The Evolution of Protein Secretion Systems by Co-option and Tinkering of Cellular Machineries

Denise, Rémi; Abby, Sophie S.; Rocha, Eduardo P. C.

doi:10.1016/j.tim.2020.01.005

Cited by 51 publications

(53 citation statements)

References 110 publications

(113 reference statements)

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“…III secretion systems for provisioning peptides or signal factors to the aphid host 13 . Indeed, the proteins retained in the Buchnera flagellum constitute the structural proteins and machinery required for a functional type III secretion system 21 Sucrose (Sigma-Aldrich) at pH 7.5).…”

Section: Discussionmentioning

confidence: 99%

“…As Buchnera is not motile and is confined to host-derived "symbiosomal" vesicles inside bacteriocytes 28 , 29 , the retention and expression of these partial flagella indicates that they have become repurposed. These complexes have previously been hypothesized to be acting as type III secretion systems for provisioning peptides or signal factors to the aphid host 13 . Indeed, the proteins retained in the Buchnera flagellum constitute the structural proteins and machinery required for a functional type III secretion system 21 Further inquiry into this protein complex could reveal how the repurposing of a motility organelle facilitates this ancient and obligate symbiosis.…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Isolation of theBuchnera aphidicolaflagellum basal body from theBuchneramembrane

Schepers

Yelland

Moran

et al. 2021

Preprint

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Buchnera aphidicola is an intracellular bacterial symbiont of aphids and maintains a small genome of only 600 kbps. Buchnera is thought to maintain only genes relevant to the symbiosis with its aphid host. Curiously, the Buchnera genome contains gene clusters coding for flagellum basal body structural proteins and for flagellum type III export machinery. These structures have been shown to be highly expressed and present in large numbers on Buchnera cells. No recognizable pathogenicity factors or secreted proteins have been identified in the Buchnera genome, and the relevance of this protein complex to the symbiosis is unknown. Here, we show isolation of Buchnera flagella from the cellular membrane of Buchnera, confirming the enrichment of flagellum proteins relative to other proteins in the Buchnera proteome. This will facilitate studies of the structure and function of the Buchnera flagellum structure, and its role in this model symbiosis.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Isolation of theBuchnera aphidicolaflagellum basal body from theBuchneramembrane

Schepers

Yelland

Moran

et al. 2021

Preprint

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“…Almost all Gram-negative bacteria and a subset of Gram-positive bacteria express type IV pili (T4p) ( 4 ). There are three major subsets of T4p, and there is a clear evolutionarily relationship with type II secretion systems (T2S) and archaeal flagella ( 5 ). T4p provide a wide range of phenotypes to the organisms that express them and are important organelles that promote bacterial colonization and pathogenesis.…”

Section: Introductionmentioning

confidence: 99%

Discovery of a New Neisseria gonorrhoeae Type IV Pilus Assembly Factor, TfpC

Yin

Ozer

et al. 2020

mBio

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Neisseria gonorrhoeae relies on type IV pili (T4p) to promote colonization of their human host and to cause the sexually transmitted infection gonorrhea. This organelle cycles through a process of extension and retraction back into the bacterial cell. Through a genetic screen, we identified the NGO0783 locus of N. gonorrhoeae strain FA1090 as containing a gene encoding a protein required to stabilize the type IV pilus in its extended, nonretracted conformation. We have named the gene tfpC and the protein TfpC. Deletion of tfpC produces a nonpiliated colony morphology, and immuno-transmission electron microscopy confirms that the pili are lost in the ΔtfpC mutant, although there is some pilin detected near the bacterial cell surface. A copy of the tfpC gene expressed from a lac promoter restores pilus expression and related phenotypes. A ΔtfpC mutant shows reduced levels of pilin protein, but complementation with a tfpC gene restored pilin to normal levels. Bioinformatic searches show that there are orthologues in numerous bacterial species, but not all type IV pilin-expressing bacteria contain orthologous genes. Coevolution and nuclear magnetic resonance (NMR) analysis indicates that TfpC contains an N-terminal transmembrane helix, a substantial extended/unstructured region, and a highly charged C-terminal coiled-coil domain. IMPORTANCE Most bacterial species express one or more extracellular organelles called pili/fimbriae that are required for many properties of each bacterial cell. The Neisseria gonorrhoeae type IV pilus is a major virulence and colonization factor for the sexually transmitted infection gonorrhea. We have discovered a new protein of Neisseria gonorrhoeae called TfpC that is required to maintain type IV pili on the bacterial cell surface. There are similar proteins found in other members of the Neisseria genus and many other bacterial species important for human health.

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“…Almost all Gram-negative bacteria and a subset of Gram-positive bacteria express T4p (4). There are three major subsets of T4p, and there is a clear evolutionarily relationship with Type II secretion system (T2S) and Archaeal flagella (5). T4p provide a wide range of phenotypes to the organisms that express them and are important organelles that promote bacterial colonization and pathogenesis.…”

Section: Introductionmentioning

confidence: 99%

Discovery of a newNeisseria gonorrhoeaeType IV pilus assembly factor, TfpC

Hu¹,

Yin²,

Ozer³

et al. 2020

Preprint

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Neisseria gonorrhoeae rely on Type IV pili (T4p) to promote colonization of their human host and to cause the sexually transmitted infection, gonorrhea. This organelle cycles through a process of extension and retraction back into the bacterial cell. Through a genetic screen, we identified the NGO0783 locus of N. gonorrhoeae strain FA1090 as containing a gene encoding a protein required to stabilize the Type IV pilus in its extended, non-retracted conformation. We have named the gene tfpC and the protein TfpC. Deletion of tfpC produces a nonpiliated colony morphology and immuno-transmission electron microscopy confirms that the pili are lost in the ΔtfpC mutant, although there is some pilin detected near the bacterial cell surface. A copy of the tfpC gene expressed from a lac promoter restores pilus expression and related phenotypes. A ΔtfpC mutant shows reduced levels of pilin protein, but complementation with a tfpC gene restored pilin to normal levels. Bioinformatic searches show there are orthologues in numerous bacteria species but not all Type IV pilin expressing bacteria contain orthologous genes. Co-evolution and NMR analysis indicates that TfpC contains an N-terminal transmembrane helix, a substantial extended/unstructured region and a highly charge C-terminal coiled-coil domain.ImportanceMost bacterial species express one or more extracellular organelles called pili/fimbriae that are required for many properties of each bacterial cell. The Neisseria gonorrhoeae Type IV pilus is a major virulence and colonization factor for the sexually transmitted infection, gonorrhea. We have discovered a new protein of Neisseria gonorrhoeae called TfpC that is required to maintain the Type IV pili on the bacterial cell surface. There are similar proteins found in the other members of the Neisseria genus and many other bacterial species important for human health.

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The Evolution of Protein Secretion Systems by Co-option and Tinkering of Cellular Machineries

Cited by 51 publications

References 110 publications

Isolation of theBuchnera aphidicolaflagellum basal body from theBuchneramembrane

Isolation of theBuchnera aphidicolaflagellum basal body from theBuchneramembrane

Discovery of a New Neisseria gonorrhoeae Type IV Pilus Assembly Factor, TfpC

Discovery of a newNeisseria gonorrhoeaeType IV pilus assembly factor, TfpC

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