Abstract
Bacterial Quorum Sensing (QS), the indirect regulation of gene expression through production and detection of small diffusible molecules, has emerged as a point of interaction between eukaryotic host organisms and their associated microbial communities. The extracellular nature of QS molecules enables interference in QS systems, in many cases via mimicry. This study targeted QS induction and inhibition in soft coral holobionts, as many soft coral species commonly contain compounds with structural similarities to the well-studied bacterial QS molecules acyl homoserine lactones. Screening with two bacterial biosensors, Agrobacterium tumefaciens A136 and Chromobacterium violaceum CV026, demonstrated that QS interference differed between the two biosensor strains and extended across the soft coral families Alcyoniidae, Clavulariidae, Nephtheidae, and Xeniidae. Bioassay-guided fractionation revealed chemical activity patterns, particularly in the induction of QS. Cembranoid diterpenes from active fractions were purified and tested for QS interference activity. Interestingly, the type of QS activity (induction or inhibition) in A. tumefaciens A136 correlated with structural variability of the secondary oxygen ring; cembranoid diterpeneswith a furan ring or five-membered lactone induced QS, while compounds with larger (six or seven membered) lactone rings inhibited QS. Addition of the dominant cembranoid diterpene in the soft coral Lobophytum compactum, isolobophytolide, to bacterial culture media increased the number and morphological diversity of bacteria recovered from the mucosal layer of this soft coral, demonstrating a selective effect on certain members of the soft coral bacterial community. The identity and QS activity of recovered isolates differed between the mucosal layers of L. compactum and Sinularia flexibilis. In conclusion, this study provides information on the complexity of the interaction between soft corals and their associated bacteria, as well as, a structural understanding of how QS mimic compounds are able to interfere with a bacterial communication system.
Highlights
Quorum Sensing (QS) is one form of cell to cell signaling employed by bacteria to coordinate gene expression across entire populations through release and detection of extracellular signal molecules (Miller and Bassler, 2001)
Crude soft coral extracts demonstrated the ability to both induce and inhibit QS in the biosensors tested. While both induction and inhibition of QS were observed for the biosensor A. tumefaciens A136, none of the extracts, regardless of source coral species, polarity, or concentration, were able to induce QS in C. violaceum CV026 (Figure 2A)
The number of active soft coral extracts was reduced at lower extract concentration, with none of the aqueous extracts retaining their activity at the lower dosage (Figure 2B)
Summary
Quorum Sensing (QS) is one form of cell to cell signaling employed by bacteria to coordinate gene expression across entire populations through release and detection of extracellular signal molecules (Miller and Bassler, 2001). Studies into the structure and functions of AHLs suggest that the G-lactone ring is required for QS activity and that the length and functionality of the acyl side chain provides specificity (Parsek and Greenberg, 2000; Watson et al, 2002; Geske et al, 2008). For this reason, it has been hypothesized that AI-1 QS mimics would contain a G lactone ring or homologous functionality such as the furanones of the red alga Delisea pulchra. The furanones are one of the few QS inhibitors to have been structurally elucidated and the presence of an oxygenated ring was demonstrated to be essential to their activity (Manefield et al, 1999)
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