DBDPE induces more persistent disturbances than BDE-209 in Crassostrea gigas: Gut microbiome-modulated physiological...

Decabromodiphenyl ether (BDE-209) and its alternative, decabromodiphenyl ethane (DBDPE), are brominated flame retardants (BFRs) globally distributed in marine environments, posing risks to marine organisms. The gut microbiome not only degrades BFRs but also undergoes BFR-induced compositional and host-microbe co-metabolic changes. In this study, Pacific oysters (Crassostrea gigas) were exposed to 1 and 100 μg l^-1 of BDE-209/DBDPE for 28 days, followed by a 14-day depuration period. The higher bioaccumulation potential of DBDPE compared to BDE-209 might be attributed to its greater hydrophobicity, along with gut damage caused by pathogen proliferation. Alterations in the gut microbiome and metabolome induced by both BFR-exposure were associated with immunity and energy supply. Compared to BDE-209, DBDPE exposure induced more severe oxidative stress. Additionally, metabolomic analysis suggested that DBDPE has the potential to cause cell membrane damage. Notably, adverse effects, such as pathogen proliferation, persisted in DBDPE-exposed groups during depuration, which challenges its safer-alternative status. During depuration, functional remodeling in BFR-exposed oysters occurred through alterations in metabolism and genetic information processing in the gut microbiome, as well as alterations in purine metabolism, ABC transporters, and glycerophospholipid metabolism within the host (the latter being exclusive to the DBDPE-exposed groups). Despite its higher initial bioaccumulation, the higher elimination efficiency of DBDPE was facilitated by the activation of host repair program characterized by Verrucomicrobiota-mediated gut barrier restoration and glycerophospholipid metabolism-supported membrane remodeling. Correlation network analysis indicated that the adverse effects of high-concentration BFRs might be mediated by the gut microbiome, specifically through indole derivatives that may have upregulated the invertebrate form of AhR. Additionally, in the high-dose DBDPE-exposed group, a correlation between IAA and CAT suggested a potential link between microbial metabolism and the host's antioxidant system. This study provides comprehensive insights into gut microbiome and metabolome responses to BDE-209 and DBDPE, elucidating recovery mechanisms and the mediating role of gut microbiome in BFR-induced adverse effects in oysters.