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In  Pseudomonas aeruginosa , the expression of a number of virulence factors, as well as biofilm formation, are controlled by quorum sensing (QS).  N -Acylhomoserine lactones (AHLs) are an important class of signaling molecules involved in bacterial QS and in many pathogenic bacteria infection and host colonization are AHL-dependent. The AHL signaling molecules are subject to inactivation mainly by hydrolases (Enzyme Commission class number EC 3) (i.e.  N -acyl-homoserine lactonases and  N -acyl-homoserine-lactone acylases). Only little is known on quorum quenching mechanisms of oxidoreductases (EC 1). Here we report on the identification and structural characterization of the first NADP-dependent short-chain dehydrogenase/reductase (SDR) involved in inactivation of  N -(3-oxo-dodecanoyl)-L-homoserine lactone (3-oxo-C 12 -HSL) and derived from a metagenome library. The corresponding gene was isolated from a soil metagenome and designated  bpiB09 . Heterologous expression and crystallographic studies established BpiB09 as an NADP-dependent reductase. Although AHLs are probably not the native substrate of this metagenome-derived enzyme, its expression in  P. aeruginosa  PAO1 resulted in significantly reduced pyocyanin production, decreased motility, poor biofilm formation and absent paralysis of  Caenorhabditis elegans . Furthermore, a genome-wide transcriptome study suggested that the level of  lasI  and  rhlI  transcription together with 36 well known QS regulated genes was significantly (≥10-fold) affected in  P. aeruginosa  strains expressing the  bpiB09  gene in pBBR1MCS-5. Thus AHL oxidoreductases could be considered as potent tools for the development of quorum quenching strategies.

A Novel Metagenomic Short-Chain Dehydrogenase/Reductase Attenuates Pseudomonas aeruginosa Biofilm Formation and Virulence on Caenorhabditis elegans