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Effects of the increase in CO2 and temperature on the carbon acquisition and assimilation mechanisms in polar macroalgae

Íñiguez Moreno, Concepción

Abstract

Ocean acidification and warming are affecting with special intensity polar regions. The coastal areas are dominated by dense macroalgal communities which represent a major trophic contribution to these systems and have a dominant role in carbon fluxes at regional scale. These macroalgae are expected to be directly affected by the increases in CO2 and temperature. The aim of this thesis is to characterise the physiological acclimation response of ecologically relevant polar seaweeds to an increase in temperature and CO2 to the levels expected by the end of this century. The species-specific differences in their acclimation mechanisms to increased CO2 and temperature will determine which species will benefit from the projected environmental scenario, and which others will be more negatively affected or not altered, enabling to identify winner and loser species as well as the degree of change expected in the community. For this purpose, different experiments using ecologically relevant Arctic and Antarctic macroalgae were done, consisting on the acclimation of thalli to an increase in CO2 and temperature. The results of this thesis have shown that the effects of elevated CO2 on the growth rate of polar macroalgae are species-specific, and that usually do not parallel the effects on photosynthesis. Instead, changes in growth rate were due to a reorganization of the energetic and carbon budget of the cell. Carbon fixation rates of all analysed Arctic species were not altered by increased CO2 levels, indicating that their photosynthesis must be C-saturated at current CO2 conditions. Moreover, all analysed red and brown seaweeds possess Rubiscos with a Kc for CO2 at 4°C of about 2-4 μM. Thus, their Rubiscos are saturated at 22 μM CO2, which is the concentration that corresponds to air-equilibrated seawater at 4°C. This significant increase in the affinity for CO2 at lower temperature observed in all analysed species suggest that polar seaweeds are more likely to possess C-saturated photosynthetic rates than temperate species at their usual environmental temperature, independently of their ability to use HCO3- for photosynthesis. The majority of the analysed polar seaweeds would need more than 1000 ppm CO2 to down-regulate their carbon concentrating mechanisms (CCMs), despite the observed high affinity for CO2 of their Rubiscos at low temperature. This highlights the importance of CCM operation in polar environments as part of a mechanism that ensures high photosynthetic rates in cold waters, of the same order of magnitude as those from temperate latitudes at their respective environmental temperature The results of this thesis provide novel and valuable data on the knowledge of cellular carbon fluxes, biochemical composition, physiology and photochemical performance, carbon acquisition and assimilation mechanisms and transcriptomic responses in polar seaweeds as they are affected by ocean acidification and warming. It includes a novel in-depth analysis of Rubisco kinetics that helps to understand the adaptation mechanisms to polar environments.

