Multiple facets of anoxic metabolism and hydrogen production in the unicellular green alga Chlamydomonas reinhardtii

Abstract

SummaryMany microbes in the soil environment experience micro-oxic or anoxic conditions for much of the late afternoon and night, which inhibit or prevent respiratory metabolism. To sustain the production of energy and maintain vital cellular processes during the night, organisms have developed numerous pathways for fermentative metabolism. This review discusses fermentation pathways identified for the soil-dwelling model alga Chlamydomonas reinhardtii, its ability to produce molecular hydrogen under anoxic conditions through the activity of hydrogenases, and the molecular flexibility associated with fermentative metabolism that has only recently been revealed through the analysis of specific mutant strains.

Induction of Photosynthetic Carbon Fixation in Anoxia Relies on Hydrogenase Activity and Proton-Gradient Regulation-Like1-Mediated Cyclic Electron Flow in Chlamydomonas reinhardtii

“…The low rate measured here is in good agreement with the rate of 2 e -s -1 PSI -1 measured for PQ reduction by NDA2 (Houille-Vernes et al, 2011) and the rate of 50 to 100 nmol H 2 mg chlorophyll -1 min -1 determined for NDA2-driven H 2 production from starch degradation (Baltz et al, 2014), the latter value also corresponding to approximately 1 to 2 e -s -1 PSI -1 , assuming 500 chlorophyll per photosynthetic unit (Kolber and Falkowski, 1993). Alternatively, this remaining ETR in the double mutant might correspond to the activity of another chloroplastic fermentative pathway linked to FDX reoxidation (Grossman et al, 2011). Regarding these possibilities, .…”

“…Under anoxia, lack of ATP synthesis by F 1 F O ATP synthase (EC 3.6.3.14) due to the absence of mitochondrial respiration is compensated by the activity of various plant-and bacterial-type fermentative enzymes that drive a sustained glycolytic activity (Mus et al, 2007;Terashima et al, 2010;Grossman et al, 2011;Yang et al, 2014). In C. reinhardtii, upstream glycolytic enzymes, including the reversible glyceraldehyde 3-P dehydrogenase, are located in the chloroplast (Johnson and Alric, 2012).…”

Cellulose degradation and assimilation by the unicellular phototrophic eukaryote Chlamydomonas reinhardtii

“…Furthermore, C. reinhardtii combines plant, as well as animal features, and has retained many genes of the last common plant-animal ancestor, which were lost from the genomes of angiosperms (flowering plants) 12 . Another important difference between flowering plants and C. reinhardtii is its use of fermentative pathways characteristic for anaerobic chemotrophs, but not for oxygenic phototrophs, which can be explained by extended periods of anoxia experienced by this soildwelling photosynthetic microbe 16 .…”

A Mutant in theADH1Gene ofChlamydomonas reinhardtiiElicits Metabolic Restructuring during Anaerobiosis

“…ACK1, Acetate kinase isoform 1; ACK2, acetate kinase isoform 2; ADH, alcohol dehydrogenase (ADH1, ADH2, or ADH3 could perform this reaction; see text); ADH1, acetaldehyde/alcohol dehydrogenase; FDX, ferredoxin; FMR, fumarate reductase; FUM, fumarase; HYDA1 and HYDA2, two putative hydrogenases; LDH, lactate dehydrogenase; MDH, malate dehydrogenase; MME4, malic enzyme; PAT1, phosphate acetyltransferase isoform 1; PAT2, phosphate acetyltransferase isoform 2; PDC3, pyruvate decarboxylase; PEPC, phosphenolpyruvate carboxylase; PFL1, pyruvate formate lyase; PFR1, pyruvate:ferredoxin oxidoreductase; PYC, pyruvate carboxylase; PYK, pyruvate kinase. This figure was modified from Grossman et al (2011). fermentation metabolism (Dubini et al, 2009;Grossman et al, 2011;Philipps et al, 2011;Catalanotti et al, 2012).…”

“…A number of these fermentation pathways are typical of those present in various prokaryotes and some eukaryotes (Mus et al, 2007). Some enzymes that function in these pathways include pyruvate:ferredoxin oxidoreductase (PFR), pyruvate decarboxylase (PDC), lactate dehydrogenase (LDH), pyruvate formate lyase (PFL), alcohol dehydrogenase (ADH), phosphate acetyltransferase (PAT), acetate kinase (ACK), and the two [FeFe] hydrogenases (HYDA1 and HYDA2) and their maturation proteins, HYDG and HYDEF (Posewitz et al, 2004;Atteia et al, 2006;Ghirardi et al, 2007;Mus et al, 2007;Hemschemeier et al, 2008;Grossman et al, 2011). The anaerobic activities of these and other enzymes result in the secretion of organic acids (formate, lactate, malate, acetate, and succinate) and alcohols (ethanol and glycerol) as well as the evolution of H 2 and CO 2 (Gfeller and Gibbs, 1984;Kreuzberg, 1984;Ohta et al, 1987;Tsygankov et al, 2002;Kosourov et al, 2003;Mus et al, 2007;Dubini et al, 2009).…”