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Environmental transitions, such as the salinity divide separating marine and fresh waters, shape biodiversity over both shallow and deep timescales, opening up new niches and creating opportunities for accelerated speciation and adaptive radiation. Understanding the genetics of environmental adaptation is central to understanding how organisms colonise and subsequently diversify in new habitats. We used time‐resolved transcriptomics to contrast the hyposalinity stress responses of two diatoms. Skeletonema marinoi has deep marine ancestry but has recently invaded brackish waters. Cyclotella cryptica has deep freshwater ancestry and can withstand a much broader salinity range. Skeletonema marinoi is less adept at mitigating even mild salinity stress compared to Cyclotella cryptica, which has distinct mechanisms for rapid mitigation of hyposaline stress and long‐term growth in low salinity. We show that the cellular mechanisms underlying low salinity tolerance, which has allowed diversification across freshwater habitats worldwide, includes elements that are both conserved and variable across the diatom lineage. The balance between ancestral and lineage‐specific environmental responses in phytoplankton have shaped marine–freshwater transitions on evolutionary timescales and, on contemporary timescales, will affect which lineages survive and adapt to changing ocean conditions. 

Abstract The salinity gradient separating marine and freshwater environments represents a major ecological divide for microbiota, yet the mechanisms by which marine microbes have adapted to and ultimately diversified in freshwater environments are poorly understood. Here, we take advantage of a natural evolutionary experiment: the colonization of the brackish Baltic Sea by the ancestrally marine diatom Skeletonema marinoi. To understand how diatoms respond to low salinity, we characterized transcriptomic responses of acclimated S. marinoi grown in a common garden. Our experiment included eight strains from source populations spanning the Baltic Sea salinity cline. Gene expression analysis revealed that low salinities induced changes in the cellular metabolism of S. marinoi, including upregulation of photosynthesis and storage compound biosynthesis, increased nutrient demand, and a complex response to oxidative stress. However, the strain effect overshadowed the salinity effect, as strains differed significantly in their response, both regarding the strength and the strategy (direction of gene expression) of their response. The high degree of intraspecific variation in gene expression observed here highlights an important but often overlooked source of biological variation associated with how diatoms respond to environmental change. 

How diatoms respond to fluctuations in osmotic pressure is important from both ecological and applied perspectives. It is well known that osmotic stress affects photosynthesis and can result in the accumulation of compounds desirable in pharmaceutical and alternative fuel industries. Gene expression responses to osmotic stress have been studied in short‐term trials, but it is unclear whether the same mechanisms are recruited during long‐term acclimation. We used RNA‐seq to study the genome‐wide transcription patterns in the euryhaline diatom,Cyclotella cryptica, following long‐term acclimation to salinity that spanned the natural range of fresh to oceanic water. Long‐term acclimatedC. crypticaexhibited induced synthesis or repressed degradation of the osmolytes glycine betaine, taurine and dimethylsulfoniopropionate (DMSP). Although changes in proline concentration is one of the main responses in short‐term osmotic stress, we did not detect a transcriptional change in proline biosynthetic pathways in our long‐term experiment. Expression of membrane transporters showed a general tendency for increased import of potassium and export of sodium, consistent with the electrochemical gradients and dependence on co‐transported molecules. Our results show substantial between‐genotype differences in growth and gene expression reaction norms and suggest that the regulation of proline synthesis important in short‐term osmotic stress might not be maintained in long‐term acclimation. Further examination using time‐course gene expression experiments, metabolomics and genetic validation of gene functions would reinforce patterns inferred from RNA‐seq data.