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Protein Secretion Systems in Pseudomonas aeruginosa: An Essay on Diversity, Evolution, and Function.

Filloux A - Front Microbiol (2011)

Bottom Line: This diversity may result from a progressive transformation of cell envelope complexes that initially may not have been dedicated to secretion.Instead of listing secretion types one after each other, it presents a melting pot of concepts indicating that secretion types are in constant evolution and use basic principles.In other words, emergence of new secretion systems could be predicted the way Mendeleïev had anticipated characteristics of yet unknown elements.

View Article: PubMed Central - PubMed

Affiliation: Division of Cell and Molecular Biology, Centre for Molecular Microbiology and Infection, Imperial College London London, UK.

ABSTRACT
Protein secretion systems are molecular nanomachines used by Gram-negative bacteria to thrive within their environment. They are used to release enzymes that hydrolyze complex carbon sources into usable compounds, or to release proteins that capture essential ions such as iron. They are also used to colonize and survive within eukaryotic hosts, causing acute or chronic infections, subverting the host cell response and escaping the immune system. In this article, the opportunistic human pathogen Pseudomonas aeruginosa is used as a model to review the diversity of secretion systems that bacteria have evolved to achieve these goals. This diversity may result from a progressive transformation of cell envelope complexes that initially may not have been dedicated to secretion. The striking similarities between secretion systems and type IV pili, flagella, bacteriophage tail, or efflux pumps is a nice illustration of this evolution. Differences are also needed since various secretion configurations call for diversity. For example, some proteins are released in the extracellular medium while others are directly injected into the cytosol of eukaryotic cells. Some proteins are folded before being released and transit into the periplasm. Other proteins cross the whole cell envelope at once in an unfolded state. However, the secretion system requires conserved basic elements or features. For example, there is a need for an energy source or for an outer membrane channel. The structure of this review is thus quite unconventional. Instead of listing secretion types one after each other, it presents a melting pot of concepts indicating that secretion types are in constant evolution and use basic principles. In other words, emergence of new secretion systems could be predicted the way Mendeleïev had anticipated characteristics of yet unknown elements.

No MeSH data available.


Related in: MedlinePlus

Structure of the P. aeruginosa EstA autotransporter (T5aSS), reproduced from van den Berg (2010). (A) Backbone representation viewed from the side, with the protein colored by a gradient from blue at the N-terminus to red at the C-terminus. (B) Backbone view 90° rotated within the plane of the membrane relative to (A), with helices colored red, β-strands colored green, and loops colored gray. The catalytic triad residues are shown as blue stick models. Horizontal lines indicate the approximate location of the outer membrane core. (C) Surface view of EstA from the side with the β-barrel domain colored green and the passenger domain colored red. (D) Stereo view of the EstA passenger from the extracellular side, colored as a rainbow from dark blue at the N-terminus to dark red at the C-terminus. The numbers are those for the central residue of the α-helix.
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Figure 1: Structure of the P. aeruginosa EstA autotransporter (T5aSS), reproduced from van den Berg (2010). (A) Backbone representation viewed from the side, with the protein colored by a gradient from blue at the N-terminus to red at the C-terminus. (B) Backbone view 90° rotated within the plane of the membrane relative to (A), with helices colored red, β-strands colored green, and loops colored gray. The catalytic triad residues are shown as blue stick models. Horizontal lines indicate the approximate location of the outer membrane core. (C) Surface view of EstA from the side with the β-barrel domain colored green and the passenger domain colored red. (D) Stereo view of the EstA passenger from the extracellular side, colored as a rainbow from dark blue at the N-terminus to dark red at the C-terminus. The numbers are those for the central residue of the α-helix.

Mentions: The type V secretion system is the most simple of all. It was originally described for the IgA protease in Neisseria gonorrhoeae (Pohlner et al., 1987). Basically, all the secretion information is contained within one single polypeptide. The protein has a cleavable signal peptide for targeting to the periplasm by the Sec system and a C-terminal domain that forms a β-barrel structure into the outer membrane. The passenger, or protease domain, could travel through the channel formed by theβ-barrel. This is still under debate since other studies indicate that the β-barrel of the autotransporter hemoglobin protease might not be fully folded and inserted in the outer membrane while the passenger domain is already accessible from the surface (Sauri et al., 2009). An alternative transport pathway in this case may involve the Bam/Omp85 complex. Once exposed to the cell surface the protease is released from the β-barrel via autocatalytic cleavage. Because there is no need for accessory proteins to help the secretion process, the mechanism was called autotransporter and coined Type Va secretion system (T5aSS; Dautin and Bernstein, 2007; Yen et al., 2008). The P. aeruginosa PAO1 genome contains three genes encoding proteins with a typical autotransporter C-terminal β-barrel attached to a N-terminal passenger domain. Two, PA3535 ad PA0328, have not been functionally characterized but are predicted to carry serine protease and metallopeptidase activity, respectively. In contrast, EstA has been extensively characterized. It has lipolytic activity (Wilhelm et al., 1999) and its 3D structure has been solved (Figure 1; van den Berg, 2010). The passenger domain is a member of the GDSL family of lipases (Akoh et al., 2004). The structure shows that the size of the barrel is too narrow to accommodate a folded protein and therefore translocation across the outer membrane should occur in an unfolded state. It is suggested that the EstA passenger may fold sequentially starting from the C-terminus. The vectorial passenger folding provides the driving force for the translocation. The catalytic triad is located on the apical surface of the passenger protein. Finally, there is a central α-helix that connects the extracellular passenger to the periplasmic side of the β-barrel that further suggests that the passenger is traveling through the channel. In this case the so-called secreted protein remains anchored at the bacterial surface and is not released into the supernatant.


