Implications of phytoplankton cell death losses forcarbon flux in Oceanic food-webs

Abstract

En el océano, las condiciones ambientales adversas independientes de la predación tienen como resultado la muerte y lisis celular del fitoplancton que resulta en la liberación de carbono orgánico disuelto (PDOC) a la columna de agua. Las comunidades bacterianas heterotróficas marinas, normalmente dependientes de esta fuente de carbono para su metabolismo, obtienen un beneficio de la liberación de carbono recién sintetizado a la vez que participan en su reciclaje a través de la red trófica microbiana. A pesar de la repercusión que este proceso puede tener en el ciclo del carbono en los océanos, actualmente se desconoce cual es su contribución en ambientes marinos naturales y en el actual escenario de cambio global. El principal objetivo de esta tesis fue analizar las relaciones existentes entre la mortalidad de células del fitoplancton, la proporción de carbono orgánico disuelto (DOC) liberado por el fitoplancton y la supervivencia microbiana bajo diversas condiciones ambientales. La salud de comunidades naturales fitoplanctónicas y bacterianas, la producción primaria total y la liberación fitoplanctónica de DOC fueron determinadas in situ en diferentes regiones oceánicas que comprendieron los mares Mediterráneo, Ártico, Antártico y Atlántico. Los resultados obtenidos en este estudio demostraron la existencia de una relación entre condiciones ambientales tales como la temperatura del agua y la disponibilidad de nutrientes en la muerte celular del fitoplancton. Además, la mortalidad celular del fitoplancton determinada en estos ambientes puede explicar un 41.4% de la PDOC relativa a la producción primaria total, y en regiones oceánicas oligotróficas del noroeste del Océano Atlántico, este proceso sustentó una alta viabilidad bacteriana. Los resultados obtenidos durantes esta tesis resaltan el crucial papel de la lisis celular del fitoplancton en los océanos y ayudan a comprender cuales son las principales vías de transferencia de carbono desde la fotosíntesis hasta el metabolismo heterotrófico bacteriano.

Important phytoplankton losses by cell death, independent of grazing are occurring in the ocean. Phytoplankton cells have been described to die upon encountering adverse environmental conditions, and cell death and lysis would result in the release of the carbon incorporated in the photosynthesis by the phytoplankton as dissolved organic carbon (PDOC). The availability of dissolved organic carbon (DOC) is a major constraint for the heterotrophic bacteria, consequently the release by cell mortality of the recently photosynthate carbon is expected to benefit the bacterial community and should be channelled through the microbial food web. All this processes have been poorly documented and the contribution of the phytoplankton cell death to the release of PDOC has not been yet explored in natural communities. The goal of this PhD Thesis is to provide quantitative information on phytoplankton and bacteria cell death in natural communities and to document the fraction of DOC released by phytoplankton (PDOC) under contrasting natural conditions. The exploration of the relationships between the phytoplankton cell mortality, DOC released by phytoplankton (PDOC) and microbial survival would contribute to better understand the path of carbon from photosynthesis to heterotrophic bacteria by cell death processes. Contrasting environmental conditions and communities from different oceanic regions including the Mediterranean Sea, Arctic, Antarctic and Atlantic oceans were studied. Evaluations of the in situ health status of the natural phytoplanktonic communities and bacteria were analyzed by testing the cell membrane permeability; a property that define cell death in cell biology. The total primary production, and the DOC production by phytoplankton were quantified to explore its dynamic with regard to the variability in phytoplankton cell mortality. The bacterial cell survival was also assessed under the same contrasting conditions mediating by the quantification of percentage of living heterotrophic bacteria. The proportion of dead of phytoplankton cells from the diverse phytoplankton populations encountered in the different communities, were related to environmental conditions as water temperature and nutrients availability, and helped to identify their competitive success. Consistent proportions of dead natural phytoplanktonic cells were found during this study that could represent in average about half of the total (40.5 %) phytoplankton abundance. Phytoplankton mortality constitutes a major process implicated in the production of dissolved organic carbon, as the percentage of phytoplankton dead cells explained the 41.4 % of the percentage of released production (PDOC) relative to total primary production. The large production of PDOC observed here, represented in average the half of the total primary production (54.4%) and supported, at the oligotrophic NE Atlantic Ocean, a higher bacterial viability.