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Abstract Marine Group II Euryarchaeota ( Candidatus Poseidoniales), abundant but yet-uncultivated members of marine microbial communities, are thought to be (photo)heterotrophs that metabolize dissolved organic matter (DOM), such as lipids and peptides. However, little is known about their transcriptional activity. We mapped reads from a metatranscriptomic time series collected at Sapelo Island (GA, USA) to metagenome-assembled genomes to determine the diversity of transcriptionally active Ca . Poseidoniales. Summer metatranscriptomes had the highest abundance of Ca . Poseidoniales transcripts, mostly from the O1 and O3 genera within Ca . Thalassarchaeaceae (MGIIb). In contrast, transcripts from fall and winter samples were predominantly from Ca . Poseidoniaceae (MGIIa). Genes encoding proteorhodopsin, membrane-bound pyrophosphatase, peptidase/proteases, and part of the ß-oxidation pathway were highly transcribed across abundant genera. Highly transcribed genes specific to Ca . Thalassarchaeaceae included xanthine/uracil permease and receptors for amino acid transporters. Enrichment of Ca . Thalassarchaeaceae transcript reads related to protein/peptide, nucleic acid, and amino acid transport and metabolism, as well as transcript depletion during dark incubations, provided further evidence of heterotrophic metabolism. Quantitative PCR analysis of South Atlantic Bight samples indicated consistently abundant Ca . Poseidoniales in nearshore and inshore waters. Together, our data suggest that Ca . Thalassarchaeaceae are important photoheterotrophs potentially linking DOM and nitrogen cycling in coastal waters.