Using a high sensitivity differential scanning calorimeter in isothermal mode, we directly measured heat production in eukaryotic protists from 5 phyla spanning over 5 orders of magnitude in carbon biomass and 8 orders of magnitude in cell volume. Our results reveal that metabolic heat production normalized to cell mass is virtually constant in these organisms, with a median of 0.037 pW pg C−1 (95% confidence interval = 0.022–0.061 pW pg C−1) at 5 °C. Contrary to allometric models, the relationship between heat production and cell carbon content or surface area is isometric (scaling exponents, 1.056 and 1.057, respectively). That heat production per unit cell surface area is constant suggests that heat flux through the cell surface is effectively instantaneous, and hence that cells are isothermal with their environment. The results further suggest that allometric models of metabolism based on metazoans are not applicable to protists, and that the underlying metabolic processes in the latter polyphyletic group are highly constrained by evolutionary selection. We propose that the evolutionary constraint leading to a universally constant heat production in single-celled eukaryotes is related to cytoplasmic packaging of organelles and surface area to volume relationships controlling diffusion of resources to these organelles.

Carbon uptake by marine phytoplankton, and its export as organic matter to the ocean interior (i.e., the “biological pump”), lowers the partial pressure of carbon dioxide (pCO2) in the upper ocean and facilitates the diffusive drawdown of atmospheric CO2. Conversely, precipitation of calcium carbonate by marine planktonic calcifiers such as coccolithophorids increases pCO2 and promotes its outgassing (i.e., the “alkalinity pump”). Over the past ≈100 million years, these two carbon fluxes have been modulated by the relative abundance of diatoms and coccolithophores, resulting in biological feedback on atmospheric CO2 and Earth's climate; yet, the processes determining the relative distribution of these two phytoplankton taxa remain poorly understood. We analyzed phytoplankton community composition in the Atlantic Ocean and show that the distribution of diatoms and coccolithophorids is correlated with the nutricline depth, a proxy of nutrient supply to the upper mixed layer of the ocean. Using this analysis in conjunction with a coupled atmosphere–ocean intermediate complexity model, we predict a dramatic reduction in the nutrient supply to the euphotic layer in the coming century as a result of increased thermal stratification. Our findings indicate that, by altering phytoplankton community composition, this causal relationship may lead to a decreased efficiency of the biological pump in sequestering atmospheric CO2, implying a positive feedback in the climate system. These results provide a mechanistic basis for understanding the connection between upper ocean dynamics, the calcium carbonate-to-organic C production ratio and atmospheric pCO2 variations on time scales ranging from seasonal cycles to geological transitions.

Abstract

On the basis of a carbon isotopic record of both marine carbonates and organic matter from the Triassic-Jurassic boundary to the present, we modeled oxygen concentrations over the past 205 million years. Our analysis indicates that atmospheric oxygen approximately doubled over this period, with relatively rapid increases in the early Jurassic and the Eocene. We suggest that the overall increase in oxygen, mediated by the formation of passive continental margins along the Atlantic Ocean during the opening phase of the current Wilson cycle, was a critical factor in the evolution, radiation, and subsequent increase in average size of placental mammals.

Abstract

The community structure and ecological function of contemporary marine ecosystems are critically dependent on eukaryotic phytoplankton. Although numerically inferior to cyanobacteria, these organisms are responsible for the majority of the flux of organic matter to higher trophic levels and the ocean interior. Photosynthetic eukaryotes evolved more than 1.5 billion years ago in the Proterozoic oceans. However, it was not until the Mesozoic Era (251 to 65 million years ago) that the three principal phytoplankton clades that would come to dominate the modern seas rose to ecological prominence. In contrast to their pioneering predecessors, the dinoflagellates, coccolithophores, and diatoms all contain plastids derived from an ancestral red alga by secondary symbiosis. Here we examine the geological, geochemical, and biological processes that contributed to the rise of these three, distantly related, phytoplankton groups.

Over the past three decades, massive bleaching events of zooxanthellate corals have been documented across the range of global distribution. Although the phenomenon is correlated with relatively small increases in sea-surface temperature and enhanced light intensity, the underlying physiological mechanism remains unknown. In this article we demonstrate that thylakoid membrane lipid composition is a key determinate of thermal-stress sensitivity in symbiotic algae of cnidarians. Analyses of thylakoid membranes reveal that the critical threshold temperature separating thermally tolerant from sensitive species of zooxanthellae is determined by the saturation of the lipids. The lipid composition is potentially diagnostic of the differential nature of thermally induced bleaching found in scleractinian corals. Measurements of variable chlorophyll fluorescence kinetic transients indicate that thermally damaged membranes are energetically uncoupled but remain capable of splitting water. Consequently, a fraction of the photosynthetically produced oxygen is reduced by photosystem I through the Mehler reaction to form reactive oxygen species, which rapidly accumulate at high irradiance levels and trigger death and expulsion of the endosymbiotic algae. Differential sensitivity to thermal stress among the various species of Symbiodinium seems to be distributed across all clades. A clocked molecular phylogenetic analysis suggests that the evolutionary history of symbiotic algae in cnidarians selected for a reduced tolerance to elevated temperatures in the latter portion of the Cenozoic.