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α-Hydroxyketone synthesis and sensing by Legionella and Vibrio.

Tiaden A, Hilbi H - Sensors (Basel) (2012)

Bottom Line: AHK signaling regulates the virulence of L. pneumophila and V. cholerae, pathogen-host cell interactions, formation of biofilms or extracellular filaments, expression of a genomic "fitness island" and competence.Here, we outline the processes, wherein AHK signaling plays a role, and review recent insights into the function of proteins encoded by the lqs and cqs gene clusters.To this end, we will focus on the autoinducer synthases catalysing the biosynthesis of AHKs, on the cognate trans-membrane sensor kinases detecting the signals, and on components of the down-stream phosphorelay cascade that promote the transmission and integration of signaling events regulating gene expression.

View Article: PubMed Central - PubMed

Affiliation: Competence Center for Applied Biotechnology and Molecular Medicine, University Zürich, Zürich, Switzerland. nicki.tiaden@cabmm.uzh.ch

ABSTRACT
Bacteria synthesize and sense low molecular weight signaling molecules, termed autoinducers, to measure their population density and community complexity. One class of autoinducers, the α-hydroxyketones (AHKs), is produced and detected by the water-borne opportunistic pathogens Legionella pneumophila and Vibrio cholerae, which cause Legionnaires' disease and cholera, respectively. The "Legionella quorum sensing" (lqs) or "cholera quorum sensing" (cqs) genes encode enzymes that produce and sense the AHK molecules "Legionella autoinducer-1" (LAI-1; 3-hydroxypentadecane-4-one) or cholera autoinducer-1 (CAI-1; 3-hydroxytridecane-4-one). AHK signaling regulates the virulence of L. pneumophila and V. cholerae, pathogen-host cell interactions, formation of biofilms or extracellular filaments, expression of a genomic "fitness island" and competence. Here, we outline the processes, wherein AHK signaling plays a role, and review recent insights into the function of proteins encoded by the lqs and cqs gene clusters. To this end, we will focus on the autoinducer synthases catalysing the biosynthesis of AHKs, on the cognate trans-membrane sensor kinases detecting the signals, and on components of the down-stream phosphorelay cascade that promote the transmission and integration of signaling events regulating gene expression.

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Genetic organization of the V. cholerae (cqs) and L. pneumophila (lqs) QS locus, and biosynthesis of AIs produced by CqsA and LqsA. (a) The cqs and lqs loci harbour AI synthases (cqsA, lqsA), cognate sensor kinases (cqsS, lqsS) and a response regulator (lqsR). AI molecules synthesized by V.chCqsA and L.pnLqsA: (a) CAI-1 and LAI-1 AHKs, and (b) C3-amino-derivatives of CAI-1 (Am-CAI-1 and Ea-CAI-1). (c) Biosynthesis of CAI-1 and C3-amino-derivatives by PLP-dependent V. cholerae and V. harveyi CqsA and presumably L. pneumophila LqsA using (S)-3-aminobutyrate (SAB) or (S)-adenosylmethionine (SAM) and acyl-CoAs. V.chCqsA utilizes decanoyl-CoA (C10) or octanoyl-CoA (C8) to produce Am-CAI-1/Ea-CAI-1 (C13) or Am-C8-CAI-1/Ea-C8-CAI-1 (C11). Ea-CAI-1 is converted into CAI-1 by spontaneous hydrolysis and a dehydrogenase. The intermediate Am-CAI-1 is converted into CAI-1 by an unknown mechanism. V.haCqsA utilizes only octanoyl-CoA to yield Am-C8-CAI-1/Ea-C8-CAI-1 and C8-CAI-1 (C11). Synthesis of LAI-1 (C15) by L.pnLqsA is not elucidated, but might use SAM (or SAB) and dodecanoyl-CoA (C12).
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f1-sensors-12-02899: Genetic organization of the V. cholerae (cqs) and L. pneumophila (lqs) QS locus, and biosynthesis of AIs produced by CqsA and LqsA. (a) The cqs and lqs loci harbour AI synthases (cqsA, lqsA), cognate sensor kinases (cqsS, lqsS) and a response regulator (lqsR). AI molecules synthesized by V.chCqsA and L.pnLqsA: (a) CAI-1 and LAI-1 AHKs, and (b) C3-amino-derivatives of CAI-1 (Am-CAI-1 and Ea-CAI-1). (c) Biosynthesis of CAI-1 and C3-amino-derivatives by PLP-dependent V. cholerae and V. harveyi CqsA and presumably L. pneumophila LqsA using (S)-3-aminobutyrate (SAB) or (S)-adenosylmethionine (SAM) and acyl-CoAs. V.chCqsA utilizes decanoyl-CoA (C10) or octanoyl-CoA (C8) to produce Am-CAI-1/Ea-CAI-1 (C13) or Am-C8-CAI-1/Ea-C8-CAI-1 (C11). Ea-CAI-1 is converted into CAI-1 by spontaneous hydrolysis and a dehydrogenase. The intermediate Am-CAI-1 is converted into CAI-1 by an unknown mechanism. V.haCqsA utilizes only octanoyl-CoA to yield Am-C8-CAI-1/Ea-C8-CAI-1 and C8-CAI-1 (C11). Synthesis of LAI-1 (C15) by L.pnLqsA is not elucidated, but might use SAM (or SAB) and dodecanoyl-CoA (C12).

