Rhizobial homologs of the fatty acid transporter FadL facilitate perception of long-chain acyl-homoserine lactone signals

• Published in: Proceedings of the National Academy of Sciences - PNAS 2014-07, Vol.111 (29), p.10702-10707
• Main Authors: Krol, Elizaveta, Becker, Anke
• Format: Article
• Language: English
• Subjects: Acyl-Butyrolactones - metabolism; Agrobacterium tumefaciens; Amino Acid Sequence; Amino acids; Bacterial proteins; Bacterial Proteins - chemistry; Bacterial Proteins - metabolism; Binding sites; Biological Sciences; Biosynthesis; Escherichia coli; Fatty acids; Fatty Acids - metabolism; Fatty Acids, Monounsaturated - pharmacology; Gene Expression Regulation, Bacterial - drug effects; Genes; Gram-negative bacteria; Lactones; Molecular Sequence Data; Molecules; Nonesterified fatty acids; Oleic Acid - pharmacology; Phenotype; Phenotypes; Protein Structure, Tertiary; Quorum sensing; Quorum Sensing - drug effects; Quorum Sensing - genetics; Sequence Homology, Amino Acid; Signal Transduction - drug effects; Sinorhizobium meliloti; Sinorhizobium meliloti - drug effects; Sinorhizobium meliloti - genetics; Sinorhizobium meliloti - growth & development; Sinorhizobium meliloti - metabolism
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1404929111

Quorum sensing (QS) using N-acyl homoserine lactones (AHLs) as signal molecules is a common strategy used by diverse Gram-negative bacteria. A widespread mechanism of AHL sensing involves binding of these molecules by cytosolic LuxR-type transcriptional regulators, which requires uptake of external AHLs. The outer membrane is supposed to be an efficient barrier for diffusion of long-chain AHLs. Here we report evidence that in Sinorhizobium meliloti , sensing of AHLs with acyl chains composed of 14 or more carbons is facilitated by the outer membrane protein FadL Sₘ, a homolog of the Escherichia coli FadL Ec long-chain fatty acid transporter. The effect of fadL Sₘ on AHL sensing was more prominent for longer and more hydrophobic signal molecules. Using reporter gene fusions to QS target genes, we found that fadL Sₘ increased AHL sensitivity and accelerated the course of QS. In contrast to FadL Ec, FadL Sₘ did not support uptake of oleic acid, but did contribute to growth on palmitoleic acid. FadL Sₘ homologs from related symbiotic α-rhizobia and the plant pathogen Agrobacterium tumefaciens differed in their ability to facilitate long-chain AHL sensing or to support growth on oleic acid. FadL Aₜ was found to be ineffective toward long-chain AHLs. We obtained evidence that the predicted extracellular loop 5 of FadL Sₘ and further α-rhizobial FadL proteins contains determinants of specificity to long-chain AHLs. Replacement of a part of loop 5 by the corresponding region from α-rhizobial FadL proteins transferred sensitivity for long-chain AHLs to FadL Aₜ.