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The broadly halotolerant green alga, Picochlorum strain SENEW3, has a highly reduced nuclear genome of 13.5 Mbp that encodes only 7367 genes. It was isolated from a shallow, mesophilic brackish-water lagoon that experiences extreme changes in temperature, light, and in particular, salinity (freshwater to 3-fold seawater). We challenged Picochlorum cells with high or low salinity shock and used transcriptomic and chlorophyll fluorescence analyses to elucidate tolerance to salinity fluctuation. The transcriptome analysis showed that one-half of the coding regions are differentially expressed in response to salinity changes. In addition, a significant number of co-expressed genes (usually from different metabolic pathways) are co-localized in the genome, forming 2–10 gene clusters. Whereas the overall salt stress response in Picochlorum SENEW3 is similar to that in other salt-tolerant algae, the “operon-like” structure in this species likely contributes to rapid recovery during salinity fluctuation. In summary, our work elucidates how evolutionary forces play out in a streamlined genome. Picochlorum SENEW3 relies on a broad array of adaptations from the reliance on horizontally transferred adaptive genes to the co-localization of stress response genes and a robust photosystem II to deal with a fluctuating environment. These attributes make Picochlorum SENEW3 of great biotechnological interest. [ABSTRACT FROM AUTHOR]