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Variation in genome content is a potent mechanism of microbial adaptation. The genomes of members of the cyanobacterial genus Acaryochloris vary greatly in gene content as a consequence of the idiosyncratic retention of both recent gene duplicates and plasmid-encoded genes acquired by horizontal transfer. For example, the genome of Acaryochloris strain MBIC11017, which was isolated from an iron-limited environment, is enriched in duplicated and novel genes involved in iron assimilation. Here, we took an integrative approach to characterize the adaptation of Acaryochloris MBIC11017 to low environmental iron availability and the relative contributions of the expression of duplicated versus novel genes. We observed that Acaryochloris MBIC11017 grew faster and to a higher yield in the presence of nanomolar concentrations of iron than did a closely related strain. These differences were associated with both a higher rate of iron assimilation and a greater abundance of iron assimilation transcripts. However, recently duplicated genes contributed little to increased transcript dosage; rather, the maintenance of these duplicates in the MBIC11017 genome is likely due to the sharing of ancestral dosage by expression reduction. Instead, novel, horizontally transferred genes are responsible for the differences in transcript abundance. The study provides insights on the mechanisms of adaptive genome evolution and gene expression in Acaryochloris.