Two-step and one-step secretion mechanisms in Gram-negative bacteria: contrasting the type IV secretion system and the chaperone-usher pathway of pilus biogenesis

Rêgo, Ana Toste; Chandran, Vidya; Waksman, Gabriel

doi:10.1042/bj20091518

Cited by 55 publications

(41 citation statements)

References 158 publications

(233 reference statements)

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“…They are also not similar to the components of the mycobacterial ESX pathway, which has been referred to as the type VII secretion system (25,26); the extracellular nucleation-precipitation (ENP) pathway involved in secretion and assembly of curly amyloid fibers, which has been proposed as the type VIII secretion system (27,28); or the components of the chaperone-usher pathway (29).…”

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confidence: 99%

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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confidence: 99%

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

2013

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“…The assembly of a large family of these appendages depends on the conserved chaperone-usher (CU) pathway (36,49). The pilin subunits that form these fibers initially cross the cytoplasmic membrane through the Sec translocon to reach the periplasmic space, where they bind to their cognate chaperones, forming binary complexes.…”

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confidence: 99%

The Fimbrial Usher FimD Follows the SurA-BamB Pathway for Its Assembly in the Outer Membrane of Escherichia coli

2011

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Fimbrial ushers are the largest ␤-barrel outer membrane proteins (OMPs) known to date, which function in the polymerization of fimbriae and their translocation to the bacterial surface. Folding and assembly of these complex OMPs are not characterized. Here, we investigate the role of periplasmic chaperones (SurA, Skp, DegP, and FkpA) and individual components of the ␤-barrel assembly machinery (BAM) complex (BamA, BamB, BamC, and BamE) in the folding of the Escherichia coli FimD usher. The FimD level is dramatically reduced (ϳ30-fold) in a surA null mutant, but a strong cell envelope stress is constitutively activated with upregulation of DegP (ϳ10-fold). To demonstrate a direct role of SurA, FimD folding was analyzed in a conditional surA mutant in which SurA expression was controlled. In this strain, FimD is depleted from bacteria in parallel to SurA without significant upregulation of DegP. Interestingly, the dependency on SurA is higher for FimD than for other OMPs. We also demonstrate that a functional BAM complex is needed for folding of FimD. In addition, FimD levels were strongly reduced (ϳ5-fold) in a mutant lacking the accessory lipoprotein BamB. The critical role of BamB for FimD folding was confirmed by complementation and BamB depletion experiments. Similar to SurA dependency, FimD showed a stronger dependency on BamB than OMPs. On the other hand, folding of FimD was only marginally affected in bamC and bamE mutants. Collectively, our results indicate that FimD usher follows the SurA-BamB pathway for its assembly. The preferential use of this pathway for the folding of OMPs with large ␤-barrels is discussed.Gram-negative bacteria display on their surfaces adhesive multimeric protein fibers known as pili, fimbriae, or fibrillae that mediate attachment to host cells and tissues for colonization and infection (12,24). The assembly of a large family of these appendages depends on the conserved chaperone-usher (CU) pathway (36, 49). The pilin subunits that form these fibers initially cross the cytoplasmic membrane through the Sec translocon to reach the periplasmic space, where they bind to their cognate chaperones, forming binary complexes. These complexes are specifically targeted to the usher, a ϳ90-kDa integral outer membrane protein (OMP), that catalyzes the polymerization of pilin subunits in an ordered manner and secretes the resulting protein fiber to the bacterial surface (32,34,37). Type 1 (fim) and P (pap) fimbriae from uropathogenic Escherichia coli (UPEC) strains have been established as paradigms of the CU pathway, and their respective chaperones and ushers are studied as models of these types of proteins. Biochemical and structural studies of the usher proteins of type 1 and P fimbriae (named FimD and PapC, respectively) indicate that these proteins may form dimers in the OM and contain the largest ␤-barrel known to date in OMPs, with 24 antiparallel ␤-strands (18,34,37). In addition to the large ␤-barrel domain, FimD and PapC ushers contain several globular domains, including periplasmic ...

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“…It is composed of Sec proteins, SecA (ATPase) and SecYEG. The other Tat (Twin Arginine Translocation) pathway is made of TatABC proteins and it is not considered essential as Sec [3,4]. T3SS is a needle like structure.…”

Section: Introductionmentioning

confidence: 99%

Comparison of the Structure, Regulation and Functions between Type Three and Type Six Secretion System in Gram-Negative Bacteria

Badr¹,

Li²,

Duan³

2016

J Med Microb Diagn

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Bacteria have evolved multiple protein secretion systems to survive and cope with surrounding environmental stresses. So far, there are seven secretion systems (type I to type VII), which have been identified and demonstrated the structural and molecular mechanisms. Among them, type three secretion system (T3SS), hallmark of acute infection, is considered as the most complicated system and can translocate effector proteins directly into host cell through a needle-like apparatus. Type six secretion system (T6SS) targets both prokaryotic and eukaryotic cells using a bacteriophage-like structure and plays a role in pathogenesis and bacterial competition. This review is based on our understanding of comparison of the structure, regulation, function and application between T3SS and T6SS. Understanding the structural and functional mechanisms, as well as the difference and relationship between these two secretion systems will help our understanding of bacterial pathogenesis and interspecies interaction.

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Two-step and one-step secretion mechanisms in Gram-negative bacteria: contrasting the type IV secretion system and the chaperone-usher pathway of pilus biogenesis

Cited by 55 publications

References 158 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

The Fimbrial Usher FimD Follows the SurA-BamB Pathway for Its Assembly in the Outer Membrane of Escherichia coli

Comparison of the Structure, Regulation and Functions between Type Three and Type Six Secretion System in Gram-Negative Bacteria

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