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Resource limitation and the biochemical composition of marine phytoplankton
Grosse, J. (2016). Resource limitation and the biochemical composition of marine phytoplankton. PhD Thesis. UvA: Amsterdam. ISBN 978-94-91407-37-6. hdl.handle.net/11245/1.541502

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Abstract
    Over the past few decades nutrient inputs into the North Sea have changedsubstantially. Anthropogenic activities altered riverine nutrient loads, whichconsequently caused shifts in the available nutrient ratios of nitrogen tophosphorus (N:P). Phytoplankton at the base of the food web is first and foremostaffected by these changes and responds by altering its biomolecule composition.The main biomolecules in phytoplankton like carbohydrates, amino acids, fattyacids and RNA/DNA bases have different C:N:P requirements for the synthesis,and phytoplankton is generally flexible in adjusting its metabolism leading forinstance to the synthesis of more only C-containing storage compounds whennutrients are limiting. In this thesis I aimed to study the effects of different nutrientlimitations on the dynamics of biomolecule synthesis and composition in NorthSea phytoplankton. Furthermore, the consequences for phytoplankton food qualitywere evaluated and a first study was conducted to determine how herbivorouszooplankton copes with low food quality. Stable isotopes were used as deliberatelyadded tracer (13C) and bulk and compound specific isotope analysis present thefoundation of this work.Incorporation of 13C into biomass is frequently used to estimate primaryproduction. Although these bulk measurements offer valuable information, theylack information about the intracellular fate of this fixed carbon. The methods todetermine 13C incorporation into different compounds (amino acids, fatty acids,carbohydrates) were already available but had not been combined to evaluate theirpotential as a tool to assemble a biomolecule based carbon budget. In Chapter 2,established methods in gas chromatography/isotope ratio mass spectrometry(GC/C-IRMS) and recently developed methods in liquid chromatography/IRMS(LC/IRMS) were therefore combined to trace 13C into carbohydrates, amino acidsand fatty acids in phytoplankton, and compare their production to total carbonfixation rates. It was found that the carbon fixation into those three fractionsaccounted for the majority of bulk carbon fixation and offers a way to investigateeffects of nutrient limitation on the physiological state of a phytoplanktoncommunity.SUMMARY186Both N- and P-limitation affect phytoplankton communities in the North Seaand translate into dynamic changes in biomolecule pools. In order to understandthe effects of different resource limitations on field populations, seasonal andspatial dynamics of amino acids, fatty acids and carbohydrates (Chapter 3) wereinvestigated. Nutrient limitation and season had large effects on composition andbiosynthesis rates of all biomolecule classes, but could not be used alone todetermine the prevalent limiting nutrient. However, short-term nutrient additionexperiments were capable of identifying the limiting nutrients. The addition of thegrowth-limiting nutrient increased amino acid synthesis while storage compoundsynthesis decreased. This response was much slower in P-limited than in N-limitedcommunities, likely because of the necessary preceding synthesis of ribosomes,suggesting that despite similar responses the regulatory mechanisms differed.Regulation of individual amino acids under N- and P-limitation differed alsofurther supporting the existence of different regulatory mechanisms. (Chapter 4).Under N-limitation the synthesis of essential amino acids was substantially slowerthan that of non-essential amino acids, a trend that was reversed immediately afterN-addition. On the other hand, P-limited communities decreased the synthesis ofall amino acids evenly. For fatty acid groups responses to N- and P-limitation werealike, showing a shift from structural to storage fatty acids, with a concurrentdecrease in the synthesis of poly-unsaturated fatty acids. Reversed effects in fattyacid synthesis after N or P addition were delayed and only apparent after 72 h. Bythen they had also translated into fatty acid concentrations in the phytoplanktonbiomass. This emphasizes the different qualitative and quantitative regulations ofamino acids and fatty acids synthesis under nutrient scarcity and also demonstratesthe far-reaching consequences for the phytoplankton’s nutritional value and foodweb structure as mainly essential amino acids and fatty acids for higher trophiclevels were affected by nutrient limitation.Nutrient availability limits phytoplankton growth, either because N or Pconcentrations are too low, or because the resulting N:P ratios are outside theoptimal range. Phytoplankton communities from the North Sea were cultured inchemostats under different nutrient loads and N:P ratios in order to verify fieldfindings and get a better picture of the N:P ratio dependency of biomoleculesynthesis (Chapter 5). Simple communities containing green algae, diatoms andcyanobacteria developed in the cultures. While green algae provided highestbiomass under light and P-limitation, diatoms dominated under both N- and Plimitation.Cyanobacteria had the biggest advantage under low N-concentrations.SUMMARY18 7Synthesis patterns of biomolecules agreed well with field findings. Amino acidcontribution was lowest under N-limitation, higher under P-limitation and highestwhen light was the limiting factor. The contribution of individual amino acids tototal amino acid concentrations was well conserved over the wide range of N:Pratios and between different phytoplankton communities. The decreasedtransformation of essential from non-essential amino acids under low N:P ratioswas also apparent in the cultures. Furthermore, this chapter shows that differentphytoplankton groups are capable of adapting their biomolecule composition todifferent extends when experiencing shifts in nutrient availability, which will helpto explain competitive advantages in mixed phytoplankton communities.The high variability in biomolecule composition of phytoplankton and thesubsequent lower food quality of nutrient limited phytoplankton will affect highertrophic levels, which are less flexible in adapting their biomolecule composition.The adaptation mechanisms of herbivorous zooplankton (copepods) to low qualityfood of N- and P-limited food algae were investigated in Chapter 6. Interestingly,the physiological adaptation as well as the limiting biomolecules differed betweentreatments fed with N- or P-limited food algae. Copepods responded to P-limitedfood by increasing their grazing rate, which in turn was regulated by thedigestibility of food particles. However, little regulation of the metabolism ofbiomolecules was apparent during P-limitation. When exposed to N-limited foodparticles copepod grazing rates increased only slightly. But higher retention ofamino acids and nitrogen in general were observed, which apparently also led toan increased need for structural poly-unsaturated fatty acids. Consequently, thesecopepods were co-limited by two essential biomolecule groups, namely essentialamino acids and fatty acids. Therefore, the different forms of nutrient limitationled to similar negative impacts on growth but triggered contrasting physiologicalresponses and potentially affect species dynamics and trophic transfer efficiencies.In conclusion, phytoplankton communities are flexible in adapting theirbiomolecule composition and biosynthesis to prevailing nutrient availabilities.Species and nutrient specific mechanisms are contributing factors and quickadaptations occur when nutrient situations change. The consequent lack ofessential compounds translates up the food chain forcing consumer organisms toadjust their feeding patterns and physiological processes.

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