The brominated flame retardant hexabromocyclododecane (HBCD) is a globally prevalent and persistent organic pollutant listed by the Stockholm Convention in 2013. It can be found in many environments, such as water bodies and soil, and its highly bioaccumulative nature poses an urgent health threat for plants, animals, and humans. This study aimed to identify HBCD biotransformation by novel or understudied environmental bacteria and elucidate the biotransformation's molecular mechanisms. We discovered a purple non-sulfur bacterium, Rhodopseudomonas palustris strain YSC3, that exhibits HBCD removal and biotransformation activity. R. palustris YSC3 is capable of degrading 90 percent of 1 ppm HBCD within ten days. Furthermore, approximately 3.5 relative-molar ratios of bromide ions were observed during the reaction, suggesting biotransformation by debromination mechanisms. We further validated this mechanism in the detection of pentabromocyclododecanol and pentabromocyclododecene metabolites and demonstrated their reduced genotoxicity.
To identify metabolic pathways in R. palustris YSC3 that are induced by HBCD, we performed transcriptomic analyses at different temperatures and time points of bacterial HBCD exposure. These transcriptome profiles revealed the HBCD-triggered expression of 126 transcripts in cells incubated at 25 °C and 35 °C. Among these genes, we found increased expression of the transcriptional regulator LysR, two-component system regulators, HBCD degradation enzymes, including haloacid dehalogenases, glutathione-S-transferase, cytochrome p450, hydrolases, and dioxygenases, which we all confirmed by qRT-PCR analysis. Based on the analysis of gene expression, we propose an HBCD-degradation pathway in R. palustris. Briefly, HBCD signal transferred from cell membrane to transcriptional regulator LysR, then further to downstream degradation working enzymes. This study presented a new perspective on the biotransformation of persistent organic pollutants (POPs), such as HBCD, with a bio-omics approach and highlighted the value of systematic transcriptomic approaches to uncover and elucidate the intrinsic metabolisms for HBCD degradation in R. palustris.

Chung-Yen Lin

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