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While it is known that increased dissolved CO 2 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 CO 2 conditions. We show that long-term warming has more pronounced impacts than elevated CO 2 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 CO 2 , 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 CO 2 . 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 CO 2 on the adaptation of marine phytoplankton in the context of global change., (© 2024 Society for Experimental Biology and John Wiley & Sons Ltd.)

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., (© The Author(s) 2023. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: journals.permissions@oup.com.)

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., Competing Interests: Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper., (Copyright © 2023 Elsevier Ltd. All rights reserved.)

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 pCO 2 , 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 CO 2 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 CO 2 can modulate these antagonistic interactions, and conclude that long-term adaptation to sea surface warming and rising CO 2 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., Competing Interests: Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper., (Copyright © 2023 Elsevier Ltd. All rights reserved.)

Although high CO 2 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 CO 2 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 CO 2 . However, this diversity loss was less under high CO 2 combined with warming, suggesting that the evolution driven by warming was constrained by high CO 2 . 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., (© 2022. The Author(s), under exclusive licence to International Society for Microbial Ecology.)

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 CO 2 selected populations at relatively high heavy metal levels. Those findings suggest that the adaptations to high CO 2 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 CO 2 conditions, and improves our understanding of the complex interactions of future OA and heavy metal pollution in marine waters., Competing Interests: Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper., (Copyright © 2022 Elsevier Ltd. All rights reserved.)

Phytoplankton are responsible for nearly half of global primary productivity and play crucial roles in the Earth's biogeochemical cycles. However, the long-term adaptive responses of phytoplankton to rising CO 2 remains unknown. Here we examine the physiological and proteomics responses of a marine diatom, Phaeodactylum tricornutum, following long-term (c. 900 generations) selection to high CO 2 conditions. Our results show that this diatom responds to long-term high CO 2 selection by downregulating proteins involved in energy production (Calvin cycle, tricarboxylic acid cycle, glycolysis, oxidative pentose phosphate pathway), with a subsequent decrease in photosynthesis and respiration. Nearly similar extents of downregulation of photosynthesis and respiration allow the high CO 2 -adapted populations to allocate the same fraction of carbon to growth, thereby maintaining their fitness during the long-term high CO 2 selection. These results indicate an important role of metabolism reduction under high CO 2 and shed new light on the adaptive mechanisms of phytoplankton in response to climate change., (© 2021 The Authors. New Phytologist © 2021 New Phytologist Foundation.)

Ocean acidification and warming are recognized as two major anthropogenic perturbations of the modern ocean. However, little is known about the adaptive response of phytoplankton to them. Here we examine the adaptation of a marine diatom Thalassiosira weissflogii to ocean acidification in combination with ocean warming. Our results show that ocean warming have a greater effect than acidification on the growth of T. weissflogii over the long-term selection experiment (~380 generations), as well as many temperature response traits (e.g., optimum temperatures for photosynthesis, maximal net photosynthetic oxygen evolution rates, activation energy) in thermal reaction norm. These results suggest that ocean warming is the main driver for the evolution of the marine diatom T. weissflogii, rather than oceanacidification. However, the evolution resulting from warming can be constrained by ocean acidification, where ocean warming did not impose any effects at high CO 2 level. Furthermore, adaptations to ocean warming alone or to the combination of ocean acidification and warming come with trade-offs by inhibiting photochemical performances. The constrains and trade-offs associated with the adaptation to ocean acidification and warming demonstrated in this study, should be considered for parameterizing evolutionary responses in eco-evolutionary models of phytoplankton dynamics in a future ocean., Competing Interests: Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper., (Copyright © 2021 Elsevier B.V. All rights reserved.)

In this study, we examined the effects of increased temperature (15, 20 and 25 °C) and different light levels (50, 200 μmol photons m -2 s -1 ) on two widely distributed diatoms, namely Phaeodactylum tricornutum and Thalassiosira weissflogii. Results showed that increasing light level counteracted the negative effects of high temperature on photosynthesis in both species, suggesting an antagonistic interaction between light and temperature. Contrary to the above results, light limitation diminished the temperature-sensitivity of carbonic anhydrase activity in two diatoms. We also observed species-specific responses of biomass, where increased temperature significantly decreased the biomass of P. tricornutum at both low and high light levels but showed no effects on T. weissflogii. Our study demonstrated that light can alter the physiological responses of diatoms to temperature but also revealed interspecific variations. We predict that in the future ocean with shallower upper mixed layer, T. weissflogii may be more competitive than P. tricornutum., Competing Interests: Declaration of competing interest The authors declare that they have no conflict of interest., (Copyright © 2020 Elsevier Ltd. All rights reserved.)