Mentions: Species-specific modifications and derivatives of these basic compounds are found in virtually every bacterial genus, thus yielding a rich microcosm of microbial signal molecules. Many Gram-negative bacteria generate AIs that belong to the first discovered class of N-acyl-L-homoserine lactones (AHLs) [2], and/or they produce the almost universally used furanosyl borate diester termed autoinducer-2 (AI-2) [6,7]. Some bacteria utilize additional AIs to regulate gene expression. A class of α,β-unsaturated fatty acids termed diffusible signal factors (DSFs) plays a prominent role in soil- and plant-associated bacteria such as Xanthomonas, Burkholderia or Pseudomonas spp. [8]. Finally, the recently discovered α-hydroxyketones (AHKs) are predominantly produced by aquatic γ-proteobacteria, including Legionella and Vibrio spp. (Figure 1(a)) [9].


α-Hydroxyketone synthesis and sensing by Legionella and Vibrio.

Tiaden A, Hilbi H - Sensors (Basel) (2012)

Genetic organization of the V. cholerae (cqs) and L. pneumophila (lqs) QS locus, and biosynthesis of AIs produced by CqsA and LqsA. (a) The cqs and lqs loci harbour AI synthases (cqsA, lqsA), cognate sensor kinases (cqsS, lqsS) and a response regulator (lqsR). AI molecules synthesized by V.chCqsA and L.pnLqsA: (a) CAI-1 and LAI-1 AHKs, and (b) C3-amino-derivatives of CAI-1 (Am-CAI-1 and Ea-CAI-1). (c) Biosynthesis of CAI-1 and C3-amino-derivatives by PLP-dependent V. cholerae and V. harveyi CqsA and presumably L. pneumophila LqsA using (S)-3-aminobutyrate (SAB) or (S)-adenosylmethionine (SAM) and acyl-CoAs. V.chCqsA utilizes decanoyl-CoA (C10) or octanoyl-CoA (C8) to produce Am-CAI-1/Ea-CAI-1 (C13) or Am-C8-CAI-1/Ea-C8-CAI-1 (C11). Ea-CAI-1 is converted into CAI-1 by spontaneous hydrolysis and a dehydrogenase. The intermediate Am-CAI-1 is converted into CAI-1 by an unknown mechanism. V.haCqsA utilizes only octanoyl-CoA to yield Am-C8-CAI-1/Ea-C8-CAI-1 and C8-CAI-1 (C11). Synthesis of LAI-1 (C15) by L.pnLqsA is not elucidated, but might use SAM (or SAB) and dodecanoyl-CoA (C12).
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Related In: Results  -  Collection

