Phytoplankton facing global changeEcological and physiological perspectives

Resumen

The global change induced by human action is the result of the interaction of multiple abiotic factors. Today, a crucial field of research concerns the study of how ecosystems will respond to future environmental conditions, since global-change factors interact synergistically or antagonistically and can aggravate or mitigate the effects of this phenomenon. In this thesis, an analysis is undertaken concerning the alteration of three abiotic factors associated with the current climatic crisis (temperature increase; greater UV radiation-exposure and increase in nutrient concentration) and the impact on phytoplanktonic organisms, located at the base of aquatic trophic webs, from a physiological and ecological perspective. The connection between these two aspects has scarcely been studied, despite that an understanding of physiological responses is necessary to understand ecological dynamics. Furthermore, this thesis focuses on photosynthetic microorganisms that have phagotrophic ability within the same cell (i.e. mixotrophic protists). In recent decades, this metabolic capacity has been discovered to be widespread among phytoplankton groups. Therefore, it becomes critical to determine how mixotrophic cells might respond to global-change factors, regulating their metabolism towards autotrophy or heterotrophy, as well as to examine the implications for the energy and nutrient fluxes. This thesis is designed to help fill these information gaps carrying out experiments and observational studies over different time scales (from hours to years); at different levels of biological organization (from the cell to ecosystems); and with organisms from different environments (natural marine samples, freshwater and laboratory cultures). The results of these experiments show the effects of global-change factors on marine and freshwater organisms. Our experiments in the Alboran Sea (Chapter 2) have revealed a dual sensitivity to Saharan dust and UVR exposure between areas located inside and outside of oligotrophic gyres, where autotrophic picoplankton plays an important role in primary production and biogeochemical cycles. The results indicate greater sensitivity in the offshore area (within the gyre) than in the nearshore area (outside the gyre), and reveal how the microbial web of two different communities can respond differently to future conditions of high UVR-incidence and higher nutrient inputs associated with Saharan dust. Global change factors (higher temperature or UVR exposure) exert a strong influence on the high mountain regions. Furthermore, peaks of the Iberian Peninsula are also exposed to dust inputs from Sahara desert. To test the impact of these factors on freshwater ecosystems, an observational study was conducted on 13 lakes in Sierra Nevada mountains (southern Spain), examining how global change has altered the algae-bacteria interaction over a 10-year period (2005-2015) (Chapter 3). The results showed that the relationship between the two components changed from bacterivory control by algae to a commensalistic relationship, just when the water temperature increased and the N:P sestonic ratio decreased in relation to higher dust inputs. This change in the algae-bacteria relationship could alter the role of mixotrophs in these lakes by acting as a carbon-bypass in the microbial web, reducing the efficiency of biomass transfer to the upper trophic levels. Based on the effect of nutrients and temperature on the algae-bacteria relationship, an investigation was made concerning how the two factors could modulate the metabolism and structure of a simplified protist community. For this, an experiment was undertaken in which two protists species of Sierra Nevada (Chromulina sp. as mixotrophic and Monoraphidium minutum as strict autotrophic species) were exposed to different temperature and nutrient conditions (Chapter 4). According to the results, increased temperature stimulated the metabolic rates while the fluctuation intensified this effect, favouring heterotrophic metabolism according to the Metabolic Theory of Ecology (MTE). However, the nutrient × increased or fluctuating temperature interaction stimulated autotroph more than mixotroph metabolism and abundance. The results show that a higher nutrient concentration limited the effect of rising and fluctuating temperature on protists. This study reveals that a straight application of MTE does not fulfill at higher nutrient concentrations. Given the ubiquity of mixotrophic metabolism in aquatic ecosystems, Chapter 5 deals with the mixotrophic balance in the cell and its regulation under stress factors (temperature and UVR). This was studied with two mixotrophic species (Chromulina sp. and Isochrysis galbana) that occupy different positions along the mixotrophic gradient. The results showed that the Temperature × UVR interaction increased the primary production: bacterivory ratio and displaced the organisms towards autotrophy, regardless of their position on the mixotrophic gradient. This effect can alter the role of mixotrophs in trophic webs and reduce carbon-transfer efficiency and organic matter at the highest levels. Previous results raise the question of whether the combination of phototrophy and phagotrophy is an advantage for mixotrophs. In Chapter 6, a physiological study of mixotrophy in I. galbana is made, analysing the changes in enzymatic activities and composition in the cell driven by phagotrophy. This study revealed that phagotrophy benefits mixotrophic cells by stimulating the activity of β-carboxylase enzymes, boosting the phosphorous-cell quota, and accelerating the cell-division rate, thereby potentially improving cell fitness. On the other hand, conditions that should stimulate phagotrophy and under which mixotrophy could be a distinctive trait (low light and low nutrients) led the cell to a state of high stress, activating mechanisms that dissipate the reducing power. These results indicate that, despite increasing phagotrophy, I. galbana is predominantly phototrophic and that conditions of low nutrients or light that encourage bacterivory do not imply a greater carbon-flux in the aquatic community. This thesis advances knowledge of the ecological and physiological effects of global change on aquatic ecosystems. The results reflect the need to consider the interaction of multiple abiotic factors that elicit different responses from the phytoplankton community. The results show that phagotrophy is an advantage for mixotrophic cells because it accelerates their growth rate. However, field and laboratory experiments support that the most extreme future environmental conditions will negatively affect mixotrophs and will benefit strict autotrophs. All this improves our predictive capacity concerning the structure and functioning of aquatic ecosystems in their adaptation to global change.