Interplay between 4-Hydroxy-3-Methyl-2-Alkylquinoline and N-Acyl-Homoserine Lactone Signaling in a Burkholderia cepacia Complex Clinical Strain

Annelise Chapalain; Marie-Christine Groleau; Servane Le Guillouzer; Aurélie Miomandre; Ludovic Vial; Sylvain Milot; Eric Déziel

doi:10.3389/fmicb.2017.01021

Interplay between 4-Hydroxy-3-Methyl-2-Alkylquinoline and N-Acyl-Homoserine Lactone Signaling in a Burkholderia cepacia Complex Clinical Strain

Front Microbiol. 2017 Jun 20:8:1021. doi: 10.3389/fmicb.2017.01021. eCollection 2017.

Authors

Annelise Chapalain¹, Marie-Christine Groleau², Servane Le Guillouzer², Aurélie Miomandre³, Ludovic Vial³, Sylvain Milot², Eric Déziel²

Affiliations

¹ CIRI, Centre International de Recherche en Infectiologie, Equipe Pathogénèse des Légionelles, Inserm, U1111, Université Claude Bernard Lyon 1, CNRS, UMR5308, École Normale Supérieure de Lyon, Université LyonLyon, France.
² INRS-Institut Armand-Frappier, LavalQC, Canada.
³ CNRS, INRA, UMR 5557, Ecologie Microbienne, Université Lyon 1Villeurbanne, France.

Abstract

Species from the Burkholderia cepacia complex (Bcc) share a canonical LuxI/LuxR quorum sensing (QS) regulation system named CepI/CepR, which mainly relies on the acyl-homoserine lactone (AHL), octanoyl-homoserine lactone (C₈-HSL) as signaling molecule. Burkholderia ambifaria is one of the least virulent Bcc species, more often isolated from rhizospheres where it exerts a plant growth-promoting activity. However, clinical strains of B. ambifaria display distinct features, such as phase variation and higher virulence properties. Notably, we previously reported that under laboratory conditions, only clinical strains of the B. ambifaria species produced 4-hydroxy-3-methyl-2-alkylquinolines (HMAQs) via expression of the hmqABCDEFG operon. HMAQs are the methylated counterparts of the 4-hydroxy-2-alkylquinolines (HAQs) produced by the opportunistic human pathogen Pseudomonas aeruginosa, in which they globally contribute to the bacterial virulence and survival. We have found that unlike P. aeruginosa's HAQs, HMAQs do not induce their own production. However, they indirectly regulate the expression of the hmqABCDEFG operon. In B. ambifaria, a strong link between CepI/CepR-based QS and HMAQs is proposed, as we have previously reported an increased production of C₈-HSL in HMAQ-negative mutants. Here, we report the identification of all AHLs produced by the clinical B. ambifaria strain HSJ1, namely C₆-HSL, C₈-HSL, C₁₀-HSL, 3OHC₈-HSL, 3OHC₁₀-HSL, and 3OHC₁₂-HSL. Production of significant levels of hydroxylated AHLs prompted the identification of a second complete LuxI/LuxR-type QS system relying on 3OHC₁₀-HSL and 3OHC₁₂-HSL, that we have named CepI2/CepR2. The connection between these two QS systems and the hmqABCDEFG operon, responsible for HMAQs biosynthesis, was investigated. The CepI/CepR system strongly induced the operon, while the second system appears moderately involved. On the other hand, a HMAQ-negative mutant overproduces AHLs from both QS systems. Even if HMAQs are not classical QS signals, their effect on AHL-based QS system still gives them a part to play in the QS circuitry in B. ambifaria and thus, on regulation of various phenotypes.

Keywords: Burkholderia ambifaria; gene regulation; quorum sensing.