Phosphorus and nitrogen starvation reveal life‐cycle specific responses in the metabolome of Emiliania huxleyi (Haptophyta)

Abstract

The coccolithophore Emiliania huxleyi is a microalga with biogeochemical and biotechnological relevance, due to its high abundance in the ocean and its ability to form intricate calcium carbonate structures. Depletion of macronutrients in oceanic waters is very common and will likely enhance with advancing climate change. We present the first comprehensive metabolome study analyzing the effect of phosphorus (P) and nitrogen (N) starvation on the diploid and haploid life‐cycle stage, applying various metabolome analysis methods to gain new insights in intracellular mechanisms to cope with nutrient starvation. P‐starvation led to an accumulation of many generic and especially N‐rich metabolites, including lipids, osmolytes, and pigments. This suggests that P‐starvation primarily arrests cell‐cycling due to lacking P for nucleic acid synthesis, but that enzymatic functionality is widely preserved. Also, the de‐epoxidation ratio of the xanthophyll cycle was upregulated in the diploid stage under P‐starvation, indicating increased nonphotochemical quenching, a response typically observed under high light stress. In contrast, N‐starvation resulted in a decrease of most central metabolites, also P‐containing ones, especially in the diploid stage, indicating that most enzymatic functionality ceased. The two investigated nutrient starvation conditions caused significantly different responses, contrary to previous assumptions derived from transcriptomic studies. Data highlight that instantaneous biochemical flux is a more dominant driver of the metabolome than the transcriptomically rearranged pathway patterns. Due to the fundamental nature of the observed responses it may be speculated that microalgae with similar nutrient requirements can cope better with P‐starvation than with N‐starvation.

Evidence for contrasting roles of dimethylsulfoniopropionate production in Emiliania huxleyi and Thalassiosira oceanica

“…One of the original hypotheses for the DMSP mechanism was that DMSP replaces nitrogen‐containing osmolytes under NO 3 − limitation (Andreae, ). Although E. huxleyi is known to produce several N‐containing osmolytes (Gebser & Pohnert, ; Wordenweber et al , ), we found no evidence to support this hypothesis. Intracellular DMSP concentrations in E. huxleyi did not increase under NO 3 − limitation, in fact concentrations decreased slightly (Fig.…”

“…Previous studies have demonstrated that growth at temperatures below the optimal growth temperature (T opt ) is metabolically balanced, with similar decreases in photosynthesis and respiration (Thomas et al, 2012;Baker et al, 2016;Barton et al, 2018). By contrast, growth at temperatures above T opt and under nutrient limitation (steadyor nonsteady-state) was linked to metabolic imbalances, in which photosynthesis and respiration are decoupled (Hockin et al, 2012;Baker et al, 2016;Wordenweber et al, 2018). The metabolic conditions of marine phytoplankton resulting from steady-state hyper-and hyposaline stresses are relatively unknown, as most previous studies have focused on euryhaline species or nonsteady-state responses to osmotic shock (Qasim et al, 1972;Macler, 1988;Jahnke & White, 2003;Bussard et al, 2017).…”

Phosphorus limitation and heat stress decrease calcification in <i>Emiliania huxleyi</i>

“…DIC limitation, however, was not the trigger for entering stationary phase as POC production continued for several days after cessation of cell division. Wördenweber et al (2017) have recently shown that although the cell cycle is arrested by P starvation, enzymatic functionality is widely preserved. P starvation blocks the synthesis of DNA and membrane phospholipids, necessary for cell replication, arresting the cells in the G1 (assimilation) phase of the cell cycle (Müller et al, 2008).…”

Bioengineering of Microalgae: Recent Advances, Perspectives, and Regulatory Challenges for Industrial Application

“…Frontiers in Bioengineering and Biotechnology | www.frontiersin.org (Guarnieri et al, 2011(Guarnieri et al, , 2013Sibi et al, 2014;Li et al, 2015b;Ouyang et al, 2015;Henard et al, 2017;Zuñiga et al, 2018;Mocsai et al, 2019) Chloroidium sp. Katz et al, 2007;Jia et al, 2009Jia et al, , 2016Gu et al, 2014;Ge et al, 2016;Lv et al, 2016;Zhao et al, 2016;Wei et al, 2017b;Wang et al, 2019d Emiliana (Benner et al, 2013;Rokitta et al, 2014;Hunter et al, 2015;McKew et al, 2015;Wördenweber et al, 2018) Fistulifera solaris (JPCC Wang et al, 2004;Tran et al, 2009;Peled et al, 2011;Gu et al, 2014;Recht et al, 2014;Su et al, 2014;Gao et al, 2016;Baumeister et al, (Chen et al, 2014;Ge et al, 2014;Jungandreas et al, 2014;Rosenwasser et al, 2014;Yang et al, 2014;Abida et al, 2015;Alipanah et al, 2015;Feng et al, 2015;Bai et al, 2016;…”