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

Abstract

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.

Keywords: Epigenetics; Euryhaline fish; Mass spectrometry; Salinity stress; Stress-induced evolution.

Fig. 1

Impact of short-term salinity treatments on histone PTMs. Volcano plots depict the differences in histone PTMs between short-term salinity treatments. All histone PTMs were plotted based on their conditioned q-value and fold change. Panels A-C depict histone PTMs in the gills when comparisons were made between the fish exposed to SW and FW treatments (A), SW/FW and FW treatments (B), and SW and SW/FW treatments (C). Panels D-F depict histone PTMs in the kidney when comparisons were made between the fish exposed to SW and FW treatments (D), SW/FW and FW treatments (E), and SW and SW/FW treatments (F). Finally, panels G-I depict histone PTMs in the testes when comparisons were made between the fish exposed to SW and FW treatments (G), SW/FW and FW treatments (H), and SW and SW/FW treatments (I). Histone PTMs were colored according to their significance in terms of conditioned q-value (blue), fold change (green), both conditioned q-value and fold change (red), or neither (gray). The salinity-responsive histone PTM H1K16ub is labeled accordingly

Fig. 2

Impact of long-term salinity treatments on histone PTMs. Volcano plots depict the differences in histone PTMs between long-term salinity treatments. All histone PTMs were plotted based on their conditioned q-value and fold change. Panels A-C depict histone PTMs in the gills when comparisons were made between the fish exposed to S1 and S0 treatments (A), S3 and S0 treatments (B), and S3 and S1 treatments (C). Panels D-F depict histone PTMs in the kidney when comparisons were made between the fish exposed to S1 and S0 treatments (D), S3 and S0 treatments (E), and S3 and S1 treatments (F). Finally, panels G-I depict histone PTMs in the testes when comparisons were made between the fish exposed to S1 and S0 treatments (G), S3 and S0 treatments (H), and S3 and S1 treatments (I). Histone PTMs were colored according to their significance in terms of conditioned q-value (blue), fold change (green), both conditioned q-value and fold change (red), or neither (gray). Salinity-responsive histone PTMs are labeled according to their abbreviated names

Fig. 3

The influence of short-term salinity stress on H1K16ub. The mean relative abundance of H1K16ub in the gills is displayed for fish exposed to each of the short-term salinity treatments (A). Error bars represent the mean ± the standard error of the mean. The quantification of H1K16ub was based on the abundance of six modified versions of peptides and 39 unmodified versions of peptides. Panels B-C correspond to one of the modified peptides, SEEAPAPAPAPAKAAK[+ 114]KKTTASKPKKVGPSVGE, that contributed to H1K16ub quantification. The library spectrum (B) and an example peak (C) of this modified peptide are presented. Panels D-E depict a distinctive library spectrum (D) and example peak (E) from one of the unmodified peptides, S[+ 42]EEAPAPAPAPAK[+ 57]AAKKKTTASKPKKVGPSVGE

Fig. 4

The influence of long-term salinity stress on H1S1ac. The mean relative abundance of H1S1ac in the gills is displayed for fish exposed to each of the long-term salinity treatments (A). Error bars represent the mean ± the standard error of the mean. The quantification of H1S1ac was based on the abundance of ten modified versions of peptides and 31 unmodified versions of peptides. Panels B-C represent one of the modified peptides that contributed to H1S1ac quantification, being S[+ 42]EEAPAPAPAPAKAAKKKKTTASK[+ 57]PKKVGPSVGE. For this modified peptide, the library spectrum (B) and an example peak (C) from the program Skyline are shown. Panels D-E correspond to one of the unmodified peptides, SEEAPAPAPAPAKAAKKKKTTASKPKKVGPSVGE, which has a distinctive library spectrum (D) and example peak (E)

Fig. 5

The influence of long-term salinity stress on H3K14ac. The mean relative abundance of H3K14ac in the testes is displayed for fish exposed to each of the long-term salinity treatments (A). Error bars represent the mean ± the standard error of the mean. The quantification of H3K14ac was based on the abundance of three modified versions of peptides and seven unmodified versions of peptides. Panels B-C represent one of the modified peptides that contributed to H3K14ac quantification, being K[+ 112]STGGK[+ 42]APR. For this modified peptide, the library spectrum (B) and an example peak (C) from the program Skyline are shown. Panels D-E correspond to one of the unmodified peptides, K[+ 112]STGGK[+ 56]APR, which has a distinctive library spectrum (D) and example peak (E)

Fig. 6

The influence of long-term salinity stress on H3K18ub. The mean relative abundance of H3K18ub in the testes is displayed for fish exposed to each of the long-term salinity treatments (A). Error bars represent the mean ± the standard error of the mean. The quantification of H3K18ub was based on the abundance of two modified versions of peptides and 13 unmodified versions of peptides. Panels B-C represent one of the modified peptides, K[+ 114]QLATK[+ 42]AAR, that contributed to H3K18ub quantification. The library spectrum (B) and an example peak (C) from the program Skyline are shown for this modified peptide. Panels D-E depict a distinctive library spectrum (D) and example peak (E) from one of the unmodified peptides, K[+ 56]QLATK[+ 42]AAR