Salinity-responsive histone PTMs identified in the gills and gonads of Mozambique tilapia (Oreochromis mossambicus).

BACKGROUND: Histone post-translational modifications (PTMs) are epigenetic marks that can be induced by environmental stress and elicit heritable patterns of gene expression. To investigate this process in an ecological context, we characterized the influence of salinity stress on histone PTMs within the gills, kidney, and testes of Mozambique tilapia (Oreochromis mossambicus). A total of 221 histone PTMs were quantified in each tissue sample and compared between freshwater-adapted fish exposed to salinity treatments that varied in intensity and duration. RESULTS: Four salinity-responsive histone PTMs were identified in this study. When freshwater-adapted fish were exposed to seawater for two hours, the relative abundance of H1K16ub significantly increased in the gills. Long-term salinity stress elicited changes in both the gills and testes. When freshwater-adapted fish were exposed to a pulse of severe salinity stress, where salinity gradually increased from freshwater to a maximum of 82.5 g/kg, the relative abundance of H1S1ac significantly decreased in the gills. Under the same conditions, the relative abundance of both H3K14ac and H3K18ub decreased significantly in the testes of Mozambique tilapia. CONCLUSIONS: This study demonstrates that salinity stress can alter histone PTMs in the gills and gonads of Mozambique tilapia, which, respectively, signify a potential for histone PTMs to be involved in salinity acclimation and adaptation in euryhaline fishes. These results thereby add to a growing body of evidence that epigenetic mechanisms may be involved in such processes.

A Strategy to Characterize the Global Landscape of Histone Post-Translational Modifications Within Tissues of Nonmodel Organisms.

Histone post-translational modifications (PTMs) are epigenetic marks that play a critical role in the expression and maintenance of DNA, but they remain largely uninvestigated in nonmodel organisms due to technical challenges. To begin alleviating this issue, we developed a workflow for histone PTM analysis in Mozambique tilapia (Oreochromis mossambicus), being a widespread and environmentally hardy fish, using mass spectrometry methods. By incorporating multiple protein digestion methods into the preparation of each sample, we reliably quantified 214 biologically relevant histone PTMs. All of these histone PTMs, collectively referred to as the global histone PTM landscape, were characterized in the gills, kidney, and testes of this fish. By comparing the global histone PTM landscape between the three tissues, we found that 91.59% of histone PTMs were tissue-dependent. The workflow and tools for histone PTM analysis described in this study are now publicly available and enable comprehensive investigation into the influence of environmental stress on histone PTMs in nonmodel organisms. Given the functionality and flexibility of histone PTMs, we anticipate that the study of histone PTMs in ecologically relevant contexts will provide ground-breaking insights into comparative physiology and evolution.

Physiological mechanisms of stress-induced evolution.

Organisms mount the cellular stress response whenever environmental parameters exceed the range that is conducive to maintaining homeostasis. This response is critical for survival in emergency situations because it protects macromolecular integrity and, therefore, cell/organismal function. From an evolutionary perspective, the cellular stress response counteracts severe stress by accelerating adaptation via a process called stress-induced evolution. In this Review, we summarize five key physiological mechanisms of stress-induced evolution. Namely, these are stress-induced changes in: (1) mutation rates, (2) histone post-translational modifications, (3) DNA methylation, (4) chromoanagenesis and (5) transposable element activity. Through each of these mechanisms, organisms rapidly generate heritable phenotypes that may be adaptive, maladaptive or neutral in specific contexts. Regardless of their consequences to individual fitness, these mechanisms produce phenotypic variation at the population level. Because variation fuels natural selection, the physiological mechanisms of stress-induced evolution increase the likelihood that populations can avoid extirpation and instead adapt under the stress of new environmental conditions.

Environmental conditions elicit a slow but enduring response of histone post-translational modifications in Mozambique tilapia.

This study sheds new light on the timescale through which histone post-translational modifications (PTMs) respond to environmental stimuli, demonstrating that the histone PTM response does not necessarily precede the proteomic response or acclimation. After a variety of salinity treatments were administered to Mozambique tilapia (Oreochromis mossambicus) throughout their lifetimes, 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 these histone PTM alterations persist for at least 4 weeks, irrespective of further salinity changes. However, histone PTMs respond minimally to 4-week-long periods of salinity acclimation during adulthood. The results of this study altogether signify that patterns of histone PTMs in individuals reflect their prolonged exposure to environmental conditions.