Diatoms are experiencing striking fluctuations in seawater carbonate chemistry in the natural marine environment, especially in coastal seawaters. Here, we show that the diatoms Thalassiosira weissflogii and Phaeodactylum tricornutum, which utilize different carbon acquisition mechanisms, respond differently to short-term changes in seawater carbonate chemistry. Our results showed that T. weissflogii showed significantly higher photosynthetic oxygen evolution rates than that of P. tricornutum at low levels of CO 2 or HCO 3 - . This suggests that T. weissflogii had higher affinities for CO 2 when their concentrations were not sufficient to support saturated growth and photosynthesis. While the activity of Rubisco in P. tricornutum positively correlated with carbonic anhydrases (CA), we observed negative relationship between Rubisco and CA activity in the diatom T. weissflogii. These contrasting physiological responses of diatoms with varied carbon acquisition mechanisms indicate different abilities to cope up with abrupt changes in seawater carbonate chemistry. We propose that the ability to respond to varying carbonate chemistry may act as one determinant of the diatom distributions and phytoplankton community structures.3 - when their concentrations were not sufficient to support saturated growth and photosynthesis. While the activity of Rubisco in P. tricornutum positively correlated with carbonic anhydrases (CA), we observed negative relationship between Rubisco and CA activity in the diatom T. weissflogii. These contrasting physiological responses of diatoms with varied carbon acquisition mechanisms indicate different abilities to cope up with abrupt changes in seawater carbonate chemistry. We propose that the ability to respond to varying carbonate chemistry may act as one determinant of the diatom distributions and phytoplankton community structures.

A classical red tide alga Skeletonema costatum was cultured under various nitrate levels to investigate its physiological response to nitrate enrichment combined with CO 2 limitation. The higher nitrate levels increased content of photosynthetic pigments (Chl a and Chl c), electron transport rate in photosystem II, photosynthetic O 2 evolution, and thus growth rate in S. costatum. On the other hand, the lower CO 2 levels (3.5-4.4 μmol kg -1 seawater) and higher pH (8.56-8.63) values in seawater were observed under higher nitrate conditions. Redox activity of plasma membrane and carbonic anhydrase in S. costatum was enhanced to address the reduced CO 2 level at higher nitrate levels. In addition, the pH compensation point was enhanced and direct HCO 3 - use was induced at higher nitrate levels. These findings indicate that nitrate enrichment would stimulate the breakout of S. costatum dominated red tides via enhancing its photosynthetic performances, and maintain a quick growth rate under CO 2 limitation conditions through improving its inorganic carbon acquisition capability. Our study sheds light on the mechanisms of S. costatum defeating CO 2 limitation during algal bloom., (Copyright © 2017 Elsevier Ltd. All rights reserved.)

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. [ABSTRACT FROM AUTHOR]

Diatoms are experiencing striking fluctuations in seawater carbonate chemistry in the natural marine environment, especially in coastal seawaters. Here, we show that the diatoms Thalassiosira weissflogii and Phaeodactylum tricornutum, which utilize different carbon acquisition mechanisms, respond differently to short-term changes in seawater carbonate chemistry. Our results showed that T. weissflogii showed significantly higher photosynthetic oxygen evolution rates than that of P. tricornutum at low levels of CO2 or HCO3−. This suggests that T. weissflogii had higher affinities for CO2 or HCO3− when their concentrations were not sufficient to support saturated growth and photosynthesis. While the activity of Rubisco in P. tricornutum positively correlated with carbonic anhydrases (CA), we observed negative relationship between Rubisco and CA activity in the diatom T. weissflogii. These contrasting physiological responses of diatoms with varied carbon acquisition mechanisms indicate different abilities to cope up with abrupt changes in seawater carbonate chemistry. We propose that the ability to respond to varying carbonate chemistry may act as one determinant of the diatom distributions and phytoplankton community structures. [ABSTRACT FROM AUTHOR]