Ecological Role of 6OH-BDE47: Is It a Chemical Offense Molecule Mediated by Enoyl-ACP Reductases?

Although hydroxylated polybrominated diphenyl ethers (OH-BDEs) are among the most abundant natural organobromine compounds, the fundamental biological rationale for marine organisms to produce OH-BDEs remains elusive. Herein, we demonstrated that natural OH-BDEs exerted strong antibacterial activities against Escherichia coli by inhibiting enoyl-[acyl-carrier-protein] reductase (FabI), while anthropogenic OH-BDEs were inactive. Distinct from E. coli , OH-BDE-producing marine γ-proteobacteria including Marinomonas mediterranea MMB-1 (MMB-1) and Pseudoalteromonas luteoviolacea 2ta16 ( Pl 2ta16) exhibited resistance to 6OH-BDE47. An alternative enoyl-[acyl-carrier-protein] (ACP) reductase, FabV, was detected in all three OH-BDE-producing marine γ-proteobacteria. Thermal stability and protein affinity purification studies revealed that 6OH-BDE47 did not bind to recombinant or endogenous FabV of MMB-1 or Pl 2ta16, demonstrating that FabV was the primary mechanism for OH-BDE-producing marine γ-proteobacteria to be resistant to 6OH-BDE47. To further confirm if the laboratory results were evidenced in the field, the 16S rRNA sequencing and metagenomics data from seven field-collected marine sponges were analyzed. Notably, the two Clade 4 sponges containing high concentrations of 6OH-BDE47 exhibited a distinct microbiome community structure compared to the other analyzed clades. Correspondingly, FabV was found to be selectively enriched in the same Clade 4 sponges. The merged evidence from the laboratory experiments and field studies demonstrated that 6OH-BDE47 may act as a chemical offense molecule in marine sponges.