Algal photosynthesis converts nitric oxide into nitrous oxide

Abstract

Nitrous oxide (N2O), a potent greenhouse gas in the atmosphere, is produced mostly from aquatic ecosystems, to which algae substantially contribute. However, mechanisms of N2O production by photosynthetic organisms are poorly described. Here we show that the green microalga Chlamydomonas reinhardtii reduces NO into N2O using the photosynthetic electron transport. Through the study of C. reinhardtii mutants deficient in flavodiiron proteins (FLVs) or in a cytochrome p450 (CYP55), we show that FLVs contribute to NO reduction in the light, while CYP55 operates in the dark. Both pathways are active when NO is produced in vivo during the reduction of nitrites and participate in NO homeostasis. Furthermore, NO reduction by both pathways is restricted to chlorophytes, organisms particularly abundant in ocean N2O-producing hot spots. Our results provide a mechanistic understanding of N2O production in eukaryotic phototrophs and represent an important step toward a comprehensive assessment of greenhouse gas emission by aquatic ecosystems.

Chlamydomonas reinhardtii, an Algal Model in the Nitrogen Cycle

“…The genes involved in the foraminifer denitrification pathway have been recently identified [20]; however, the genes encoding the enzymes responsible for the first and last steps of this pathway, the dissimilatory nitrate reductases and nitrous oxide reductase, are missing in most of the foraminifer genomes but found in the associated bacteria. Partial nitrate denitrification to N 2 O has also been well documented in fungi [21][22][23][24][25] and recently described in the green microalga Chlamydomonas reinhardtii, where a NO reductase (CYP55) [26] and flavodiiron proteins (FLVs) [27] catalyze the reduction of NO to N 2 O in dark and light conditions, respectively. These two proteins constitute the molecular evidence that supports that microalgae contribute to N 2 O emissions, something known for decades [28].…”

“…The dark NO reduction attributed to CYP55 activity has also been shown to be stronger when cells are grown in the presence of nitrate [27]. Although found in the mitochondrial proteome, CYP55 is also predicted to be targeted to the chloroplast [27]. Thus, it is possible that the protein is targeted to both organelles.…”

“…The Chlamydomonas genome contains two genes encoding for both proteins, NIRK and CYP55 (Table 1). CYP55 appears to be responsible for N 2 O production in the dark [26,27]. Accordingly, CYP55 is located in mitochondria [38] and its transcript is accumulated in the dark [64] and in the presence of nitrate [38].…”

“…Accordingly, CYP55 is located in mitochondria [38] and its transcript is accumulated in the dark [64] and in the presence of nitrate [38]. The dark NO reduction attributed to CYP55 activity has also been shown to be stronger when cells are grown in the presence of nitrate [27]. Although found in the mitochondrial proteome, CYP55 is also predicted to be targeted to the chloroplast [27].…”

“…The second type of protein shown to reduce NO to N 2 O, in Chlamydomonas, corresponds to FLVs (flavodiiron proteins) [27]. Flavodiiron proteins belong to a singular family of oxygen and/or nitric oxide reductases widespread in prokaryote and eukaryote organisms.…”