Temperature‐dependent evolution of cell morphology and carbon and nutrient content in a marine diatom

Abstract

Phytoplankton are key players in global biogeochemical cycles, and the effects of ocean warming on their carbon–nitrogen–phosphorus (CNP) stoichiometry, photosynthesis, size, morphology, growth rates, and other traits are of great ecological consequence. The physiological mechanisms of adaptation to temperature in phytoplankton are poorly understood, as are the consequences of the evolution of these processes (e.g., nutrient uptake, photosynthesis) for global biogeochemistry. In general, high temperatures favor smaller cells with higher surface area‐to‐volume ratios, but repeatable patterns in cellular CNP stoichiometry across temperature remain elusive. Here, we compared thermal reaction norms for cellular C, N, P, and chlorophyll a (Chl a) content and for carbon assimilation rate in replicate populations of the marine diatom Thalassiosira pseudonana evolved for 500 generations at 16°C and 31°C. We also examined the thermal reaction norms for cell volume and morphological traits. T. pseudonana has a cylindrical frustule and likely primarily exchanges materials with the environment through the round valve faces. We found that the 31°C‐selected T. pseudonana populations had smaller cells and higher per‐biovolume densities of nutrients and Chl a than the 16°C‐selected populations across assay temperatures but there were no detectable patterns in CNP stoichiometry. The 31°C‐selected populations also had higher valve surface area‐to‐cell volume ratio that increased more with temperature, suggesting better nutrient uptake capabilities than in the 16°C‐selected populations. Our study demonstrates that temperature‐dependent physiological plasticity may evolve differently at different temperatures and suggests that future phytoplankton communities will consist of smaller, more nutrient‐dense cells.

Multi-Omics Profiling Reveals Resource Allocation and Acclimation Strategies to Temperature Changes in a Marine Dinoflagellate

“…Meanwhile, the POC/PON ratio of P. shikokuense increased and peaked at 25℃ with a value of 6.68 (very close to 106:16). This change in POC/PON ratio may be due to the fact that the PON content decreased faster than POC when exposed to higher temperature, and is consistent with the finding of a previous study that diatom cells with smaller size at high temperature may increase photosynthetic efficiency per Chl a and boost cellular C per biovolume with low N input (34). Among the detected carbohydrates, L-fucose and mannitol varied largely and accumulated gradually with increasing temperatures (Fig.…”

Mechanistic constraints on the trade-off between photosynthesis and respiration in response to warming

“…Solid lines correspond to the model simulation calibrated to data from T. pseudonana CCMP1335 ( 13 ), dashed lines correspond to Chaetoceros sp. CCMP160 ( 29 ), and dotted lines correspond to T. pseudonana CCMP1335 (table S3) ( 14 ). Here, we assume that the cell can only invest in glycolysis to fuel dark respiration, but model validation was also performed assuming that the cell can only invest in lipid degradation (fig.…”

“…This is motivated by recent work that showed that some trait correlations (e.g., between metabolism and size) can be altered through adaptation ( 12 ). An experimental evolution study found that phytoplankton evolved larger cell sizes and higher growth rates due to warming ( 13 ), opposed to the expected smaller cell sizes ( 14 ).…”

“…4B) to accommodate the same concentration of transporters and a higher concentration of lipids in the membrane. S3) (14). Here, we assume that the cell can only invest in glycolysis to fuel dark respiration, but model validation was also performed assuming that the cell can only invest in lipid degradation (fig.…”

Mechanistic constraints on the trade-off between photosynthesis and respiration in response to warming

“…between metabolism and size) can be altered through adaptation (12). In fact, an experimental evolution study found that phytoplankton evolved larger cell sizes and higher growth rates due to warming (13), opposed to the expected smaller cell sizes (14).…”