Diffusible Signaling Factor, a Quorum-Sensing Molecule, Interferes with and Is Toxic Towards Bdellovibrio bacteriovorus 109J

Abstract

Bdellovibrio bacteriovorus 109J is a predatory bacterium which lives by predating on other Gram-negative bacteria to obtain the nutrients it needs for replication and survival. Here, we evaluated the effects two classes of bacterial signaling molecules (acyl homoserine lactones (AHLs) and diffusible signaling factor (DSF)) have on B. bacteriovorus 109J behavior and viability. While AHLs had a non-significant impact on predation rates, DSF considerably delayed predation and bdelloplast lysis. Subsequent experiments showed that 50 μM DSF also reduced the motility of attack-phase B. bacteriovorus 109J cells by 50% (38.2 ± 14.9 vs. 17 ± 8.9 μm/s). Transcriptomic analyses found that DSF caused genome-wide changes in B. bacteriovorus 109J gene expression patterns during both the attack and intraperiplasmic phases, including the significant downregulation of the flagellum assembly genes and numerous serine protease genes. While the former accounts for the reduced speeds observed, the latter was confirmed experimentally with 50 μM DSF completely blocking protease secretion from attack-phase cells. Additional experiments found that 30% of the total cellular ATP was released into the supernatant when B. bacteriovorus 109J was exposed to 200 μM DSF, implying that this QS molecule negatively impacts membrane integrity.

Phylogenomic insights into distribution and adaptation of Bdellovibrionota in marine waters

“…Because of the special lifestyle of Bdellovibrionota, there may be other protein factors serving as the quorum sensing regulators during the predatory growth phase. The latest study indicated that diffusible signaling factor (DSF) considerably delayed predation and bdelloplast lysis (40). Sec-type II system is almost complete in all Bdellovibrionota groups (Fig.…”

Identification of FadT as a Novel Quorum Quenching Enzyme for the Degradation of Diffusible Signal Factor in Cupriavidus pinatubonensis Strain HN-2

“…DSF has multiple effects on various cellular processes of bacteria. It has been reported that DSF can block protease secretion from attack-phase cells of Bdellovibrio bacteriovorus 109 J completely at the concentration of 50 mM and negatively regulate the membrane integrity at a concentration of 200 mM [75]. Additionally, DSF inhibits biofilm formation with no impacts on the growth of P. aeruginosa under static and continuous conditions [76].…”

DSF-family quorum sensing signal-mediated intraspecies, interspecies, and inter-kingdom communication

“…At 50 μM, XcDSF reduced strain 109J attack-phase motility by 50%. A higher dose of 200 μM leads to a significant loss in membrane integrity and the viability of strain 109J [58]. Transcriptome analysis revealed that XcDSF induced stress responses, including osmotic shock, reactive oxygen species (ROS), MarR regulon activation, and the downregulation of the flagellum assembly genes and serine protease genes in 109J [58].…”

“…A higher dose of 200 μM leads to a significant loss in membrane integrity and the viability of strain 109J [58]. Transcriptome analysis revealed that XcDSF induced stress responses, including osmotic shock, reactive oxygen species (ROS), MarR regulon activation, and the downregulation of the flagellum assembly genes and serine protease genes in 109J [58]. Furthermore, XcDSF at a concentration of 200 μM was shown to have similar inhibitory activity towards B. bacteriovorus as sodium dodecyl sulfate, a highly toxic chemical surfactant, whereas it only altered gene expression of this predator at a lower and nontoxic concentration of 50 μM [58].…”