Algal p-coumaric acid induces oxidative stress and siderophore biosynthesis in the bacterial symbiont Phaeobacter inhibens

The Roseobacter Group sometimes referred to as the Marine Rhodobacteraceae, is a significant genus of heterotrophic bacteria in the marine environment. Being able to undergo anoxygenic photosynthesis, metabolize a wide range of organic molecules, break down dimethylsulfoniopropionate, and create a variety of secondary metabolites, they have a highly versatile metabolism. They are most frequently connected to micro- and macroalgae, with which they may interact in mutualistic and pathogenic ways. Symbiosis is a close, targeted, and the prolonged relationship between organisms of two or more different species. Natural products such as nutrition supplies, invasive toxins, developmental triggers, partner localization cues, or defensive agents can be crucial in these systems. Phaeobacter inhibens 2.10 can outcompete other bacteria and is a potent biofilm former and marine surface colonizer. The development of heritable morphotypes variations that are white in appearance and deficient in their capacity to prevent the growth of the bacterium P. tunicate is caused by the biofilm growth and distribution of P. inhibens 2.10. However, when the algae release p-coumaric acid (pCA) or other phenylpropanoids, such as sinapic acid or ferulic acid, the interaction between P. inhibens and the microalgae changes. P. inhibens produces the roseobacticides in these circumstances, which are effective algaecides that kill E. huxleyi. Sinapic acid also causes the release of a second algaecide called roseochelin B. Roseochelin B is produced by many Roseobacter strains and is produced at higher titers than roseobacticides, although being less effective.

In a new study published in Cell Chemical Biology journal, researchers from Princeton University: Rurun Wang, Etienne Gallant, Maxwell Wilson, Yihan Wu, Dr. Anran Li, Zemer Gitai and led by Professor Mohammad Seyedsayamdost studied the global transcriptomic response of P. inhibens 2.10 to pCA. The study reveals cell-wide effects, including energy depletion, sulfur assimilation, oxidative stress response, and secondary metabolism. The research team isolated and structurally clarify the product of this locus, an unreported catecholate siderophore, which authors dubbed roseobactin, as a result of the considerable induction of gene clusters coding for TDA and the elusive siderophore in response to pCA.

The authors showed that pCA has a mild antibiotic effect against P. inhibens, with a MIC of 2.5 mM. It causes worldwide transcriptome changes and ROS generation at sub-inhibitory dosages. The stimulation of secondary metabolism, possibly through the oxidative stress response, stands out among these. The pCA-challenged transcriptome of P. inhibens 2.10 demonstrates three characteristics of resistance against oxidative stress: production of metal chelators, expression of antioxidant enzymes, and accelerated repair or manufacture of crucial biopolymers. The findings demonstrate that algal pCA affects P. inhibens in a very comparable manner. Thus, whereas during the symbiosis’s mutualistic phase, the two symbionts exchange advantageous compounds, the parasitic phase is characterized by one partner inflicting oxidative harm on the other utilizing endogenous secondary metabolites. The rbt gene cluster in P. inhibens 2.10 produces roseobactin, a new siderophore, which researchers discovered and characterized thanks to the transcriptome findings. This molecule adds a new phrase to the algal-bacterial conversation and shows that during the parasitic stage of the association, P. inhibens 2.10 activates the biosynthesis of iron-scavenging compounds. According to the authors, pCA induces oxidative stress that causes the cell to build a secondary metabolite response and repair damaged biopolymers. Shutting down non-essential processes, such as the creation of macromolecular machinery involved in motility and flagellar movement, may be used to provide the energy required for these processes. This rewired energy may subsequently be utilized through oxidative stress to produce secondary metabolites like roseobactin and roseobacticides.

In summary, the new study by Professor Mohammad Seyedsayamdost and his colleagues illuminates the parasitic phase of this interaction, where one symbiont exerts oxidative stress on the other with a strain-specific arsenal of chemicals. The production of roseobactin and the algaecidal roseobacticides in P. inhibens is correlated with and possibly triggered by oxidative stress. The study also highlights the benefits of researching symbiotic relationships as potential sources of novel natural products. Furthermore, it unifies algal-bacterial interactions as streamlined models for more intricate bacterial-eukaryote connections in microbially active environments like soil or human microbiomes.