Phosphorus supply drives rapid turnover of membrane phospholipids in the diatom Thalassiosira pseudonana

Abstract

In low-phosphorus (P) marine systems, phytoplankton replace membrane phospholipids with nonphosphorus lipids, but it is not known how rapidly this substitution occurs. Here, when cells of the model diatom Thalassiosira pseudonana were transferred from P-replete medium to P-free medium, the phospholipid content of the cells rapidly declined within 48 h from 45±0.9 to 21±4.5% of the total membrane lipids; the difference was made up by non-phosphorus lipids. Conversely, when P-limited T. pseudonana were resupplied with P, cells reduced the percentage of their total membrane lipids contributed by a non-phosphorus lipid from 43 ± 1.5 to 7.3 ± 0.9% within 24 h, whereas the contribution by phospholipids rose from 2.2±0.1 to 44±3%. This dynamic phospholipid reservoir contained sufficient P to synthesize multiple haploid genomes, suggesting that phospholipid turnover could be an important P source for cells. Field observations of phytoplankton lipid content may thus reflect short-term changes in P supply and cellular physiology, rather than simply long-term adjustment to the environment. The ISME Journal ( Subject Category: geomicrobiology and microbial contributions to geochemical cycles Keywords: betaine lipids; DGCC; lipid substitution; non-phosphorus lipids; phosphatidylcholine; diatoms Phosphate is chronically scarce in oligotrophic oceans (Krom et al., 1991;Karl et al., 1997;Wu et al., 2000), and phytoplankton appear to posses highly effective physiological mechanisms to reduce their phosphorus (P) quota in these environments (Twining et al., 2010). For example, all phytoplankton groups examined to date, both in culture and in situ, substitute non-phosphorus (sulfur-and nitrogen-containing) lipids for phospholipids in their membranes under low-P conditions (Van Mooy et al., 2009). Such lipid substitution in bacteria (Minnikin et al., 1974;Benning et al., 1995) can take place within hours (Zavaleta-Pastor et al., 2010). However, it is not known how rapidly phytoplankton remodel their membranes, and whether field observations (Van Mooy et al., 2009) reflect longterm adjustment to the environment or an immediate cellular response to low-P conditions.The diatom Thalassiosira pseudonana and other eukaryotic phytoplankton contain the phospholipids phosphatidylcholine (PC), phosphatidylglycerol (PG) and phosphatidylethanolamine (PE). Under low-P conditions, T. pseudonana substitutes PC with the betaine lipid diacylglycerylcarboxyhydroxymethylcholine (DGCC), and PG with the sulfolipid sulfoquinovosyldiacylglycerol (SQDG) (Van Mooy et al., 2009).Two culture experiments were conducted to test how rapidly lipid substitution occurs in T. pseudonana upon changes in phosphate concentration. In the first experiment, T. pseudonana CCMP1335 was grown in P-replete medium (in triplicate, Supplementary Methods) until early log-phase. Cells were then gently filtered onto 0.2 mm polycarbonate membranes and resuspended in either phosphatefree (ÀP) or phosphate-replete ( þ P, 36 mmol l À1 phosphate) medium. However, as the ÀP cultures con...

Gradients in intact polar diacylglycerolipids across the Mediterranean Sea are related to phosphate availability

“…With less phospholipids in the membrane, the balance of IP-DAGs is expected to come from glycolipids and betaine lipids. The particular substitutions that have been observed in cultures are SQDG substituting for PG, and betaine lipids substituting for PC (Benning et al, 1993(Benning et al, , 1995Martin et al, 2011;Van Mooy et al, 2006, 2009. Across the Mediterranean, the ratios of SQDG:PG and betaine lipids:PC were both highest in the east.…”

“…The variation of IP-DAGs with different microbial groups has been well studied in cultures (Oliver and Colwell, 1973;Guschina and Harwood, 2006;Kato et al, 1996;Van Mooy et al, 2006), and some work has also been done measuring the diversity of IP-DAGs in microbial groups from environmental samples (Popendorf et al, 2011). The physiological response has also been well studied in monocultures (Benning et al, 1993(Benning et al, , 1995Martin et al, 2011;Van Mooy et al, 2009), however it remains to be shown whether the influence of changes in physiology can be detected in changes in IP-DAGs in a natural, mixed planktonic community.…”

“…Different groups of plankton contain different arrays of IP-DAG headgroups (Popendorf et al, 2011;Van Mooy et al, 2006), such that a community dominated by phytoplankton could be expected to have a different total IP-DAG composition than a community dominated by heterotrophic bacteria. Some types of plankton have been shown to be capable of substituting non-phosphorus lipids for phospholipids in conditions of phosphorus stress (Benning et al, 1993(Benning et al, , 1995Martin et al, 2011;Minnikin et al, 1974;Van Mooy et al, 2009), adjusting the composition of their membrane as a physiological response to nutrient conditions. This physiological response has been demonstrated in culture, but has not previously been observed in a natural, mixed planktonic community.…”

Effects of prolonged darkness and temperature on the lipid metabolism in the benthic diatom Navicula perminuta from the Arctic Adventfjorden, Svalbard

“…3). Those peaks could potentially refer to diphosphatidylglycerol, phosphatic acid, the unidentified sulfur-containing lipids or DGCC (Kates and Volcani 1966;Opute 1974b;Martin et al 2011).…”

Accumulation and enhanced cycling of polyphosphate by Sargasso Sea plankton in response to low phosphorus

“…This modulation of P-containing biochemicals results in basin-scale relationships between P availability and biomass carbon-to-phosphorus (C:P) ratios (13). Presently, the only class of molecules known to consistently contribute to these gradients in cellular P are lipids because P stress in phytoplankton triggers substitution of non-P-membrane lipids for phospholipids, such as the sulfolipid sulfoquinovosyldiacylglycerol (SQDG) for the phospholipid phosphatidylglycerol (PG) (1,14). However, lipid substitution alone probably cannot account for the full range of C:P observed in the ocean, and yet an understanding of other biochemical drivers of the C:P gradient remains elusive.…”