A reduction in metabolism explains the tradeoffs associated with the long-term adaptation of phytoplankton to high CO2 concentrations.

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 CO2 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 CO2 conditions. Our results show that this diatom responds to long-term high CO2 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 CO2 -adapted populations to allocate the same fraction of carbon to growth, thereby maintaining their fitness during the long-term high CO2 selection. These results indicate an important role of metabolism reduction under high CO2 and shed new light on the adaptive mechanisms of phytoplankton in response to climate change.

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.

Adaptation of a marine diatom to ocean acidification and warming reveals constraints and trade-offs.

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 CO2 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.

Light alters the responses of two marine diatoms to increased warming.

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.