Microbial community function in freshwater sediments is influenced by the presence and persistence of anthropogenic pollutants, yet simultaneously imposes significant control on their transformation. Thus, microbes provide valuable ecosystem services in terms of biodegradation and bioindicators of compromised habitats. From a remediation perspective it is valuable to leverage the suite of microbial genes at the transcriptional level that are active in either natural versus stressed environments to provide insight into the cycling and fate of contaminants. Metatranscriptomic analysis of total bacterial and archaeal messenger RNA (mRNA) is a useful tool in this facet and was applied to sediments sampled from the Detroit River; a binational Area of Concern (AOC) in the Great Lakes. Previously established sediment surveys and modelling delineated the river into contaminant gradients based on concentrations of polycyclic aromatic hydrocarbons (PAHs), polychlorinated biphenyls (PCBs), and metals. Differential expression analysis through DESeq2 revealed that microbial transcripts associated with nitrate reduction, methanogenesis, and beta-oxidation were significant in legacy polluted sediments and linked with energetic pathways key in the generation of cellular currencies (acetyl-CoA, succinyl-CoA). Gluconeogenesis and polyester synthesis also showed high abundance in contaminated regions, along with increased expression of stress response genes and transposons, despite decreases in community α-diversity. Aromatic cleavage genes were detected, but in low abundance across the contaminant gradient. These results suggest that microbial communities within the Detroit River exploit unique anabolic and catabolic pathways to derive and store energy from legacy organic contaminants while simultaneously recruiting stress-response and gene transfer mechanisms to cope with xenobiotic pressures. By coupling well-resolved chemical datasets with metatranscriptomics, this study adds to the spatial understanding of in-situ microbial activities in pristine and perturbed freshwater sediments.