Environmental contamination by Cr(VI) leaching from chromite ore processing residue (COPR) legacy disposal sites can pose a threat to human health. Under iron-reducing conditions, microbial activity can convert mobile and toxic Cr(VI) to less mobile and less toxic Cr(III); however, COPR waste is a very hostile environment for microbial life. Microcosms using soil from beneath a COPR disposal site were challenged with Cr(VI) with and without acetate to stimulate microbial metabolism. Geochemistry showed that when the microbial populations were reducing iron, Cr(VI) was also reduced, and 16S rRNA gene sequencing showed that the community composition evolved over the course of the experiment. Meta-transcriptome data revealed ~3% of transcripts were differentially regulated (p = 0.01) between the acetate amended and unamended systems, with twice as many transcripts downregulated by acetate. Gene ontology (GO) terms for processes involving the cell wall, cell periphery, plasma membrane and encapsulating structures as well as catabolic processes, especially carbohydrate metabolism, were significantly enriched in the unamended microcosm meta-transcriptome. Transcripts for alternative sigma (σ) factors and anti-σ factors were prominent among the differentially regulated genes. The study provides insight into how the provision of acetate shapes metabolic processes and life history strategies in an alkaline Cr(VI) impacted environment.