DNA methylation and gene transcription act cooperatively in driving the adaptation of a marine diatom to global change.

Genetic changes together with epigenetic modifications such as DNA methylation have been demonstrated to regulate many biological processes and thereby govern the response of organisms to environmental changes. However, how DNA methylation might act cooperatively with gene transcription and thereby mediate the long-term adaptive responses of marine microalgae to global change is virtually unknown. Here we performed a transcriptomic analysis, and a whole-genome bisulfite sequencing, along with phenotypic analysis of a model marine diatom Phaeodactylum tricornutum adapted for 2 years to high CO2 and/or warming conditions. Our results show that the methylated islands (peaks of methylation) mCHH were positively correlated with expression of genes in the subregion of the gene body when the populations were grown under high CO2 or its combination with warming for ~2 years. We further identified the differentially expressed genes (DEGs), and hence the metabolic pathways in which they function, at the transcriptomics level in differentially methylated regions (DMRs). Although DEGs in DMRs contributed only 18-24% of the total DEGs, we found that those DEGs acted cooperatively with DNA methylation and then regulated key processes such as central carbon metabolism, amino acid metabolism, ribosome biogenesis, terpenoid backbone biosynthesis, and degradation of misfolded proteins. Taken together, by integrating transcriptomic, epigenetic, and phenotypic analysis, our study provides evidence for DNA methylation acting cooperatively with gene transcription to contribute to the adaptation of microalgae to global changes.

Long-term adaptation to elevated temperature but not CO2 alleviates the negative effects of ultraviolet-B radiation in a marine diatom.

Multifaceted changes in marine environments as a result of anthropogenic activities are likely to have a compounding impact on the physiology of marine phytoplankton. Most studies on the combined effects of rising pCO2, sea surface temperature, and UVB radiation on marine phytoplankton were only conducted in the short-term, which does not allow to test the adaptive capacity of phytoplankton and associated potential trade-offs. Here, we investigated populations of the diatom Phaeodactylum tricornutum that were long-term (∼3.5 years, ∼3000 generations) adapted to elevated CO2 and/or elevated temperatures, and their physiological responses to short-term (∼2 weeks) exposure of two levels of ultraviolet-B (UVB) radiation. Our results showed that while elevated UVB radiation showed predominantly negative effects on the physiological performance of P. tricornutum regardless of adaptation regimes. Elevated temperature alleviated these effects on most of the measured physiological parameters (e.g., photosynthesis). We also found that elevated CO2 can modulate these antagonistic interactions, and conclude that long-term adaptation to sea surface warming and rising CO2 may alter this diatom's sensitivity to elevated UVB radiation in the environment. Our study provides new insights into marine phytoplankton's long-term responses to the interplay of multiple environmental changes driven by climate change.

Increased genetic diversity loss and genetic differentiation in a model marine diatom adapted to ocean warming compared to high CO2.

Although high CO2 and warming could act interactively on marine phytoplankton, little is known about the molecular basis for this interaction on an evolutionary scale. Here we explored the adaptation to high CO2 in combination with warming in a model marine diatom Phaeodactylum tricornutum. Whole-genome re-sequencing identifies, in comparison to populations grown under control conditions, a larger genetic diversity loss and a higher genetic differentiation in the populations adapted for 2 years to warming than in those adapted to high CO2. However, this diversity loss was less under high CO2 combined with warming, suggesting that the evolution driven by warming was constrained by high CO2. By integrating genomics, transcriptomics, and physiological data, we found that the underlying molecular basis for this constraint is associated with the expression of genes involved in some key metabolic pathways or biological processes, such as the glyoxylate pathway, amino acid and fatty acid metabolism, and diel variability. Our results shed new light on the evolutionary responses of marine phytoplankton to multiple environmental changes in the context of global change and provide new insights into the molecular basis underpinning interactions among those multiple drivers.

Additive impacts of ocean acidification and ambient ultraviolet radiation threaten calcifying marine primary producers.

Ocean acidification (OA) represents a threat to marine organisms and ecosystems. However, OA rarely exists in isolation but occurs concomitantly with other stressors such as ultraviolet radiation (UVR), whose effects have been neglected in oceanographical observations. Here, we perform a quantitative meta-analysis based on 373 published experimental assessments from 26 studies to examine the combined effects of OA and UVR on marine primary producers. The results reveal predominantly additive stressor interactions (69-84% depending on the UV waveband), with synergistic and antagonistic interactions being rare but significantly different between micro- and macro-algae. In microalgae, variations in interaction type frequencies are related to cell volume, with antagonistic interactions accounting for a higher proportion in larger sized species. Despite additive interactions being most frequent, the small proportion of antagonistic interactions appears to have a stronger power, leading to neutral effects of OA in combination with UVR. High levels of UVR at near in situ conditions in combination with OA showed additive inhibition of calcification, but not when UVR was low. The results also reveal that the magnitude of responses is strongly dependent on experimental duration, with the negative effects of OA on calcification and pigmentation being buffered and amplified by increasing durations, respectively. Tropical primary producers were more vulnerable to OA or UVR alone compared to conspecifics from other climatic regions. Our analysis highlights that further multi-stressor long-term adaptation experiments with marine organisms of different cell volumes (especially microalgae) from different climatic regions are needed to fully disclose future impacts of OA and UVR.

Lipid Remodeling Reveals the Adaptations of a Marine Diatom to Ocean Acidification.

Ocean acidification is recognized as a major anthropogenic perturbation of the modern ocean. While extensive studies have been carried out to explore the short-term physiological responses of phytoplankton to ocean acidification, little is known about their lipidomic responses after a long-term ocean acidification adaptation. Here we perform the lipidomic analysis of a marine diatom Phaeodactylum tricornutum following long-term (∼400 days) selection to ocean acidification conditions. We identified a total of 476 lipid metabolites in long-term high CO2 (i.e., ocean acidification condition) and low CO2 (i.e., ambient condition) selected P. tricornutum cells. Our results further show that long-term high CO2 selection triggered substantial changes in lipid metabolites by down- and up-regulating 33 and 42 lipid metabolites. While monogalactosyldiacylglycerol (MGDG) was significantly down-regulated in the long-term high CO2 selected conditions, the majority (∼80%) of phosphatidylglycerol (PG) was up-regulated. The tightly coupled regulations (positively or negatively correlated) of significantly regulated lipid metabolites suggest that the lipid remodeling is an organismal adaptation strategy of marine diatoms to ongoing ocean acidification. Since the composition and content of lipids are crucial for marine food quality, and these changes can be transferred to high trophic levels, our results highlight the importance of determining the long-term adaptation of lipids in marine producers in predicting the ecological consequences of climate change.