The adaptive mechanisms of the marine diatom Thalassiosira weissflogii to long-term high CO2 and warming.

While it is known that increased dissolved CO2 concentrations and rising sea surface temperature (ocean warming) can act interactively on marine phytoplankton, the ultimate molecular mechanisms underlying this interaction on a long-term evolutionary scale are relatively unexplored. Here, we performed transcriptomics and quantitative metabolomics analyses, along with a physiological trait analysis, on the marine diatom Thalassiosira weissflogii adapted for approximately 3.5 years to warming and/or high CO2 conditions. We show that long-term warming has more pronounced impacts than elevated CO2 on gene expression, resulting in a greater number of differentially expressed genes (DEGs). The largest number of DEGs was observed in populations adapted to warming + high CO2, indicating a potential synergistic interaction between these factors. We further identified the metabolic pathways in which the DEGs function and the metabolites with significantly changed abundances. We found that ribosome biosynthesis-related pathways were upregulated to meet the increased material and energy demands after warming or warming in combination with high CO2. This resulted in the upregulation of energy metabolism pathways such as glycolysis, photorespiration, the tricarboxylic acid cycle, and the oxidative pentose phosphate pathway, as well as the associated metabolites. These metabolic changes help compensate for reduced photochemical efficiency and photosynthesis. Our study emphasizes that the upregulation of ribosome biosynthesis plays an essential role in facilitating the adaptation of phytoplankton to global ocean changes and elucidates the interactive effects of warming and high CO2 on the adaptation of marine phytoplankton in the context of global change.

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.

Multi-trait analysis reveals large interspecific differences for phytoplankton in response to thermal change.

Understanding the responses of multiple traits in phytoplankton, and identifying interspecific variabilities to thermal changes is crucial for predicting the impacts of ocean warming on phytoplankton distributions and community structures in future scenarios. Here, we applied a trait-based approach by examining the patterns in multi-traits variations (eight traits) and interspecific variabilities in five phytoplankton species (two diatoms, three dinoflagellates) in response to a wide range of ecologically relevant temperatures (14-30 °C). Our results show large inter-traits and interspecific variabilities of thermal reaction norms in all of the tested traits. We also found that the interspecific variability exceeded the variations induced by thermal changes. Constrained variations and trade-offs between traits both revealed substantial interspecific differences and shifted as the temperature changed. Our study helps to understand the species-specific response patterns of multiple traits to ocean warming and to investigate the implications of these responses in the context of global 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.

Adaptation of a marine diatom to ocean acidification increases its sensitivity to toxic metal exposure.

Most previous studies investigating the interplay of ocean acidification (OA) and heavy metal on marine phytoplankton were only conducted in short-term, which may provide conservative estimates of the adaptive capacity of them. Here, we examined the physiological responses of long-term (~900 generations) OA-adapted and non-adapted populations of the diatom Phaeodactylum tricornutum to different concentrations of the two heavy metals Cd and Cu. Our results showed that long-term OA selected populations exhibited significantly lower growth and reduced photosynthetic activity than ambient CO2 selected populations at relatively high heavy metal levels. Those findings suggest that the adaptations to high CO2 results in an increased sensitivity of the marine diatom to toxic metal exposure. This study provides evidence for the costs and the cascading consequences associated with the adaptation of phytoplankton to elevated CO2 conditions, and improves our understanding of the complex interactions of future OA and heavy metal pollution in marine waters.