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Transcriptomes shed light on transgenerational and developmental effects of ocean warming on embryos of the sea urchin Strongylocentrotus intermedius.

ABSTRACT: Ocean warming increasingly endangers the fitness of marine invertebrates. Transgenerational effects (TE) potentially mitigate the impacts of environmental stress on the embryos of marine invertebrates. The molecular mechanisms, however, remain largely unknown. Using high-throughput RNA sequencing technology, we investigated the gene expression patterns of embryos (the gastrula stage) of the sea urchin Strongylocentrotus intermedius at different developmental temperatures, whose parents were exposed to long-term (15 months) elevated temperature (A) or not (B). The temperatures at which adults were held for ~4 weeks prior to the start of the experiment (21?°C for A and 18?°C for B) were also used for the development of offspring (high: 21?°C and ambient (laboratory): 18?°C) resulting in four experimental groups (HA and HB at 21?°C, and LA and LB at 18?°C). The embryos were sampled ~24?h after fertilization. All samples were in the gastrula stage. Twelve mRNA libraries (groups HA, HB, LA, LB, 3 replicates for each group) were established for the following sequencing. Embryos whose parents were exposed to elevated temperatures or not showed 1891 significantly different DEGs (differentially expressed genes) at the ambient developmental temperature (LB vs LA, LB as control) and 2203 significantly different DEGs at the high developmental temperature (HB vs HA, HB as control), respectively. This result indicates complex molecular mechanisms of transgenerational effects of ocean warming, in which a large number of genes are involved. With the TE, we found 904 shared DEGs in both LB vs LA (LB as control) and HB vs HA (HB as control) changed in the same direction of expression (i.e., up- or down-regulated), indicating that parental exposed temperatures affect the expression of these genes in the same manner regardless of the development temperature. With developmental exposure, we found 198 shared DEGs in both HB vs LB (HB as control) and HA vs LA (HA as control) changed in the same direction of expression. Of the 198 DEGs, more genes were up-regulated at high developmental temperature. Interestingly, embryos whose parents were exposed to high temperature showed fewer differently expressed DEGs between high and low developmental temperatures than the individuals whose parents were exposed to ambient temperature. The results indicate that gene expressions are probably depressed by the transgenerational effect of ocean warming. The roles of hsp70 and hnf6 in thermal acclimation are highlighted for future studies. The present study provides new insights into the molecular mechanisms of the transgenerational and developmental effects of ocean warming on the embryos of sea urchins.

SUBMITTER: Shi D

PROVIDER: S-EPMC7221070 | biostudies-literature | 2020 May

REPOSITORIES: biostudies-literature

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Transcriptomes shed light on transgenerational and developmental effects of ocean warming on embryos of the sea urchin Strongylocentrotus intermedius.

Shi Dongtao D Zhao Chong C Chen Yang Y Ding Jingyun J Zhang Lisheng L Chang Yaqing Y

Scientific reports 20200513 1

Ocean warming increasingly endangers the fitness of marine invertebrates. Transgenerational effects (TE) potentially mitigate the impacts of environmental stress on the embryos of marine invertebrates. The molecular mechanisms, however, remain largely unknown. Using high-throughput RNA sequencing technology, we investigated the gene expression patterns of embryos (the gastrula stage) of the sea urchin Strongylocentrotus intermedius at different developmental temperatures, whose parents were expo ...[more]

PMID: 32404890

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Project description:Small sea urchins Strongylocentrotus intermedius (1-2 cm of test diameter) are exposed to different environments of light intensities after being reseeded to the sea bottom. With little information available about the behavioral responses of S. intermedius to different light intensities in the environment, we carried out an investigation on how S. intermedius is affected by three light intensity environments in terms of phototaxis, foraging and righting behaviors. They were no light (zero lx), low light intensity (24-209 lx) and high light intensity (252-2,280 lx). Light intensity had obvious different effects on phototaxis. In low light intensity, sea urchins moved more and spent significantly more time at the higher intensity (69-209 lx) (P = 0.046). S. intermedius in high light intensity, in contrast, spent significantly more time at lower intensity (252-690 lx) (P = 0.005). Unexpectedly, no significant difference of movement (average velocity and total distance covered) was found among the three light intensities (P > 0.05). Foraging behavior of S. intermedius was significantly different among the light intensities. In the no light environment, only three of ten S. intermedius found food within 7 min. In low light intensity, nine of 10 sea urchins showed successful foraging behavior to the food placed at 209 lx, which was significantly higher than the ratio of the number (two of 10) when food was placed at 24 lx (P = 0.005). In the high light intensity, in contrast, significantly less sea urchins (three of 10) found food placed at the higher light intensity (2,280 lx) compared with the lower light intensity (252 lx) (10/10, P = 0.003). Furthermore, S. intermedius showed significantly longer righting response time in the high light intensity compared with both no light (P = 0.001) and low light intensity (P = 0.031). No significant difference was found in righting behavior between no light and low light intensity (P = 0.892). The present study indicates that light intensity significantly affects phototaxis, foraging and righting behaviors of S. intermedius and that ~200 lx might be the appropriate light intensity for reseeding small S. intermedius.

Project description:BACKGROUND: Predicting effects of rapid climate change on populations depends on measuring the effects of climate stressors on performance, and potential for adaptation. Adaptation to stressful climatic conditions requires heritable genetic variance for stress tolerance present in populations. METHODOLOGY/PRINCIPAL FINDINGS: We quantified genetic variation in tolerance of early development of the ecologically important sea urchin Centrostephanus rodgersii to near-future (2100) ocean conditions projected for the southeast Australian global change hot spot. Multiple dam-sire crosses were used to quantify the interactive effects of warming (+2-4 °C) and acidification (-0.3-0.5 pH units) across twenty-seven family lines. Acidification, but not temperature, decreased the percentage of cleavage stage embryos. In contrast, temperature, but not acidification decreased the percentage of gastrulation. Cleavage success in response to both stressors was strongly affected by sire identity. Sire and dam identity significantly affected gastrulation and both interacted with temperature to determine developmental success. Positive genetic correlations for gastrulation indicated that genotypes that did well at lower pH also did well in higher temperatures. CONCLUSIONS/SIGNIFICANCE: Significant genotype (sire) by environment interactions for both stressors at gastrulation indicated the presence of heritable variation in thermal tolerance and the ability of embryos to respond to changing environments. The significant influence of dam may be due to maternal provisioning (maternal genotype or environment) and/or offspring genotype. It appears that early development in this ecologically important sea urchin is not constrained in adapting to the multiple stressors of ocean warming and acidification. The presence of tolerant genotypes indicates the potential to adapt to concurrent warming and acidification, contributing to the resilience of C. rodgersii in a changing ocean.

Dataset Information

Transcriptomes shed light on transgenerational and developmental effects of ocean warming on embryos of the sea urchin Strongylocentrotus intermedius.

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Transcriptomes shed light on transgenerational and developmental effects of ocean warming on embryos of the sea urchin Strongylocentrotus intermedius.

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