses generally 20 kDa higher than expected from the sequence (Glew et al 2012). A-LPS modification of CTD proteins has suggested a role for CTDs in export, at the modification site after their release, and cell surface attachment (Seers et al 2006;Shoji et al 2011).…”

Section: Discussionmentioning

confidence: 99%

“…The P. gingivalis T9SS comprises more than 10 proteins, including PorK, PorL, PorM, PorN, PorP, PorQ, PorT, PorU, PorV, PorW, and Sov (Nakayama 2015). The proteins secreted by the T9SS all have conserved C-terminal domains (CTDs) that are removed by PorU, a C-terminal signal peptidase (Glew et al 2012) when these proteins are exported and attached to the cell surface. RgpA, RgpB, and Kgp are examples of CTD-containing virulence factors that are translocated across the outer membrane by the T9SS (Sato et al 2010;Shoji et al 2011;Nakayama 2015).…”

Section: Introductionmentioning

confidence: 99%

Role of Mfa5 in Expression of Mfa1 Fimbriae in Porphyromonas gingivalis

et al. 2016

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Fimbriae are protein-based filamentous appendages that protrude from the bacterial cell surface and facilitate host adhesion. Two types of fimbriae, FimA and Mfa1, of the periodontal pathogen Porphyromonas gingivalis are responsible for adherence to other bacteria and to host cells in the oral cavity. Both fimbrial forms are composed of 5 proteins, but there is limited information about their polymerization mechanisms. Here, the authors evaluated the function of Mfa5, one of the Mfa1 fimbrial accessory proteins. Using mfa5 gene disruption and complementation studies, the authors revealed that Mfa5 affects the incorporation of other accessory proteins, Mfa3 and Mfa4, into fibers and the expression of fimbriae on the cell surface. Mfa5 is predicted to have a C-terminal domain (CTD) that uses the type IX secretion system (T9SS), which is limited to this organism and related Bacteroidetes species, for translocation across the outer membrane. To determine the relationship between the putative Mfa5 CTD and the T9SS, mutants were constructed with in-frame deletion of the CTD and deletion of porU, a C-terminal signal peptidase linked to T9SS-mediated secretion. The ∆CTD-expressing strain presented a similar phenotype to the mfa5 disruption mutant with reduced expression of fimbriae lacking all accessory proteins. The ∆porU mutants and the ∆CTD-expressing strain showed intracellular accumulation of Mfa5. These results indicate that Mfa5 function requires T9SS-mediated translocation across the outer membrane, which is dependent on the CTD, and subsequent incorporation into fibers. These findings suggest the presence of a novel polymerization mechanism of the P. gingivalis fimbriae.

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“…They have been studied not only in F. johnsoniae but also in the nonmotile oral pathogen Porphyromonas gingivalis, which uses its T9SS to secrete gingipain protease virulence factors and other proteins (6,7,21). Proteins secreted by T9SSs have N-terminal signal peptides, allowing transit across the cytoplasmic membrane via the Sec system, and conserved C-terminal domains (CTDs) that are thought to target the proteins to the T9SS (5,7,18,(22)(23)(24)(25). These CTDs typically belong to TIGRFAM family TIGR04131 or TIGR04183.…”

mentioning

confidence: 99%

Flavobacterium johnsoniae Chitinase ChiA Is Required for Chitin Utilization and Is Secreted by the Type IX Secretion System

Kharade

McBride

2013

Journal of Bacteriology

110

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Flavobacterium johnsoniae, a member of phylum Bacteriodetes, is a gliding bacterium that digests insoluble chitin and many other polysaccharides. A novel protein secretion system, the type IX secretion system (T9SS), is required for gliding motility and for chitin utilization. Five potential chitinases were identified by genome analysis. Fjoh_4555 (ChiA), a 168.9-kDa protein with two glycoside hydrolase family 18 (GH18) domains, was targeted for analysis. Disruption of chiA by insertional mutagenesis resulted in cells that failed to digest chitin, and complementation with wild-type chiA on a plasmid restored chitin utilization. Antiserum raised against recombinant ChiA was used to detect the protein and to characterize its secretion by F. johnsoniae. ChiA was secreted in soluble form by wild-type cells but remained cell associated in strains carrying mutations in any of the T9SS genes, gldK, gldL, gldM, gldNO, sprA, sprE, and sprT. Western blot and liquid chromatography-tandem mass spectrometry (LC-MS/MS) analyses suggested that ChiA was proteolytically processed into two GH18 domain-containing proteins. Proteins secreted by T9SSs typically have conserved carboxy-terminal domains (CTDs) belonging to the TIGRFAM families TIGR04131 and TIGR04183. ChiA does not exhibit strong similarity to these sequences and instead has a novel CTD. Deletion of this CTD resulted in accumulation of ChiA inside cells. Fusion of the ChiA CTD to recombinant mCherry resulted in secretion of mCherry into the medium. The results indicate that ChiA is a soluble extracellular chitinase required for chitin utilization and that it relies on a novel CTD for secretion by the F. johnsoniae T9SS.

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PG0026 Is the C-terminal Signal Peptidase of a Novel Secretion System of Porphyromonas gingivalis

Cited by 129 publications

References 43 publications

Gliding Motility and Por Secretion System Genes Are Widespread among Members of the Phylum Bacteroidetes

Gliding Motility and Por Secretion System Genes Are Widespread among Members of the Phylum Bacteroidetes

Role of Mfa5 in Expression of Mfa1 Fimbriae in Porphyromonas gingivalis

Flavobacterium johnsoniae Chitinase ChiA Is Required for Chitin Utilization and Is Secreted by the Type IX Secretion System

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