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f1-sensors-12-02899: Genetic organization of the V. cholerae (cqs) and L. pneumophila (lqs) QS locus, and biosynthesis of AIs produced by CqsA and LqsA. (a) The cqs and lqs loci harbour AI synthases (cqsA, lqsA), cognate sensor kinases (cqsS, lqsS) and a response regulator (lqsR). AI molecules synthesized by V.chCqsA and L.pnLqsA: (a) CAI-1 and LAI-1 AHKs, and (b) C3-amino-derivatives of CAI-1 (Am-CAI-1 and Ea-CAI-1). (c) Biosynthesis of CAI-1 and C3-amino-derivatives by PLP-dependent V. cholerae and V. harveyi CqsA and presumably L. pneumophila LqsA using (S)-3-aminobutyrate (SAB) or (S)-adenosylmethionine (SAM) and acyl-CoAs. V.chCqsA utilizes decanoyl-CoA (C10) or octanoyl-CoA (C8) to produce Am-CAI-1/Ea-CAI-1 (C13) or Am-C8-CAI-1/Ea-C8-CAI-1 (C11). Ea-CAI-1 is converted into CAI-1 by spontaneous hydrolysis and a dehydrogenase. The intermediate Am-CAI-1 is converted into CAI-1 by an unknown mechanism. V.haCqsA utilizes only octanoyl-CoA to yield Am-C8-CAI-1/Ea-C8-CAI-1 and C8-CAI-1 (C11). Synthesis of LAI-1 (C15) by L.pnLqsA is not elucidated, but might use SAM (or SAB) and dodecanoyl-CoA (C12).
Mentions: Species-specific modifications and derivatives of these basic compounds are found in virtually every bacterial genus, thus yielding a rich microcosm of microbial signal molecules. Many Gram-negative bacteria generate AIs that belong to the first discovered class of N-acyl-L-homoserine lactones (AHLs) [2], and/or they produce the almost universally used furanosyl borate diester termed autoinducer-2 (AI-2) [6,7]. Some bacteria utilize additional AIs to regulate gene expression. A class of α,β-unsaturated fatty acids termed diffusible signal factors (DSFs) plays a prominent role in soil- and plant-associated bacteria such as Xanthomonas, Burkholderia or Pseudomonas spp. [8]. Finally, the recently discovered α-hydroxyketones (AHKs) are predominantly produced by aquatic γ-proteobacteria, including Legionella and Vibrio spp. (Figure 1(a)) [9].

Bottom Line: AHK signaling regulates the virulence of L. pneumophila and V. cholerae, pathogen-host cell interactions, formation of biofilms or extracellular filaments, expression of a genomic "fitness island" and competence.Here, we outline the processes, wherein AHK signaling plays a role, and review recent insights into the function of proteins encoded by the lqs and cqs gene clusters.To this end, we will focus on the autoinducer synthases catalysing the biosynthesis of AHKs, on the cognate trans-membrane sensor kinases detecting the signals, and on components of the down-stream phosphorelay cascade that promote the transmission and integration of signaling events regulating gene expression.

View Article: PubMed Central - PubMed

Affiliation: Competence Center for Applied Biotechnology and Molecular Medicine, University Zürich, Zürich, Switzerland. nicki.tiaden@cabmm.uzh.ch

ABSTRACT
Bacteria synthesize and sense low molecular weight signaling molecules, termed autoinducers, to measure their population density and community complexity. One class of autoinducers, the α-hydroxyketones (AHKs), is produced and detected by the water-borne opportunistic pathogens Legionella pneumophila and Vibrio cholerae, which cause Legionnaires' disease and cholera, respectively. The "Legionella quorum sensing" (lqs) or "cholera quorum sensing" (cqs) genes encode enzymes that produce and sense the AHK molecules "Legionella autoinducer-1" (LAI-1; 3-hydroxypentadecane-4-one) or cholera autoinducer-1 (CAI-1; 3-hydroxytridecane-4-one). AHK signaling regulates the virulence of L. pneumophila and V. cholerae, pathogen-host cell interactions, formation of biofilms or extracellular filaments, expression of a genomic "fitness island" and competence. Here, we outline the processes, wherein AHK signaling plays a role, and review recent insights into the function of proteins encoded by the lqs and cqs gene clusters. To this end, we will focus on the autoinducer synthases catalysing the biosynthesis of AHKs, on the cognate trans-membrane sensor kinases detecting the signals, and on components of the down-stream phosphorelay cascade that promote the transmission and integration of signaling events regulating gene expression.

Show MeSH
Related in: MedlinePlus