New Vocabulary for Bacterial Communication

Abstract

Quorum sensing (QS) is widely accepted as a procedure that bacteria use to converse. However, prevailing thinking places acyl homoserine lactones (AHLs) at the forefront of this communication pathway in Gram-negative bacteria. With the advent of high-throughput genomics and the subsequent influx of bacterial genomes, bioinformatics analysis has determined that the genes encoding AHL biosynthesis, originally discovered to be indispensable for QS (LuxI-like proteins and homologues), are often absent in QS-capable bacteria. Instead, the sensing protein (LuxR-like proteins) is present with an apparent inability to produce any outgoing AHL signal. Recently, several signals for these LuxR solos have been identified. Herein, advances in the field of QS are discussed, with a particular focus on recent research in the field of bacterial cell-cell communication.

Keywords: bacterial communication; biosynthesis; gene sequencing; quorum quenching; quorum sensing.

Figure 1

A) Representation of classical QS signalling pathways with AHL; AI‐2; peptides from S. aureus and B. subtilis; and (R)‐methyl 3‐hydroxymyristic acid methyl ester (3‐OH MAME)/(R)‐methyl 3‐hydroxypalmitic acid methyl ester (3‐OH PAME) from Ralstonia solanacearum and Ralstonia pseudosolanacearum. B) The nonclassical communication pathways of Rhodopseudomonas palustris, Photorhabdus asymbiotica, Photorhabdus luminescens, Vibrio cholerae and P. aeruginosa, as well as plant–bacteria inter‐kingdom signalling in Pseudomonas GM79. The QS molecules are drawn at the site at which they are sensed by the cell (IN or OUT); transport over the cytoplasmic membrane (CM) is not depicted. Similar protein colour represents a similar protein family. LuxI homologues are depicted in yellow, LuxR homologues in green and LysR homologues in light blue. Typical domains of bacterial two‐component systems are purple. HK=histidine kinase; RR=response regulator. LuxS/LsrR‐derived AI‐2 sensing is simplified and depicted without periplasmic capturing, transport and phosphorylation (see text for details). Notably, LsrR senses the phosphorylated form of AI‐2, but LuxS produces non‐phosphorylated AI‐2. HEHEAA: N‐(2‐hydroxyethyl)‐2‐(2‐hydroxyethylamino). HEHEAA is formed by the condensation of ethanolamine (EA) and N‐(2‐hydroxyethyl)glycine (HeGly).

Figure 2

Biosynthetic pathways of PPY and DAR in Photorhabdus. Both pathways share one precursor (grey boxes). The different acyl moieties can be derived from fatty acid biosynthesis (FAB) or fatty acid degradation (FAD). PpyS and DarB represent the ketosynthases involved in biosynthesis and DarA is an aromatase that transforms CHD into DAR compounds.

Figure 3

A) LuxR solos identified in bacteria. Highlighted are clades containing PluR/PauR responsible for sensing PPY and DAR, respectively (orange); plant‐associated bacteria (green); those with an annotated unidentified fold in the sensor region (red); and protein homologues with a PAS4 domain (blue). B) KS phylogeny by using data from different subtypes of known ketosynthase collected through a BLASTp search against PpyS. Highlighted are clades containing DarB (green) and PpyS‐like (orange) proteins; the inset shows the phylogeny of PpyS‐like sequences and their strain of origin. Trees were formed by using a maximum‐likelihood algorithm with the PHYML plugin of Geneious (v8.0.4). Values on branches represent bootstrapping (n=100) percentages.

Figure 4

Neighbour‐joining consensus tree of DarB homologues. DarB (WP_012794414.1) from Chitinophaga pinensis DSM 2588 was used to identify homologue‐containing strains by using BLASTp. These strains were subsequently searched by using DarA (WP_012794415.1) and DarC (WP_012794409.1), also from C. pinensis DSM 2588, as query sequences. The phylogenetic tree was constructed in Geneious (v8.0.4) by using the PHYML plugin and bootstrapping to support branch formation (n=100). The resulting tree was exported in Newick format and annotated by using the interactive tree of life (v2.1).102, 103 The innermost circle contains species and strain information highlighting dominant bacterial genera, with outer circles (from inside to outside) representing the genetic organisation of DarABC in the genome (greyscale), the number of LuxI homologues (red) and the number of LuxR homologues (blue).