In Vivo Interactions between Photosynthesis, Mitorespiration, and Chlororespiration in Chlamydomonas reinhardtii

Abstract

Interactions between photosynthesis, mitochondrial respiration (mitorespiration), and chlororespiration have been investigated in the green alga Chlamydomonas reinhardtii using flash illumination and a bare platinum electrode. Depending on the physiological status of algae, flash illumination was found to induce either a fast (t 1/2 Ϸ 300 ms) or slow (t 1/2 Ϸ 3 s) transient inhibition of oxygen uptake. Based on the effects of the mitorespiratory inhibitors myxothiazol and salicyl hydroxamic acid (SHAM), and of propyl gallate, an inhibitor of the chlororespiratory oxidase, we conclude that the fast transient is due to the flash-induced inhibition of chlororespiration and that the slow transient is due to the flash-induced inhibition of mitorespiration. By measuring blue-green fluorescence changes, related to the redox status of the pyridine nucleotide pool, and chlorophyll fluorescence, related to the redox status of plastoquinones (PQs) in C. reinhardtii wild type and in a photosystem I-deficient mutant, we show that interactions between photosynthesis and chlororespiration are favored when PQ and pyridine nucleotide pools are reduced, whereas interactions between photosynthesis and mitorespiration are favored at more oxidized states. We conclude that the plastid oxidase, similar to the mitochondrial alternative oxidase, becomes significantly engaged when the PQ pool becomes highly reduced, and thereby prevents its over-reduction.Photosynthesis and respiration, the two major bioenergetic processes of living organisms, coexist within plant cells. Although the photosynthetic electron transport chain (ETC) is clearly restricted to chloroplasts, a respiratory ETC, originally thought to be solely located in mitochondria, has been suggested to be also present in chloroplasts (Bennoun, 1982;Peltier et al., 1987). This chloroplast-based respiration, which has been called chlororespiration to differentiate it from mitorespiration (Bennoun, 1982), probably has its origins in the cyanobacterial endosymbiotic ancestor of chloroplasts (Scherer, 1990). The concept of chlororespiration was initially proposed to account for the effects of respiratory inhibitors, and particularly of inhibitors of terminal oxidases, on photosynthesis in unicellular green algae (Bennoun, 1982). It was reported that cyanide, CO, or salicyl hydroxamic acid (SHAM) increased the redox level of the plastoquinone (PQ) pool, as measured by chlorophyll (Chl) fluorescence induction curves. In addition, flash illumination of algae was found to induce the inhibition of a respiratory process (Peltier et al., 1987). The insensitivity of the flash-induced O 2 signal to both antimycin A and SHAM, inhibitors of the mitochondrial ETC, and the requirement for PS I led to the conclusion that chlororespiration, rather than mitorespiration, was inhibited by flash excitation of PS I (Peltier et al., 1987). However, reduction of the PQ pool or inhibitions of O 2 uptake could also be explained by an inhibition of mitorespiration coupled to interactions between chloropla...

Genome-Based Approaches to Understanding Phosphorus Deprivation Responses and PSR1 Control in Chlamydomonas reinhardtii

“…The PTOX1 protein may represent the terminal oxidase activity responsible for chlororespiration (8,38). This terminal oxidase may relieve redox pressure associated with photosynthetic electron transfer by withdrawing electrons from plastoquinol and combining them with O 2 .…”

Combined Increases in Mitochondrial Cooperation and Oxygen Photoreduction Compensate for Deficiency in Cyclic Electron Flow in Chlamydomonas reinhardtii

“…For this purpose, the effect of respiratory inhibitors was assessed on photosynthetic activities ( Figure 4). In C. reinhardtii, simultaneous addition of inhibitors of cytochrome bc and of the alternative respiration pathway is required to fully inhibit the respiratory chain (Cournac et al, 2002). When salicyl hydroxamic acid (SHAM), an inhibitor of the alternative oxidase was added, no significant change in chlorophyll fluorescence was observed.…”

“…The cell suspension (1.5 mL) was placed in the reaction vessel and bicarbonate (5 mM final concentration) was added to reach a saturating CO 2 concentration. O] (m/e = 32) were monitored, and O 2 exchange rates were determined as described previously (Cournac et al, 2002). When indicated, mitochondrial respiratory inhibitors myxothiazol and SHAM were added 15 min before starting measurements at final concentrations of 2 mM and 0.4 mM, respectively.…”

Alternative oxidase: an inter-kingdom perspective on the function and regulation of this broadly distributed 'cyanide-resistant' terminal oxidase

“…These inhibitors include sulfide (Azcón-Bieto et al 1989), cadmium (CastroGuerrero et al 2008), nitric oxide (NO) (Huang et al 2002), azide (Baurain et al 2003), antimycin A (Chae et al 2007a) and myxothiazol (Cournac et al 2002). These inhibitors might accumulate in tissues as a result of their abundance in particular environments or simply as products of normal physiological and biochemical processes.…”