Molecular complexity of the differential growth of freshwater diatoms along pH gradients

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Abstract Diatoms originated in marine waters, and many clades have invaded fresh waters, radiating throughout the continental aquatic environments. pH gradients have been a primary axis of species differentiation, from which environmental assessments have taken advantage using diatoms as bioindicators. However, a comprehensive view of the molecular variation underlying the diatom sensitivity to pH is missing. This study used twelve freshwater diatom strains across a broad phylogenetic range within raphid pennate clades and three distinct environmental pH conditions, pH 4.7, 7.0, and 8.2, for a common garden experiment. The transcriptomic analysis showed that environmental pH variation regulated many molecular processes and biological functions, especially those involved in biosynthesis and transport. Despite sharing many known functions, strains responded to pH changes in a highly idiosyncratic manner. Such specificity in the physiological response to pH aligns with the considerably divergent genetic backgrounds observed among the twelve diatom strains. This variation was likely shaped by different evolutionary trajectories in adaptive molecular landscapes, which were probably already differentiated in the initial marine environment and subjected to varying pH selection pressures in the complex chemical mosaic of inland waters. Overall, our results indicate that continental pH selection pressures do not determine a necessarily unique adaptive physiological response in diatoms, but instead allow for multiple adaptive solutions built on the evolutionary historical background and inland contingencies. Therefore, specific studies on the identified plastic responses to pH are needed to assess their adaptive function across clades.