Environmental factors influencing phytoplankton productivity in the context of climate change

Anthropogenic activities are increasing CO2 in the atmosphere and in the ocean, raising global temperatures and lowering the oceanic pH. Since phytoplankton perform nearly half of the global carbon fixation via photosynthesis, and control the biological sequestration of CO2 in the ocean, their response to increasing CO2/decreasing pH is a key to the effect of “ocean acidification” on marine ecosystems. Previous work on this question has shown contradictory results, possibly as a consequence of separate and opposite effects of environmental parameters on photosynthesis and respiration. The primary goal of this thesis was therefore to disentangle these effects, and determine how they translate into changes in productivity. To do so, I conducted a combination of laboratory experiments with model organisms, and field research on natural phytoplankton communities.

Effects of pH and pCO2 changes on photosynthesis and respiration were investigated with the diatom Thalassiosira weissflogii, using H218O as a tracer. The effects at saturating light were examined in long term incubations (several hours) using an isotope ratio mass spectrometer. To expand the matrix of conditions, short term experiments were also performed, under different light intensities, with a membrane inlet mass spectrometer (MIMS). The MIMS allowed real time measurements of photosynthesis and respiration. Under all light conditions, no effects of either pH or pCO 2 were found on photosynthesis or respiration, despite an acclimation of the carbon concentrating mechanism (CCM) with pCO2, measured via the activity of carbonic anhydrase, one of the CCM enzyme. Calculations using Rubisco selectivity and half-saturation constant, predicted that, under nutrient replete conditions, a doubling of CO2 would result in less than ∼3% change on photosynthesis in T. weissflogii, and at most ∼8.5% in other diatoms. These results are due to the energetic efficiency of the CCM in diatoms and would vary for other groups of phytoplankton with different CCM.

During a field campaign near the Western Antarctic Peninsula (WAP), we analyzed some of the metabolic characteristics of the natural community responsible δfor the high productivity of the region, despite cold temperatures. Three different techniques were used to measure productivity: 1) 14C incubations, measuring fixation of CO2 into the biomass during the dark reactions of photosynthesis, 2) H218O incubations, measuring the splitting of water during the light reaction of photosynthesis and 3) in situ measurements of O2 /Ar and triple oxygen isotope, which allowed derivation of time-integrated ratios of Net/Gross production. The spring bloom represented more than half of the production of the growing season (spring-summer). During this event, the net-to-gross production ratios were ∼60%, among the highest ever reported. This study showed that these high ratios were partly due to low daylight respiration and low heterotrophic respiration. Additional laboratory experiments with the polar diatom Fragilariopsis cyclindrus, demonstrated an important level of cyclic electron flow (CEF) in this organism. CEF is an alternative pathway that allow the cell to produce energy from light, in the form of adenosine triphosphate (ATP), independently of mitochondrial respiration. As such, it could also contribute to the high productivity in the field.

To follow-up on the field findings, diel cycle experiments were performed on the psychrophilic diatom Proboscia alata. This organism (obtained from A. Marchetti) was isolated in the WAP. Measurements of total protein, particulate organic carbon and nitrogen were taken throughout the day. They revealed a synthesis of proteins in the morning, likely from recycling of other cellular molecules (i.e. lipids and ribosomes), and an increase of the biomass around midday. Carbon fixation was assessed using time course incubations of 20, 40 or 60 min, and net and gross photosynthesis were determined using H218O incubations. A comparison of 14C time course and H218O revealed a shift between the morning and afternoon from low to high respiration and recycling. These results provide new insights into the mechanisms used by this psychrophilic organism for energy balance and carbon storage during a diel cycle.

Goldman J. A. L., 2016. Environmental factors influencing phytoplankton productivity in the context of climate change. Ph.D. thesis, Princeton University, 163 p. Thesis (restricted access).

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