Biogenic ROS mediated degradation mechanism of marine toxin domoic acid.

Domoic acid (DA) is a compound generated as a secondary metabolite during harmful algal blooms, has historically received attention as the potent neurotoxicity in marine environment. However, the aerobic degradation mechanism of DA and the DA-degrader remain largely unknown. Here, we revealed the mechanism of aerobic degradation of DA by a ubiquitous marine Pseudoalteromonas sp., and more importantly, we confirmed that the degradation of DA is mediated by biogenic reactive oxygen species (ROS), rather than direct enzyme-mediated as traditionally conceived. Results indicated that DA degradation was caused by biogenic O2- and OH, where DA underwent reactions of decarboxylation, hydroxylation, and oxidation to yield the detoxification terminal product. Besides, whole genome sequencing and RT-qPCR analysis revealed that the genes conferring to encoding leucine dehydrogenase (ldh) and Na+-translocated NADH-quinone oxidoreductase (nqrA, nqrF) are responsible for biogenic ROS production. Finally, we found through comparative proteomic analysis that biogenic ROS mediated the DA degradation may be prevalent in the environment. Overall, this work not only reveals aerobic biotransformation mechanism of DA, but also identifies a novel mechanism of DA degradation, which provides new perspective into the environmental fate of DA and the artificial bioremediation of DA.

Applying metabolic modeling and multi-omics to elucidate the biotransformation mechanisms of marine algal toxin domoic acid (DA) in sediments.

Domoic acid (DA)-producing algal blooms are a global marine environmental issue. However, there has been no previous research addressing the question regarding the fate of DA in marine benthic environments. In this work, we investigated the DA fate in the water-sediment microcosm via the integrative analysis of a top-down metabolic model, metagenome, and metabolome. Results demonstrated that biodegradation is the leading mechanism for the nonconservative attenuation of DA. Specifically, DA degradation was prominently completed by the sediment aerobic community, with a degradation rate of 0.0681 ± 0.00954 d-1. The DA degradation pathway included hydration, dehydrogenation, hydrolysis, decarboxylation, automatic ring opening of hydration, and ß oxidation reactions. Moreover, the reverse ecological analysis demonstrated that the microbial community transitioned from nutrient competition to metabolic cross-feeding during DA degradation, further enhancing the cooperation between DA degraders and other taxa. Finally, we reconstructed the metabolic process of microbial communities during DA degradation and confirmed that the metabolism of amino acid and organic acid drove the degradation of DA. Overall, our work not only elucidated the fate of DA in marine environments but also provided crucial insights for applying metabolic models and multi-omics to investigate the biotransformation of other contaminants.