Histone post-translational modifications (PTMs) are epigenetic marks that operate within the central dogma of molecular biology: upon an environmental stimulus, the histone PTMs surrounding DNA can be changed in a way that modifies gene expression, and, therefore, the abundance and composition of RNA and proteins within cells (1). Once a change is induced, histone PTMs can offer organisms resilience to their environments through processes such as developmental plasticity (2, 3). The purpose of this study was to investigate whether histone PTMs mediate developmental plasticity in Mozambique tilapia facing salinity challenges. To this aim, we exposed fish to either freshwater or hypersalinity during their early critical window of development, then continued to raise the fish in either freshwater or seawater, respectively, for 18 months. Once the fish reached adulthood, we acclimated them to either freshwater or seawater. Following salinity treatments, we quantified 343 histone PTMs in the gills of each fish. We show here that histone PTMs differ dramatically between fish exposed to distinct environmental conditions for 18 months, and that the majority of histone PTM alterations persist for at least four weeks. However, histone PTMs respond minimally to salinity acclimation during adulthood. These results challenge our prior assumptions regarding the timescale of the histone PTM response, demonstrating that it does not necessarily precede the proteomic response or acclimation. Although this finding complicates our interpretation of developmental plasticity, it signifies that histone PTMs reflect prolonged exposure to environmental conditions.

In total, four distinct salinity treatments were administered to fish over the course of their lifetimes: 1) salinity stress during development and seawater during adulthood (HS*/S), 2) salinity stress during development and freshwater during adulthood (HS*/F), 3) freshwater during development and seawater during adulthood (FF*/S), and 4) freshwater during both development and adulthood (FF*/F). Following all salinity treatments, we quantified 343 biologically relevant histone PTMs, collectively referred to as the global histone PTM landscape, in the gills of each fish. By comparing the global histone PTM landscape between fish given different salinity treatments, we investigated not only developmental plasticity, but also whether histone PTMs are impacted by environmental conditions when exposures are lifelong, long-term throughout development, or four weeks during adulthood.

Following salinity treatments, we sampled the gills of 40 fish for histone PTM analysis.