RNA-guided host defense mechanisms associated with Clustered Regularly Interspersed Short Palindromic Repeat (CRISPR) arrays exist in a majority of bacteria and archaea. Often described as prokaryotic adaptive immune systems, their target specificity derives from a series of unique “spacers” – many identical to DNA sequences from phage, transposon, and plasmid mobilomes – interspersed within CRISPR arrays. CRISPR systems have been grouped into three broad types; observations that Type III CRISPR systems are capable of targeting RNA in some prokaryotes raise the question of how spacers might be acquired from invasive RNA species - such as RNA phage - that do not have a DNA stage in their replication cycle. In several Type III CRISPR systems, the Cas1 gene is naturally fused to a reverse transcriptase (RT). Working with the marine bacterium Marinomonas mediterranea (MMB-1), we have shown that RT-Cas1 fusions enable the acquisition of both DNA and RNA spacers in vivo, with RNA acquisition (but not DNA acquisition) depending on RT activity. Biochemical experiments with purified RT-Cas1 and Cas2 from MMB-1 indicate that these proteins catalyze direct ligation of RNA segments into the CRISPR array, followed by reverse transcription. These observations outline a novel host-elucidated mechanism for reverse information flow from RNA to DNA.