Plastisphere Microbiomes Respiring Persistent Organohalide Pollutants

Plastics are invading nearly all ecosystems on earth, acting as emerging repositories for toxic organic pollutants and thereby imposing substantial threats to ecological integrity. The colonization of plastics by microorganisms, forming the plastisphere, has garnered attention due to its potential influence on biogeochemical cycles. However, the capability of plastisphere microorganisms to attenuate organohalide pollutants remains to be evaluated. This study revealed that the plastisphere, collected from coastal ecosystems, harbors unique microbiomes, while the natural accumulation of organohalide pollutants on plastics may favor the proliferation of organohalide-respiring bacteria (OHRB). Laboratory tests further elucidated the high potential of plastisphere microbiota to reductively dehalogenate a variety of organohalide pollutants. Notably, over 70% tested plastisphere completely debrominated tetrabromobisphenol A (TBBPA) and polybrominated diphenyl ethers (PBDEs) to nonhalogenated products, whereas polychlorinated biphenyls (PCBs) were converted to lower congeners under anaerobic conditions. <i>Dehalococcoides</i>, <i>Dehalogenimonas</i>, and novel <i>Dehalococcoidia</i> populations might contribute to the observed dehalogenation based on their growth during incubation and positive correlations with the quantity of halogens removed. Intriguingly, large fractions of these OHRB populations were identified in a lack of the currently known TBBPA/PBDEs/PCBs reductive dehalogenase (RDase) genes, suggesting the presence of novel RDase genes. Microbial community analyses identified organohalides as a crucial factor in determining the composition, diversity, interaction, and assembly of microbes derived from the plastisphere. Collectively, this study underscores the overlooked roles of the plastisphere in the natural attenuation of persistent organohalide pollutants and sheds light on the unignorable impacts of organohalide compounds on the microbial ecology of the plastisphere.