Photosynthetic energy conversion under extreme conditions—I: important role of lipids as structural modulators and energy sink under N-limited growth in Antarctic sea ice diatoms

Abstract

The availability of dissolved nutrients such as nitrate under extreme low temperatures is a strong determinant in the development and growth of ice diatoms. Consequently we investigated regulation of photosynthesis in a mixed culture of three diatom species, which grew in chemostats at À1 C, 15 mmol photons m À2 s À1 under N-limitation. When nitrogen is limiting, pigment-protein complexes are one of the most affected structures under low-light conditions. The loss of integral polar thylakoid components destabilized the bilayer structure of the membrane with consequences for lipid composition and the degree of fatty acid desaturation. N-Limitation caused a decrease in monogalactosydiacylglycerol (MGDG) and a simultaneous increase in bilayer forming digalactosyldiacylglycerol (DGDG). Their ratio MGDG:DGDG decreased from 3.4AE 0.1 to 1.1 AE 0.4, while 20:5 n-3 fatty acids of chloroplast related phospholipid classes such as phosphatidylglycerol (PG) increased under N-limitation. These data reveal that lipids are important components, required to sustain membrane structure under a deficiency of integral membrane bound proteins and pigments. Nonetheless, energy conversion at photosystem II is still affected by N-limitation despite this structural regulation. Photosynthetic quantum yield (F v /F m ) and electron transport rates decreased under N-limitation caused by an increasing amount of electron acceptors (second stable electron acceptor=Q B ) which had slower reoxidation kinetics. The energy surplus under these conditions is stored in triacylglycerols, the main energy sink in Antarctic sea ice diatoms under N-limitation. #

The Response of Diatom Central Carbon Metabolism to Nitrogen Starvation Is Different from That of Green Algae and Higher Plants

“…There are reports of increased lipid and fatty acid production in diatoms and many other microalgae under nitrogen-starved conditions (Collyer and Fogg, 1955;Mock and Kroon, 2002;Palmucci et al, 2011). Although we found no changes in the abundance of proteins associated with this pathway and there were few changes in transcript levels , these studies provide an alternative hypothesis to explain the responses to nitrogen starvation seen here.…”

“…Therefore, it is not surprising that five proteins involved in the synthesis of chlorophyll and its precursors decreased by 1.5-to 2.5-fold in abundance under nitrogen starvation (Table II), including a geranylgeranyl reductase (ProtID 10234) that has been shown to catalyze a critical step in chlorophyll synthesis in vascular plants (Tanaka et al, 1999). Transcript levels of six genes involved in chlorophyll biosynthesis (ProtIDs 32201, 26573, 32431, 5077, 262279, and 31012) were also found to decrease , and reduced chlorophyll content (Mock and Kroon, 2002) and chlorophyll degradation (D. Franklin, personal communication) have previously been measured in T. pseudonana under nitrogen starvation.…”

Southern Ocean phytoplankton physiology in a changing climate

“…The cellular energy partitioning and macromolecular composition (lipids: proteins: carbohydrates) will determine the nutritional value of the phytoplankton and ultimately, through trophic transfer, the productivity of the ecosystem. Under sea ice conditions (sub-zero temperature, low light and high salinity), microalgae preferentially produce lipid macromolecules for energy storage (Mock and Kroon 2002;Sackett et al, 2013). Lipids are the most energy-rich macromolecules, with approximately double the caloric value of proteins and carbohydrates (Whyte, 1987).…”

“…Lipids are the most energy-rich macromolecules, with approximately double the caloric value of proteins and carbohydrates (Whyte, 1987). Organisms such as juvenile krill depend on these rich sources of lipids for growth and productivity, particularly during the long, winter months (Falk-Petersen et al, 1998;Mock and Kroon, 2002;Lee et al, 2008). However, with predicted reductions in the duration, extent and thickness of sea ice expected with future warming, the physico-chemical conditions that currently drive this large allocation of energy into lipids stores, may alter, causing a shift in cellular resource allocation.…”

Metatranscriptomes reveal functional variation in diatom communities from the Antarctic Peninsula

“…Particularly striking was the 5-10-fold enrichment of acetyl-CoA carboxylase (ACAC, Figure 4b), which catalyzes one of the initial steps in fatty acid biosynthesis. Diatoms accumulate lipids under nutrient-limited conditions (N, Si or Fe; Roessler, 1988;Mock and Kroon, 2002a;Allen et al, 2008), particularly relevant in light of enriched transport functions (see following section).…”