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AUTOR: Concepción Íñiguez Moreno http://orcid.org/0000-0002-6452-8280 EDITA: Publicaciones y Divulgación Científica. Universidad de Málaga Esta obra está bajo una licencia de Creative Commons ReconocimientoNoComercial-SinObraDerivada 4.0 Internacional: http://creativecommons.org/licenses/by-nc-nd/4.0/legalcode Cualquier parte de esta obra se puede reproducir sin autorización pero con el reconocimiento y atribución de los autores. No se puede hacer uso comercial de la obra y no se puede alterar, transformar o hacer obras derivadas. Esta Tesis Doctoral está depositada en el Repositorio Institucional de la Universidad de Málaga (RIUMA): riuma.uma.es UNIVERSIDAD DE MÁLAGA FACULTAD DE CIENCIAS DEPARTAMENTO DE ECOLOGÍA Y GEOLOGÍA Área de Ecología Visado en Málaga a 10 de Octubre de 2016 Los directores Fdo. Francisco J. López Gordillo Fdo. F. Xavier Niell Castanera Prof. Titular del Área de Ecología Catedrático del Área de Ecología Universidad de Málaga Universidad de Málaga Memoria presentada para optar al Grado de Doctor en Ciencias Ambientales Fdo. Concepción Iñiguez Moreno UNIVERSIDAD DE MÁLAGA FACULTAD DE CIENCIAS DEPARTAMENTO DE ECOLOGÍA Y GEOLOGÍA Área de Ecología D. Francisco J. López Gordillo, Profesor Titular del Departamento de Ecología y Geología (Área de Ecología) de la Facultad de Ciencias de la Universidad de Málaga, y D. F. Xavier Niell Castanera, Catedrático del Departamento de Ecología y Geología (Área de Ecología) de la Facultad de Ciencias de la Universidad de Málaga CERTIFICAN: Que la presente memoria titulada “Effects of the Increase in CO2 and Temperature on the Carbon Acquisition and Assimilation Mechanisms in Polar Macroalgae” presentada por la Licenciada en Ciencias Ambientales, Concepción Iñiguez Moreno, ha sido realizada bajo nuestra dirección y el trabajo presentado y las publicaciones que lo avalan no han sido utilizado en tesis anteriores. Y considerando que representa trabajo de Tesis Doctoral, autorizamos su exposición y defensa para optar al Grado de Doctor en Ciencias Ambientales. Y para que así conste, a los efectos oportunos, firma el presente en Málaga a 10 de Octubre de 2016. Fdo. Francisco J. López Gordillo Fdo. F. Xavier Niell Castanera Prof. Titular del Área de Ecología Catedrático del Área de Ecología Universidad de Málaga Universidad de Málaga | | | | ∼ ∼ | | δ | δ | | | DIVERGING RESPONSES IN ARCTIC SEAWEEDS TO CO2 |"45" Increased CO2 modifies the carbon balance and the photosynthetic yield of two common Arctic brown seaweeds: Desmarestia aculeata and Alaria esculenta Concepción Iñiguez, Raquel Carmona, M. Rosario Lorenzo, F. Xavier Niell, Christian Wiencke, Francisco J. L. Gordillo Polar Biology (2015) doi: 10 .1007/s00300-015-1724-x Abstract Ocean acidification affects with special intensity Arctic ecosystems, being marine photosynthetic organisms a primary target, although the consequences of this process in the carbon fluxes of Arctic algae are still unknown. The alteration of the cellular carbon balance due to physiological acclimation to an increased CO2 concentration (1300 ppm) in the common Arctic brown seaweeds Desmarestia aculeata and Alaria esculenta from Kongsfjorden (Svalbard) was analysed. Growth rate of D. aculeata was negatively affected by CO2 enrichment while A. esculenta was positively affected, as a result of a different reorganization of the cellular carbon budget in both species. Desmarestia aculeata showed increased respiration, enhanced accumulation of storage biomolecules and elevated release of dissolved organic carbon, whereas A. esculenta showed decreased respiration and lower accumulation of storage biomolecules. Gross photosynthesis (measured both as O2-evolution and 14C-fixation) was not affected in any of them, suggesting that photosynthesis was already saturated at normal CO2 conditions and did not participate in the acclimation response. However, electron transport rate changed in both species in opposite directions, indicating different energy requirements between treatments and species-specificity. High CO2 levels also affected the N-metabolism, and 13C isotopic discrimination values from algal tissue pointed to a deactivation of carbon concentrating mechanisms. Since increased CO2 has the potential to modify physiological mechanisms in different ways in the species studied, it is expected that this may lead to changes in the Arctic seaweed community, which may propagate to the rest of the food web. | INCREASED CO2 AND TEMPERATURE IN TWO ARTIC KELPS |"71" Increased temperature, rather than elevated CO2, modulates the carbon assimilation of the Arctic kelps Saccharina latissima and Laminaria solidungula Concepción Iñiguez, Raquel Carmona, M. Rosario Lorenzo, F. Xavier Niell, Christian Wiencke, Francisco J. L. Gordillo Marine biology (2016) 163: 248, doi:10.1007/s00227-016-3024-6 Abstract Ocean acidification and warming are affecting with special intensity the Arctic Ocean. Arctic coastal ecosystems are dominated by kelp forests with a high biomass production, which are expected to be directly affected by the increases in CO2 and temperature. This study presents the different physiological responses of the Arctic kelps Saccharina latissima and Laminaria solidungula from Kongsfjorden (Svalbard) cultured at 4 and 9°C in combination with current (390 ppm) and increased (1200 ppm) levels of atmospheric CO2. Both species were largely unaffected by increased CO2 conditions. Carbon fixation was not influenced by CO2, indicating that photosynthesis was C-saturated at present levels, and 13C isotopic discrimination values from algal tissue suggested no deactivation of carbon concentrating mechanisms at increased CO2 levels. Inhibition of photosynthesis by carbonic anhydrases (CAs) inhibitors highlighted the important role of external CAs in inorganic carbon acquisition in Arctic kelps. Saccharina latissima showed a significantly higher growth rate at 9°C than at 4°C, probably due to the decrease in the dark respiration rate observed. Growth rate of L. solidungula was not affected by temperature or CO2, and increases in photosynthesis at 9°C could be partially related to a higher dissolved organic carbon release rate. The photochemical performance of both species was not altered by any of the treatments. These results suggest that S. latissima might be more benefited than L. solidungula in a future warmer Arctic, while both populations seem to be resilient to higher CO2 concentrations. | | | | δ δ | δ δ δ | | | | | | δ δ δ | | | | | | | | δ | δ ∆ ε | δ δ δ δ | | | δ δ | | δ | | | ε δ Φ α