Arginine-fed cultures generates triacylglycerol by triggering nitrogen starvation responses during robust growth in Chlamydomonas

Jacob Munz, Yuan Xiong, Jaoon Young Hwan Kim, Young Joon Sung, Seungbeom Seo, Ran Ha Hong, Thamali Kariyawasam, Nolan Shelley, Jenny Lee, Sang Jun Sim, Eon Seon Jin, Jae Hyeok Lee

Research output: Contribution to journalArticle

Abstract

Under nitrogen (N) starvation, certain microalgae increase carbon storage in the form of lipid droplets while also downregulating photosynthesis and eventually terminating growth. To improve lipid yield, we asked whether lipid droplets and N starvation responses can be induced without limiting growth or photosynthesis. In the chlorophyte Chlamydomonas reinhardtii, N starvation induces gametogenesis alongside lipid droplet accumulation, and gametogenesis has been observed in arginine-fed cultures wherein the arginine was provided as the sole N source. We therefore assessed whether arginine-fed cultures displayed N starvation responses other than gametogenesis in mixo- and phototrophic conditions, representing two primary modes of nutrition that may affect N starvation responses. We showed that arginine-fed cultures using two lab strains of C. reinhardtii supported normal mixotrophic growth, constitutively turned on N starvation-induced genes at the equivalent level to N-starved cells, and increased the triacylglycerol content of total fatty acids by 125–400% relative to ammonium-fed cultures. The lipid profile of triacylglycerol in these arginine-fed mixotrophic cultures exhibited 3 to 5.5-fold enrichment of saturated and monounsaturated fatty acids, a preferred characteristic of biodiesel precursors. Arginine-fed phototrophic cultures likewise turned on N starvation-induced genes, accumulated lipid droplets, and led to a 50% reduced growth rate per day while reaching a 3 to 6.5-fold more cell density at the stationary phase relative to ammonium-fed cultures. To test the applicability of our result to algae outside the green lineage, we conducted similar experiments with the diatom Phaeodactylum tricornutum, which also accumulated 2 to 7-fold more neutral lipids in arginine-fed phototrophic cultures without growth impairment relative to nitrate-fed cultures. We document a system wherein N starvation responses are induced without compromising photosynthesis or growth, thereby suited to the production of valuable chemicals and biofuel precursors without requiring stressors in microalgae.

Original languageEnglish
Article number101782
JournalAlgal Research
Volume46
DOIs
Publication statusPublished - 2020 Mar

Fingerprint

Chlamydomonas
arginine
starvation
triacylglycerols
nitrogen
droplets
gametogenesis
lipids
Chlamydomonas reinhardtii
photosynthesis
microalgae
Phaeodactylum tricornutum
Bacillariophyceae
biodiesel
monounsaturated fatty acids
biofuels
carbon sequestration
Chlorophyta
saturated fatty acids
genes

Keywords

  • Arginine-fed culture
  • Chlamydomonas
  • Lipid droplet production
  • Nitrogen signaling
  • Nitrogen starvation
  • Phaeodactylum

ASJC Scopus subject areas

  • Agronomy and Crop Science

Cite this

Arginine-fed cultures generates triacylglycerol by triggering nitrogen starvation responses during robust growth in Chlamydomonas. / Munz, Jacob; Xiong, Yuan; Kim, Jaoon Young Hwan; Sung, Young Joon; Seo, Seungbeom; Hong, Ran Ha; Kariyawasam, Thamali; Shelley, Nolan; Lee, Jenny; Sim, Sang Jun; Jin, Eon Seon; Lee, Jae Hyeok.

In: Algal Research, Vol. 46, 101782, 03.2020.

Research output: Contribution to journalArticle

Munz, J, Xiong, Y, Kim, JYH, Sung, YJ, Seo, S, Hong, RH, Kariyawasam, T, Shelley, N, Lee, J, Sim, SJ, Jin, ES & Lee, JH 2020, 'Arginine-fed cultures generates triacylglycerol by triggering nitrogen starvation responses during robust growth in Chlamydomonas', Algal Research, vol. 46, 101782. https://doi.org/10.1016/j.algal.2019.101782
Munz, Jacob ; Xiong, Yuan ; Kim, Jaoon Young Hwan ; Sung, Young Joon ; Seo, Seungbeom ; Hong, Ran Ha ; Kariyawasam, Thamali ; Shelley, Nolan ; Lee, Jenny ; Sim, Sang Jun ; Jin, Eon Seon ; Lee, Jae Hyeok. / Arginine-fed cultures generates triacylglycerol by triggering nitrogen starvation responses during robust growth in Chlamydomonas. In: Algal Research. 2020 ; Vol. 46.
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AU - Seo, Seungbeom

AU - Hong, Ran Ha

AU - Kariyawasam, Thamali

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AB - Under nitrogen (N) starvation, certain microalgae increase carbon storage in the form of lipid droplets while also downregulating photosynthesis and eventually terminating growth. To improve lipid yield, we asked whether lipid droplets and N starvation responses can be induced without limiting growth or photosynthesis. In the chlorophyte Chlamydomonas reinhardtii, N starvation induces gametogenesis alongside lipid droplet accumulation, and gametogenesis has been observed in arginine-fed cultures wherein the arginine was provided as the sole N source. We therefore assessed whether arginine-fed cultures displayed N starvation responses other than gametogenesis in mixo- and phototrophic conditions, representing two primary modes of nutrition that may affect N starvation responses. We showed that arginine-fed cultures using two lab strains of C. reinhardtii supported normal mixotrophic growth, constitutively turned on N starvation-induced genes at the equivalent level to N-starved cells, and increased the triacylglycerol content of total fatty acids by 125–400% relative to ammonium-fed cultures. The lipid profile of triacylglycerol in these arginine-fed mixotrophic cultures exhibited 3 to 5.5-fold enrichment of saturated and monounsaturated fatty acids, a preferred characteristic of biodiesel precursors. Arginine-fed phototrophic cultures likewise turned on N starvation-induced genes, accumulated lipid droplets, and led to a 50% reduced growth rate per day while reaching a 3 to 6.5-fold more cell density at the stationary phase relative to ammonium-fed cultures. To test the applicability of our result to algae outside the green lineage, we conducted similar experiments with the diatom Phaeodactylum tricornutum, which also accumulated 2 to 7-fold more neutral lipids in arginine-fed phototrophic cultures without growth impairment relative to nitrate-fed cultures. We document a system wherein N starvation responses are induced without compromising photosynthesis or growth, thereby suited to the production of valuable chemicals and biofuel precursors without requiring stressors in microalgae.

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