Nitric Oxide Mediates Nitrite-Sensing and Acclimation and Triggers a Remodeling of Lipids

Abstract

Nitric oxide (NO) is an intermediate of the nitrogen cycle, an industrial pollutant, and a marker of climate change. NO also acts as a gaseous transmitter in a variety of biological processes. The impact of environmental NO needs to be addressed. In diatoms, a dominant phylum in phytoplankton, NO was reported to mediate programmed cell death in response to diatom-derived polyunsaturated aldehydes. Here, using the Pt1 strain, 2E,4E-decadienal supplied in the micromolar concentration range led to a nonspecific cell toxicity. We reexamined NO biosynthesis and response in NO inhibits cell growth and triggers triacylglycerol (TAG) accumulation. Feeding experiments indicate that NO is not produced from Arg but via conversion of nitrite by the nitrate reductase. Genome-wide transcriptional analysis shows that NO up-regulates the expression of the plastid nitrite reductase and genes involved in the subsequent incorporation of ammonium into amino acids, via both Gln synthesis and Orn-urea pathway. The phosphopyruvate dehydrogenase complex is also up-regulated, leading to the production of acetyl-CoA, which can feed TAG accumulation upon exposure to NO. Transcriptional reprogramming leading to higher TAG content is balanced with a decrease of monogalactosyldiacylglycerol (MGDG) in the plastid via posttranslational inhibition of MGDG synthase enzymatic activity by NO. Intracellular and transient NO emission acts therefore at the basis of a nitrite-sensing and acclimating system, whereas a long exposure to NO can additionally induce a redirection of carbon to neutral lipids and a stress response.

Algal photosynthesis converts nitric oxide into nitrous oxide

“…NO is a known signal molecule involved in various regulatory mechanisms in all living organisms. In microalgae, NO is involved in the regulation of the nitrate and nitrite assimilation pathways (43,44), in the down-regulation of photosynthesis upon nitrogen and sulfur starvation (45,46), in hypoxic growth (47), or during acclimation to phosphate deficiency (48). NO homeostasis results from an equilibrium between NO production by different enzymatic systems, which have been well documented in plants (49), and its active degradation mediated by different mechanisms including truncated hemoglobin that catalyze NO oxidation to nitrate in aerobic conditions (50,51).…”

The lipid biochemistry of eukaryotic algae

“…Lipid production in N. gaditana is doubled by knocking out a homolog of fungal Zn(II)2Cys6 encoding a transcriptional regulator of N assimilation pathways [227]. Furthermore, manipulation of the target of rapamycin (TOR) or nitric oxide (NO) signaling pathway is also shown to impact lipid production in algae [228][229][230]. It is worth noting that molecular targets or the regulatory circuits of above regulatory proteins related to lipid metabolism have not yet been worked out, and biochemical or molecular research in this direction is needed.…”

Stepwise Biogenesis of Subpopulations of Lipid Droplets in Nitrogen Starved Phaeodactylum tricornutum Cells

“…Some P. tricornutum mutants accumulating more TAG, such as lines overexpressing the NOA gene (NOAOE) (Dolch et al, 2017), have larger cells than wild type (WT) ( Figure 8B). The expression of NOA was correlated with nitric oxide (NO) emission within the cell, which triggered a transcriptional reprogramming and a metabolic rewiring diverting glycerolipid lipids toward TAG production.…”

“…Like most photosynthetic eukaryotes living in an environment subjected to frequent variations, diatoms have to cope with abiotic stresses of very diverse natures. An intense remodeling of glycerolipids leading to the formation of lipid droplets (LDs) is a common feature of the response of phytoplankton to stresses such as nutrients' starvation (Nguyen et al, 2011;Abida et al, 2015;Popko et al, 2016), high temperature (Yao et al, 2012;Alboresi et al, 2016), high light (Alboresi et al, 2016), exposure to nitric oxide (Dolch et al, 2017), hydrogen peroxide (Burch and Franz, 2016;Collins et al, 2016;Conte et al, 2018) or to a variety of chemicals (Kim et al, 2017;Wase et al, 2017;Conte et al, 2018;Wase et al, 2018). Glycerolipids consist of a three-carbon glycerol backbone (numbered sn-1, 2, and 3) esterified to fatty acids (FAs) at positions sn-1 and sn-2, which sn-3 position can be linked to a polar head.…”