Membrane Homeostasis upon Nutrient (C, N, P) Limitation
Natural environments are dynamic systems where organisms have to constantly acclimate to fluctuations in external conditions, including the bioavailability of essential nutrients carbon (C), nitrogen (N), and phosphorus (P). Membrane lipid plasticity plays an important role to adjust to these environmental challenges by either reducing the cellular need of these macronutrients or to help protect the cell and keep it viable during a prolonged state of reduced energy supply. When P limited, many organisms are able to replace their phospholipids with non-phosphorus containing glycolipids or aminolipids, liberating P for other cellular processes. Under N depletion, a common stress response is the increased production of triacylglycerol (TAG) lipids that serve as energy and carbon storage until nutrients become available again. During severe C starvation, the cell switches to survival mode and membrane lipids are remodeled to conserve energy and stabilize the cell against external stressors, but are also degraded and serve as an endogenous carbon and energy supply. These homeostatic adjustments are found among all domains of life with different specificities and play decisive roles during natural selection of populations in marine and terrestrial ecosystems.
This work was supported in part by the Central Research Development Fund of the University of Bremen, Germany.
- Abida H, Dolch L-J, Meï C, Villanova V, Conte M, Block MA, Finazzi G, Bastien O, Tirichine L, Bowler C, Rébeillé F, Petroutsos D, Jouhet J, Maréchal E (2014) Membrane glycerolipid remodeling triggered by nitrogen and phosphorus starvation in Phaeodactylum tricornutum. Plant Physiol 167:118–136PubMedPubMedCentralCrossRefGoogle Scholar
- Aguilar-López JL, Funes S (2018) Autophagy in stationary phase of growth. In: Geiger O (ed) Biogenesis of fatty acids, lipids and membranes, Handbook of hydrocarbon and lipid microbiology. Springer Nature Switzerland AG, pp 1–18Google Scholar
- Dowhan W, Bogdanov M, Mileykovskaya E (2016) Functional roles of lipids in membranes. In: Ridgway ND, McLeod RS (eds) Biochemistry of lipids, lipoproteins and membranes. Elsevier, Boston, pp 1–40Google Scholar
- Houser JR, Barnhart C, Boutz DR, Carroll SM, Dasgupta A, Michener JK, Needham BD, Papoulas O, Sridhara V, Sydykova DK, Marx CJ, Trent MS, Barrick JE, Marcotte EM, Wilke CO (2015) Controlled measurement and comparative analysis of cellular components in E. coli reveals broad regulatory changes in response to glucose starvation. PLoS Comput Biol 11:e1004400PubMedPubMedCentralCrossRefGoogle Scholar
- López-Lara IM, Gao J-L, Soto MJ, Solares-Pérez A, Weissenmayer B, Sohlenkamp C, Verroios GP, Thomas-Oates J, Geiger O (2005) Phosphorus-free membrane lipids of Sinorhizobium meliloti are not required for the symbiosis with Alfalfa but contribute to increased cell yields under phosphorus-limiting conditions of growth. Mol Plant Microbe Interact 18:973–982PubMedPubMedCentralCrossRefGoogle Scholar
- Meador TB, Gagen EJ, Loscar ME, Goldhammer T, Yoshinaga MY, Wendt J, Thomm M, Hinrichs K-U (2014) Thermococcus kodakarensis modulates its polar membrane lipids and elemental composition according to growth stage and phosphate availability. Front Microbiol 5:10PubMedPubMedCentralCrossRefGoogle Scholar
- Moore CM, Mills MM, Arrigo KR, Berman-Frank I, Bopp L, Boyd PW, Galbraith ED, Geider RJ, Guieu C, Jaccard SL, Jickells TD, La Roche J, Lenton TM, Mahowald NM, Maranon E, Marinov I, Moore JK, Nakatsuka T, Oschlies A, Saito MA, Thingstad TF, Tsuda A, Ulloa O (2013) Processes and patterns of oceanic nutrient limitation. Nat Geosci 6:701–710CrossRefGoogle Scholar
- Popko J, Herrfurth C, Feussner K, Ischebeck T, Iven T, Haslam R, Hamilton M, Sayanova O, Napier J, Khozin-Goldberg I, Feussner I (2016) Metabolome analysis reveals betaine lipids as major source for triglyceride formation, and the accumulation of sedoheptulose during nitrogen-starvation of Phaeodactylum tricornutum. PLoS One 11:e0164673PubMedPubMedCentralCrossRefGoogle Scholar
- Sebastian M, Smith AF, González JM, Fredricks HF, Van Mooy B, Koblížek M, Brandsma J, Koster G, Mestre M, Mostajir B, Pitta P, Postle AD, Sánchez P, Gasol JM, Scanlan DJ, Chen Y (2016) Lipid remodelling is a widespread strategy in marine heterotrophic bacteria upon phosphorus deficiency. ISME J 10:968–978PubMedCrossRefGoogle Scholar
- Senik SV, Maloshenok LG, Kotlova ER, Shavarda AL, Moiseenko KV, Bruskin SA, Koroleva OV, Psurtseva NV (2015) Diacylglyceryltrimethylhomoserine content and gene expression changes triggered by phosphate deprivation in the mycelium of the basidomycete Flammulina velutipes. Phytochemistry 117:34–42PubMedCrossRefGoogle Scholar
- Yao M, Elling FJ, Jones C, Nomosatryo S, Long CP, Crowe SA, Antoniewicz MR, Hinrichs K-U, Maresca JA (2015) Heterotrophic bacteria from an extremely phosphate-poor lake have conditionally reduced phosphorus demand and utilize diverse sources of phosphorus. Environ Microbiol 18:656–667PubMedPubMedCentralCrossRefGoogle Scholar
- Yoon K, Han D, Li Y, Sommerfeld M, Hu Q (2012) Phospholipid: diacylglycerol acyltransferase is a multifunctional enzyme involved in membrane lipid turnover and degradation while synthesizing triacylglycerol in the unicellular green microalga Chlamydomonas reinhardtii. Plant Cell 24:3708–3724PubMedPubMedCentralCrossRefGoogle Scholar