Quorum Sensing Interference and Structural Variation of Quorum Sensing Mimics in Australian Soft Coral

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 diterpenes with 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.

AHL-Lactonase Producing Psychrobacter sp. From Palk Bay Sediment Mitigates Quorum Sensing-Mediated Virulence Production in Gram Negative Bacterial Pathogens

“…Secondary metabolites from marine organisms are considered an important source of biomolecules for drug discovery (Newman and Cragg, 2004;Borges and Simões, 2019). Bacteria associated with corals, sponges, and other organisms have been recognized as the factual producers of many bioactive compounds (Kelman et al, 2006;Freckelton et al, 2018). Though AHL degradation enzymes from bacterial isolates have been identified from different sources (Dong et al, 2002;Uroz et al, 2003;Ulrich, 2004;Hassan et al, 2016), the investigation of antibiofilm activity of bacteria, particularly from marine resources, are expected to act against antibiotic resistant bacterial pathogens (Huang et al, 2019;Zhou et al, 2019).…”

Quorum sensing disruption regulates hydrolytic enzyme and biofilm production in estuarine bacteria

“…This is in contrast with previous studies that reported no clear pattern of QS activity in Vibrionaceae strains, including Vibrio sp. (Tait et al ., 2010; Freckelton et al ., 2018). The AHL production among Pseudomonas and Acinetobacter was much more diverse, with no clear production pattern.…”

“…The observation of bacteria that simultaneously emit pro‐ and anti‐QS compounds has been evidenced in a few strains, for example, in Agrobacterium tumefaciens (Zhang et al ., 2004), a marine Shewanella sp. (Tait et al ., 2009), in two isolates related to Endozoicomonas (Freckelton et al ., 2018) or Acinetobacter and Burkholderia strains isolated from the rhizosphere (Chan et al ., 2011). Such co‐occurrence of QS and QQ features in our collection of estuarine strains raises the question of the co‐expression of these two phenotypes, especially within the natural environment.…”

Quorum Sensing Regulates Bacterial Processes That Play a Major Role in Marine Biogeochemical Cycles

“…The Gammaproteobacteria class probably contains bacteria with the best-characterized AHL-based QS systems, such as members of the Vibrio, Pseudomonas, and Acinetobacter genera. They are also among the most common AHL producers isolated from various marine habitats (Cuadrado-Silva et al, 2013;Jatt et al, 2015;Freckelton et al, 2018;Charlesworth et al, 2019;Reen et al, 2019;Su et al, 2019;Urvoy et al, 2021a; Supplementary Table 2). In addition, they constitute the main class contributing to AHL production and sensing genes in marine metagenomics surveys, especially members of Vibrionales, Pseudomonadales, or Alteromonadales (Doberva et al, 2015;Huang et al, 2018;Su et al, 2021; Supplementary Table 1).…”

“…Marine Gammaproteobacteria are also actively engaged in AHL-QQ mechanisms involving both QQ enzymes and QSIs. Several studies have reported that isolated marine Gammaproteobacteria strains possess QQ capacities, in which they were often the most represented taxon (Torres et al, 2016;Freckelton et al, 2018;Su et al, 2019;Urvoy et al, 2021a; Supplementary Table 2). In their review, Zhao et al (2019) reported that 27% of marine bacterial isolates with QQ capacities were Gammaproteobacteria.…”