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We used a combination of approaches to measure primary production and plankton photophysiology in oligotrophic Flathead Lake, Montana (USA). Estimates of net ecosystem production (NEP) based on measurements of O2 to Ar ratios, together with radiocarbon (14C) assimilation incubations, revealed seasonal patterns in NEP and 14C-primary production. NEP was elevated during the summer, becoming negative during the winter. Rates of 14C-primary production were similarly seasonal, with peak rates in the summer and lower rates in the winter. Photosynthesis-irradiance curves indicated that plankton productivity in the subsurface chlorophyll maximum was light-limited year-round, while plankton production in the near-surface waters was light-saturated during the summer. We found that, despite physiological evidence of photoinhibition during the summer, this process appears to play a minor role in constraining primary production in Flathead Lake. Finally, use of metagenomic sequencing provided insight into photophysiological potential among the abundant cyanobacteria in the lake. Cyanobacteria belonging to Synechococcus/Cyanobium were well represented, some of which demonstrated seasonality while others appeared to be present year-round. Analyses of the metagenomic assembled genomes (MAGs) from these cyanobacteria revealed genes involved in phycoerythrin and phycoerythrobilin syntheses, with one MAG also possessing genes that encode phycourobilin. Such results point to flexibility in pigmentation as central to the physiology and competitive success of cyanobacteria in this lake.