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.

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.

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.

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.