Gene expression patterns of red sea urchins (Mesocentrotus franciscanus) exposed to different combinations of temperature and pCO2 during early development

Abstract

Background: The red sea urchin Mesocentrotus franciscanus is an ecologically important kelp forest herbivore and an economically valuable wild fishery species. To examine how M. franciscanus responds to its environment on a molecular level, differences in gene expression patterns were observed in embryos raised under combinations of two temperatures (13 °C or 17 °C) and two pCO₂ levels (475 μatm or 1050 μatm). These combinations mimic various present-day conditions measured during and between upwelling events in the highly dynamic California Current System with the exception of the 17 °C and 1050 μatm combination, which does not currently occur. However, as ocean warming and acidification continues, warmer temperatures and higher pCO₂ conditions are expected to increase in frequency and to occur simultaneously. The transcriptomic responses of the embryos were assessed at two developmental stages (gastrula and prism) in light of previously described plasticity in body size and thermotolerance under these temperature and pCO₂ treatments.

Results: Although transcriptomic patterns primarily varied by developmental stage, there were pronounced differences in gene expression as a result of the treatment conditions. Temperature and pCO₂ treatments led to the differential expression of genes related to the cellular stress response, transmembrane transport, metabolic processes, and the regulation of gene expression. At each developmental stage, temperature contributed significantly to the observed variance in gene expression, which was also correlated to the phenotypic attributes of the embryos. On the other hand, the transcriptomic response to pCO₂ was relatively muted, particularly at the prism stage.

Conclusions: M. franciscanus exhibited transcriptomic plasticity under different temperatures, indicating their capacity for a molecular-level response that may facilitate red sea urchins facing ocean warming as climate change continues. In contrast, the lack of a robust transcriptomic response, in combination with observations of decreased body size, under elevated pCO₂ levels suggest that this species may be negatively affected by ocean acidification. High present-day pCO₂ conditions that occur due to coastal upwelling may already be influencing populations of M. franciscanus.

Keywords: Climate change; Early development; Mesocentrotus franciscanus; Ocean acidification; RNA-seq; Red sea urchin; Transcriptomics; Warming.

Fig. 1

General gene expression patterns. Principal component analysis (PCA) plots of a all samples, c the gastrula stage only, and e the prism stage only are displayed with the two components that explained the most variance. Pie charts (b, d, and f) display the percent of variation explained by fixed factors determined using permutational multivariate ANOVAs (*p < 0.05 and ***p < 0.001). For b all samples, fixed factors included developmental stage, temperature treatment, and pCO₂ treatment. The interactions of the three fixed factors have been consolidated into a single, “Interactions” pie chart segment for figure simplicity. For d the gastrula stage and f the prism stage, fixed factors only included temperature and pCO₂ treatment

Fig. 2

Correlations at a the gastrula stage and b the prism stage between PC1-PC8 (columns), which contribute > 80% of the explained variation in gene expression, and metadata variables (rows) of the experiment treatments (i.e., temperature and pCO₂), body size (i.e. embryo length in mm), and thermotolerance (i.e. LT₅₀ in °C, prism stage only). The orange-purple color scale represents the strength of the Pearson’s correlation (1 to − 1). *p < 0.05, **p < 0.01, and ***p < 0.001

Fig. 3

Temperature, and to a lesser degree, pCO₂ treatments caused differential gene expression at a, b the gastrula stage and c, d the prism stage of early development. Genes that were not differentially expressed are displayed in gray while significant DE genes (adjusted p-value < 0.05) are displayed in color with a few selected genes labelled. Significant DE genes that were up-regulated are shown in pink (0 < log₂ FC < 1) and red (log₂ FC ≥ 1) and significant DE genes that were down-regulated are shown in light blue (− 1 < log₂ FC < 0) and blue (log₂ FC ≤ − 1)

Fig. 4

GO results of genes expressed at the gastrula stage. Analysis determined significant enrichment within GO categories of genes up-regulated (red text) and down-regulated (blue text) due to a temperature and b pCO₂ treatments in gastrula embryos. Font sizes of the category names indicate the level of statistical significance as noted in the legend. The fraction preceding each category name is the number of genes with moderated t-statistic absolute values > 1 relative to the total number of genes belonging to the category. GO categories of molecular function (MF) and biological process (BP) are shown

Fig. 5

GO results of genes expressed at the prism stage. Analysis determined significant enrichment within GO categories of genes up-regulated (red text) and down-regulated (blue text) due to a temperature and b pCO₂ treatments in prism embryos. Font sizes of the category names indicate the level of statistical significance as noted in the legend. The fraction preceding each category name is the number of genes with moderated t-statistic absolute values > 1 relative to the total number of genes belonging to the category. GO categories of molecular function (MF) and biological process (BP) are shown