Interspecific variability in phosphorus‐induced lipid remodelling among marine eukaryotic phytoplankton

Abstract

The response of marine microalgal lipids to phosphorus is of central importance in phytoplankton ecology but remains poorly understood. We determined how taxonomically diverse microalgal species remodelled their lipid class profile in response to phosphorus availability and whether these changes coincided with those already known to occur in land plants and in the limited number of phytoplankton species for which data are available. The complete lipid class profile and specific lipid ratios influenced by phosphorus availability were quantified in two green microalgae and seven Chromalveolates exposed to phosphorus repletion, deprivation and replenishment. Lipid class cell quota changes in the two green microalgae resembled the currently described pattern of betaine lipids substituting for phospholipids under phosphorus depletion, whereas only two of the studied Chromalveolates showed this pattern. Sulpholipids counterbalanced phosphatidylglycerol only in Picochlorum atomus. In all other species, both lipids decreased simultaneously under phosphorus deprivation, although sulpholipids declined more slowly. Phosphorus deprivation always induced a decrease in digalactosyl-diacylglycerol. However, the ratio of digalactosyl-diacylglycerol to total phospholipids increased in eight species and remained unchanged in Isochrysis galbana. Marine phytoplankton seems to have evolved a diversified mechanism for remodelling its lipid class profile under the influence of phosphorus, with cryptophytes and particularly haptophytes exhibiting previously unobserved lipid responses to phosphorus.

Mechanisms of Phosphorus Acquisition and Lipid Class Remodeling under P Limitation in a Marine Microalga

“…This phenomenon of BL replacing PC under low P was shown to be common in freshwater and marine algae (Khozin-Goldberg and Cohen, 2006;Van Mooy et al, 2009;Martin et al, 2011;Iwai et al, 2015;Cañavate et al, 2017b). Recent studies comparing lipid class and P-uptake profiles of eight algae at low P i showed replacement of phospholipid by BL with concomitant high P uptake in the green alga Tetraselmis suesica and the stramenopiles P. tricornutum, N. gaditana, and P. atomus (Cañavate et al, 2017a(Cañavate et al, , 2017b. Phospholipid replacement and high P uptake under P stress indicate that these algae have a mechanism vital in temporal P limitation.…”

“…Low P content triggering TAG increase also is seen in the model algae C. reinhardtii and P. tricornutum, additionally replacing extraplastidial phosphatidylcholine (PC) by taxonomically specific betaine lipid (BL) classes such as diacylglyceroltrimethylhomoserine (DGTS; Iwai et al, 2014;Abida et al, 2015). This phenomenon of BL replacing PC under low P was shown to be common in freshwater and marine algae (Khozin-Goldberg and Cohen, 2006;Van Mooy et al, 2009;Martin et al, 2011;Iwai et al, 2015;Cañavate et al, 2017b). Recent studies comparing lipid class and P-uptake profiles of eight algae at low P i showed replacement of phospholipid by BL with concomitant high P uptake in the green alga Tetraselmis suesica and the stramenopiles P. tricornutum, N. gaditana, and P. atomus (Cañavate et al, 2017a(Cañavate et al, , 2017b.…”

“…in the form of triacylglycerols [TAGs]). To cope with P limitation, the interplay of P recycling and changes in lipid classes is observed in the open sea and in culture studies of several stramenopiles and green algae (Van Mooy et al, 2009;Martin et al, 2011;Cañavate et al, 2017b). These studies showed a taxonomically diverse lipid response under P stress with unresolved questions related to the diversified mechanism behind the lipid responses.…”

“…These studies showed a taxonomically diverse lipid response under P stress with unresolved questions related to the diversified mechanism behind the lipid responses. So far, only cursory insights into the lipidremodeling process have been provided by either transcriptomic or lipidomic studies on P limitation (Riekhof et al, 2005;Cruz de Carvalho et al, 2016;Shemi et al, 2016;Cañavate et al, 2017b). To capture the taxonomically diverse response and niche partitioning, studies include ecological successful algae, such as Emiliania huxleyi and Thalassiosira pseudonana (Lessard et al, 2005;Van Mooy et al, 2009), and algae featuring high resilience and lipid content during low P, like Phaeodactylum tricornutum and Nannochloropsis spp.…”

“…have been shown to accumulate TAGs, increasing their lipid content up to 50% of cell dry weight (Rodolfi et al, 2009;Mayers et al, 2014;Cañavate et al, 2017b). Low P content triggering TAG increase also is seen in the model algae C. reinhardtii and P. tricornutum, additionally replacing extraplastidial phosphatidylcholine (PC) by taxonomically specific betaine lipid (BL) classes such as diacylglyceroltrimethylhomoserine (DGTS; Iwai et al, 2014;Abida et al, 2015).…”