Daily changes in phytoplankton lipidomes reveal mechanisms of energy storage in the open ocean

Abstract

Sunlight is the dominant control on phytoplankton biosynthetic activity, and darkness deprives them of their primary external energy source. Changes in the biochemical composition of phytoplankton communities over diel light cycles and attendant consequences for carbon and energy flux in environments remain poorly elucidated. Here we use lipidomic data from the North Pacific subtropical gyre to show that biosynthesis of energy-rich triacylglycerols (TAGs) by eukaryotic nanophytoplankton during the day and their subsequent consumption at night drives a large and previously uncharacterized daily carbon cycle. Diel oscillations in TAG concentration comprise 23 ± 11% of primary production by eukaryotic nanophytoplankton representing a global flux of about 2.4 Pg C yr^-1. Metatranscriptomic analyses of genes required for TAG biosynthesis indicate that haptophytes and dinoflagellates are active members in TAG production. Estimates suggest that these organisms could contain as much as 40% more calories at sunset than at sunrise due to TAG production.

Fig. 1

Diel oscillation of lipid biomarkers. a Concentrations of storage lipids (TAGs), a class of structural membrane lipids from eukaryotic phytoplankton (DGCCs) and lipid-soluble electron transporters (UQs) over 8 day/night cycles at 15 m water depth in July and August 2015 at Station ALOHA. Values represent the average of environmental triplicates and error bars the standard deviation. b Time-of-day average of fold change relative to 06:00 h (local time) of TAG, DGCC and UQ concentrations. c Ratios of intact non-phosphorus membrane lipids (SQDG and BLs) to membrane phospholipids (PG, PE, and PC). Lipid ratios are based on known lipid substitutions in eukaryotic phytoplankton and cyanobacteria under nutrient limitation. d and e Time-of-day average of diacylglycerol acyltransferase 1 (DGAT1) and DGAT2 abundance, respectively, in major eukaryotic phytoplankton (* not including Dinophyceae (dinoflagellates), ** not including Bacillariophyta (diatoms)). Shaded areas around lines in b and c represent the standard deviation of averaged values for each time of day (n ≥ 6). Vertical gray shaded areas in each graph indicate night. TAG triacylglycerol; DGCC diacylglycerylcarboxy-N-hydroxymethyl-choline, UQ ubiquinone; SQDG sulfoquinovosyl diacylglycerol; PG phosphatidylglycerol; BL betaine lipid (sum of DGCC, diacylglyceryl trimethylhomoserine (DGTS), and diacylglyceryl hydroxymethyl-trimethyl-β-alanine (DGTA)); PC phosphatidylcholine; PE phosphatidylethanolamine

Fig. 2

Diel patterns in triacylglycerols at different water depths. a Concentrations of triacylglycerols (TAGs) for dusk (~06:00 h, local time) and dawn (~18:00 h) over 4 day/night cycles (gray areas in indicate night) in March 2016 at different water depths at Station ALOHA. b Time-of-day average of depth profiles of TAGs and derived production rates (mg TAG C m⁻³ d⁻¹) as well as primary production (PP, mg C m⁻³ d⁻¹). c TAG composition averaged for time of day at 5 and 150 m water depth. Bars in b and c are the mean ± SD (n ≥ 3)