Interactive effects of cell size, temperature and nutrient supply on resource allocation, metabolic rates and growth of marine phytoplankton

Resumo

Phytoplankton are photosynthetic unicellular organisms that belong to 8 different phyla and span more than 9 orders of magnitude in cell volume. Through photosynthesis they control the carbon fluxes in the ocean where they are exposed to multiple and simultaneous environmental changes that can alter the metabolic activity of individual organisms with community and ecosystem implications. Temperature and nutrient supply are two major environmental drivers that control phytoplankton ecophysiology whereas cell size is a key functional trait that profoundly influences phytoplankton growth and community structure in the ocean. While the effect of temperature on metabolic rates has been shown to be nutrient-dependent, the role of these two drivers is commonly investigated in isolation. In addition, there is evidence that phytoplankton growth rates peak at intermediate cell sizes, but it is still unknown if this pattern may have resulted from the effect of experimental temperature. The metabolic theory of ecology and the ecological stoichiometry serve to integrate observations of processes and patterns at the individual, population, and community level. Based on this theoretical framework, this Thesis investigates the combined role of cell size, temperature and nutrient availability as determinants of phytoplankton physiology and ecology at different levels of biological organization, from molecules to populations and communities. The results obtained show that the unimodal relationship between phytoplankton cell size and maximum growth rate, with a peak at intermediate cell sizes, persists irrespective of temperature (18ºC, 25ºC and Topt) and of the metric employed to quantify standing stocks. Growth rates calculated with chlorophyll a concentration, in vivo fluorescence or cellular abundance tend to overestimate the growth rate calculated with biomass (particulate organic carbon or nitrogen). Temperature and nutrient supply are shown to interactively control resource allocation, photosynthetic strategy and metabolism of the cosmopolitan cyanobacterium Synechococcus. Resource investment into PSII and chlorophyll a increases with temperature (to balance the presumably higher activity of RuBisCO) under nutrient-replete conditions but not under strong nutrient limitation. Low temperature and abundant nutrients caused increased RuBisCO abundance, a pattern observed both in Synechococcus cultures and in natural phytoplankton assemblages across a wide latitudinal range in the Atlantic Ocean. Furthermore, the stimulating effect of increasing temperature upon photosynthesis and respiration of Synechococcus sp. takes place only under nutrient-replete conditions. The combined role of temperature and nutrient supply still had not been addressed experimentally in the vast oligotrophic regions of the tropical and subtropical ocean. After conducting four microcosms experiments in the tropical and subtropical Atlantic (29ºN-27ºS), we found that chlorophyll a concentration and the biomass of pico- and small nanophytoplankton consistently increased in response to nutrient addition, whereas changes in temperature over a 6°C range had a smaller and more variable effect. Nutrient enrichment led to increased picoeukaryote abundance, depressed Prochlorococcus abundance, and increased contribution of small nanophytoplankton to total biomass. The largest biomass increase in response to nutrient addition was measured in the least oligotrophic and warmest site, where we also found the highest cellular chlorophyll a content, an effect synergistically enhanced under combined warming and nutrient-enriched conditions. These observations do not support the hypothesis that phytoplankton living in the warmest regions are most vulnerable to temperature increases. The results of this Thesis demonstrate the need to address the complexity of marine ecosystems by accounting for the interaction of several factors together and contribute to increase our understanding of the interactive effects of cell size, temperature and nutrient availability for phytoplankton ecophysiology across multiple levels of biological organization.