Organohalide respiration by a Desulforhopalus-dominated community

Marine sediments harbor diverse organohalide-respiring bacteria (OHRB), but their functional roles and metabolic interactions remains poorly understood. To investigate these interactions, we obtained and characterized a debrominating consortium from Aarhus Bay marine sediments. The consortium transformed 2,6-dibromophenol (2,6-DBP) to phenol under sulfate-reducing conditions, with bacterial growth demonstrating respiratory energy conservation. Metagenomic analysis and binning revealed five new species-level populations (>85% complete, <3% contaminated) dominated by Desulforhopalus (bin.5). Critically, bin.5 encodes a thiolytic tetrachloro-p-hydroquinone reductive dehalogenase (RDase), previously characterized only in aerobic bacteria, representing evidence of this enzyme functioning in a strictly anaerobic sulfate-reducing bacterium. Two additional populations (Desulfoplanes bin.3 and Marinifilaceae bin.4) encoded two and one putative respiratory corrinoid-dependent RDase, respectively. Transcription of all four RDase genes was rapidly induced upon 2,6-DBP addition, indicating multi-population response. Acetylene inhibited debromination post-transcriptionally without affecting RDase gene transcription, or sulfate metabolism, confirming RDase-mediated catalysis. Genome analysis indicated bin.5 encodes a near-complete vitamin B12 biosynthesis pathway (lacking only cbiJ, which can be bypassed through alternative reductases), consistent with debromination activity independent of exogenous B12 addition. Comparative genomics identified Marinifilum and Ancylomarina as candidate OHRB taxa, substantially expanding known phylogenetic diversity of marine organohalide respirers. This work reveals previously unrecognized biochemical versatility in anaerobic dehalogenation and demonstrates metabolic self-sufficiency enabling organohalide respiration in oligotrophic marine sediments.