Protein Secretion Systems in Pseudomonas aeruginosa: An Essay on Diversity, Evolution, and Function.

Filloux A - Front Microbiol (2011)

Structure of the P. aeruginosa EstA autotransporter (T5aSS), reproduced from van den Berg (2010). (A) Backbone representation viewed from the side, with the protein colored by a gradient from blue at the N-terminus to red at the C-terminus. (B) Backbone view 90° rotated within the plane of the membrane relative to (A), with helices colored red, β-strands colored green, and loops colored gray. The catalytic triad residues are shown as blue stick models. Horizontal lines indicate the approximate location of the outer membrane core. (C) Surface view of EstA from the side with the β-barrel domain colored green and the passenger domain colored red. (D) Stereo view of the EstA passenger from the extracellular side, colored as a rainbow from dark blue at the N-terminus to dark red at the C-terminus. The numbers are those for the central residue of the α-helix.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3140646&req=5

Figure 1: Structure of the P. aeruginosa EstA autotransporter (T5aSS), reproduced from van den Berg (2010). (A) Backbone representation viewed from the side, with the protein colored by a gradient from blue at the N-terminus to red at the C-terminus. (B) Backbone view 90° rotated within the plane of the membrane relative to (A), with helices colored red, β-strands colored green, and loops colored gray. The catalytic triad residues are shown as blue stick models. Horizontal lines indicate the approximate location of the outer membrane core. (C) Surface view of EstA from the side with the β-barrel domain colored green and the passenger domain colored red. (D) Stereo view of the EstA passenger from the extracellular side, colored as a rainbow from dark blue at the N-terminus to dark red at the C-terminus. The numbers are those for the central residue of the α-helix.
Mentions: The type V secretion system is the most simple of all. It was originally described for the IgA protease in Neisseria gonorrhoeae (Pohlner et al., 1987). Basically, all the secretion information is contained within one single polypeptide. The protein has a cleavable signal peptide for targeting to the periplasm by the Sec system and a C-terminal domain that forms a β-barrel structure into the outer membrane. The passenger, or protease domain, could travel through the channel formed by theβ-barrel. This is still under debate since other studies indicate that the β-barrel of the autotransporter hemoglobin protease might not be fully folded and inserted in the outer membrane while the passenger domain is already accessible from the surface (Sauri et al., 2009). An alternative transport pathway in this case may involve the Bam/Omp85 complex. Once exposed to the cell surface the protease is released from the β-barrel via autocatalytic cleavage. Because there is no need for accessory proteins to help the secretion process, the mechanism was called autotransporter and coined Type Va secretion system (T5aSS; Dautin and Bernstein, 2007; Yen et al., 2008). The P. aeruginosa PAO1 genome contains three genes encoding proteins with a typical autotransporter C-terminal β-barrel attached to a N-terminal passenger domain. Two, PA3535 ad PA0328, have not been functionally characterized but are predicted to carry serine protease and metallopeptidase activity, respectively. In contrast, EstA has been extensively characterized. It has lipolytic activity (Wilhelm et al., 1999) and its 3D structure has been solved (Figure 1; van den Berg, 2010). The passenger domain is a member of the GDSL family of lipases (Akoh et al., 2004). The structure shows that the size of the barrel is too narrow to accommodate a folded protein and therefore translocation across the outer membrane should occur in an unfolded state. It is suggested that the EstA passenger may fold sequentially starting from the C-terminus. The vectorial passenger folding provides the driving force for the translocation. The catalytic triad is located on the apical surface of the passenger protein. Finally, there is a central α-helix that connects the extracellular passenger to the periplasmic side of the β-barrel that further suggests that the passenger is traveling through the channel. In this case the so-called secreted protein remains anchored at the bacterial surface and is not released into the supernatant.

Bottom Line: This diversity may result from a progressive transformation of cell envelope complexes that initially may not have been dedicated to secretion.Instead of listing secretion types one after each other, it presents a melting pot of concepts indicating that secretion types are in constant evolution and use basic principles.In other words, emergence of new secretion systems could be predicted the way Mendeleïev had anticipated characteristics of yet unknown elements.

View Article: PubMed Central - PubMed

Affiliation: Division of Cell and Molecular Biology, Centre for Molecular Microbiology and Infection, Imperial College London London, UK.

ABSTRACT
Protein secretion systems are molecular nanomachines used by Gram-negative bacteria to thrive within their environment. They are used to release enzymes that hydrolyze complex carbon sources into usable compounds, or to release proteins that capture essential ions such as iron. They are also used to colonize and survive within eukaryotic hosts, causing acute or chronic infections, subverting the host cell response and escaping the immune system. In this article, the opportunistic human pathogen Pseudomonas aeruginosa is used as a model to review the diversity of secretion systems that bacteria have evolved to achieve these goals. This diversity may result from a progressive transformation of cell envelope complexes that initially may not have been dedicated to secretion. The striking similarities between secretion systems and type IV pili, flagella, bacteriophage tail, or efflux pumps is a nice illustration of this evolution. Differences are also needed since various secretion configurations call for diversity. For example, some proteins are released in the extracellular medium while others are directly injected into the cytosol of eukaryotic cells. Some proteins are folded before being released and transit into the periplasm. Other proteins cross the whole cell envelope at once in an unfolded state. However, the secretion system requires conserved basic elements or features. For example, there is a need for an energy source or for an outer membrane channel. The structure of this review is thus quite unconventional. Instead of listing secretion types one after each other, it presents a melting pot of concepts indicating that secretion types are in constant evolution and use basic principles. In other words, emergence of new secretion systems could be predicted the way Mendeleïev had anticipated characteristics of yet unknown elements.

No MeSH data available.


Related in: MedlinePlus