Substrate-driven microbial specialization and cooperative dechlorination of chlorinated pollutants in estuarine ecosystems

ABSTRACT Organohalide-respiring bacteria (OHRB) are globally distributed, yet their ecological roles in marine environments remain poorly understood, with few isolates characterized from these systems. Here, we describe a stable anaerobic consortium from estuarine sediments that performs sustained dechlorination of 1,1,2-trichloroethane (1,1,2-TCA) to vinyl chloride (VC) at a rate of 126.3 ± 0.9 µM d −1 . This activity was associated with the stable co-enrichment of two key populations, Dehalogenimonas and Desulfitobacterium , which increased to dominate the community at 49.7% and 32.5%, respectively. Metagenome-assembled genomes confirmed both populations represent novel species with distinct genomic adaptations. Dehalogenimonas sp. strain H harbors 24 putative reductive dehalogenase genes and complete ectoine biosynthesis pathways ( ectABC ) essential for osmotolerance, while Desulfitobacterium sp. strain Y represents the first cultivated marine-associated member of this genus. Proteomic analysis confirmed active expression of multiple reductive dehalogenases from strain H, strongly supporting its role as the primary dechlorinator. Concurrently, physiological and genomic data suggest that strain Y is strongly co-selected under 1,1,2-TCA-amended conditions and likely occupies a crucial supportive niche. Alongside its extensive metabolic versatility that likely buffers the consortium against environmental fluctuations, its complete de novo corrinoid biosynthesis pathway implies a complementary role as a vitamin B 12 provider for the extreme corrinoid-auxotrophic strain H. This study provides evidence for a stable co-enrichment consistent with nutritional niche differentiation within native microbial communities and suggests a potential cooperative interaction between novel Dehalogenimonas and Desulfitobacterium species, advancing our understanding of halogen cycling in coastal ecosystems. IMPORTANCE Estuaries serve as critical interfaces between terrestrial and marine ecosystems, yet the microbial processes governing chlorinated pollutant fate in these vulnerable zones remain largely unexplored. Our discovery of a novel partnership between Dehalogenimonas and Desulfitobacterium species challenges the conventional understanding that Desulfitobacterium is restricted to terrestrial habitats. Integrative multi-omic and physiological analyses reveal that Dehalogenimonas strain H serves as the highly specialized primary dechlorinator, while Desulfitobacterium strain Y is stably co-enriched and exhibits genomic potential to sustain the consortium by providing essential corrinoid cofactors. The identification of genomic determinants underlying salt tolerance in Dehalogenimonas , including ectoine and mannosylglycerate biosynthesis pathways, provides mechanistic insights into OHRB adaptation to fluctuating salinity. These findings have direct implications for developing bioremediation strategies for contaminated coastal sites and highlight the importance of characterizing microbial diversity in transitional ecosystems.