Redox mechanisms in “oxidant-dependent” hexose fermentation by Rhodopseudomonas capsulata

Trimethylamine N-oxide (TMAO) can function as an electron acceptor in the anaerobic metabolism of both Rhodopseudomonas capsulata and Escherichia coli. In both bacteria, anaerobic growth in the presence of TMAO induces a system that can reduce TMAO to trimethylamine (TMA). Comparative studies, however, show that TMAO reduction serves different purposes in the organisms noted. In E. coli, anaerobic growth on sugars does not require the presence of TMAO, but in cells induced for TMAO reductase, TMAO can act as the terminal electron acceptor for membrane-associated oxidative phosphorylation. Anaerobic dark growth of R. capsulata is dependent on the presence of TMAO (or an analog) and in this organism a soluble system catalyzes anaerobic oxidation of NADH with TMAO. The mechanism, in R. capsulata, appears to involve a flavoprotein of the flavodoxin type and presumably represents a system for maintenance of redox balance during anaerobic dark fermentation of hexoses and related compounds.     

Photoproduction of H2 from Cellulose by an Anaerobic Bacterial Coculture

Cellulomonas sp. strain ATCC 21399 is a facultatively anaerobic, cellulose-degrading microorganism that does not evolve hydrogen but produces organic acids during cellulose fermentation. Rhodopseudomonas capsulata cannot utilize cellulose, but grows photoheterotrophically under anaerobic conditions on organic acids or sugars. This report describes an anaerobic coculture of the Cellulomonas strain with wild-type R. capsulata or a mutant strain lacking uptake hydrogenase, which photoevolves molecular hydrogen by the nitrogenase system of R. capsulata with cellulose as the sole carbon source. In coculture, the hydrogenase-negative mutant produced 4.6 to 6.2 mol of H₂ per mol of glucose equivalent, compared with 1.2 to 4.3 mol for the wild type.     

Regulation of cyclic electron transport through photosystem I in cyanobacterium <Emphasis Type="Italic">Synechocystis</Emphasis> sp. PCC 6803 mutants deficient in respiratory dehydrogenases

The rate of PSI mediated cyclic electron transport was studied in wild type and mutant cells of Synechocystis sp. PCC 6803 deficient in NDH-1 (M55) or succinate dehydrogenase (SDH⁻) that are responsible for the dark reduction of the plastoquinone pool. Kinetics of P700 photooxidation and P700⁺ dark reduction in the presence of 5·10⁻⁵ M 3-(3,4-dichlorophenyl)-1,1-dimethylurea have been registered as light induced absorbance changes at 810 nm resulting from illumination of cells with 730-nm actinic light for 1 sec. It is shown that in the absence of dehydrogenases the rate of dark reduction of P700⁺ in both mutants did not decrease but even increased in NDH-1-less mutant cells as compared with the rate in wild type cells. Dibromothymoquinone drastically reduced the rate of P700⁺ dark reduction both in wild type and in mutant cells. Thus, the cyclic electron transfer from ferredoxin through the plastoquinone pool to P700⁺, which is independent from dehydrogenases, takes place in all the types of cells. Preillumination of cells of wild type and both mutants for 30 min or anaerobic conditions resulted in delay of P700 photooxidation and acceleration of P700⁺ dark reduction, while the level of photosynthesis and respiration terminal acceptors (NAD(P)⁺ and oxygen) decreased. It appears that the rate of P700 photooxidation and P700⁺ dark reduction in cyclic electron transport in Synechocystis wild type and mutant cells is determined by the level of NADP⁺ and oxygen in stroma. A possible approach to evaluation of the levels of these acceptors in vivo is proposed, based on kinetic curve parameters of P700 photoconversions induced by 730-nm light with 1-sec duration.     

Fermentation and anaerobic respiration by Rhodospirillum rubrum and Rhodopseudomonas capsulata

Rhodospirillum rubrum and Rhodopseudomonas capsulata were able to grow anaerobically in the dark either by a strict mixed-acid fermentation of sugars or, in the presence of an appropriate electron acceptor, by an energy-linked anaerobic respiration. Both species fermented fructose without the addition of accessory oxidants, but required the initial presence of bicarbonate before fermentative growth could begin. Major products of R. rubrum fermentation were succinate, acetate, propionate, formate, hydrogen, and carbon dioxide; R. capsulata produced major amounts of lactate, acetate, succinate, hydrogen, and carbon dioxide. R. rubrum and R. capsulata were also capable of growing strictly through anaerobic, respiratory mechanisms. Nonfermentable substrates, such as succinate, malate, or acetate, supported growth only in the presence of an electron acceptor such as dimethyl sulfoxide or trimethylamine oxide. Carbon dioxide and dimethyl sulfide were produced during growth of R. rubrum and R. capsulata on succinate plus dimethyl sulfoxide. Molar growth yields from cultures grown anaerobically in the dark on fructose plus dimethyl sulfoxide were 3.8 to 4.6 times higher than values obtained from growth on fructose alone and were 56 to 60% of the values obtained from aerobic, respiratory growth with fructose. Likewise, molar growth yields from anaerobic, respiratory growth conditions with succinate plus dimethyl sulfoxide were 51 to 54% of the values obtained from aerobic, respiratory growth with succinate. The data indicate that dimethyl sulfoxide or trimethylamine oxide as a terminal oxidant is approximately 33 to 41% as efficient as O₂ in conserving energy through electron transport-linked respiration.     

Reconstitution of light-dependent electron transport in membranes from a bacteriochlorophyll-less mutant of Rhodopseudomonas spheroides

A mutant, O₁, of Rhodopseudomonas spheroides has been prepared that is not capable of bacteriochlorophyll synthesis, but excretes pigments spectroscopically similar to green plant chlorophylls. The cytochrome content and respiratory activity of membranes from O₁ resemble those of aerobically grown wild type R. spheroides, but the mutant could not adapt to grow photosynthetically. Photosynthetic reaction centres were purified from the blue green mutant, of R. spheroides, added to membranes from O₁, and the detergent used in reaction centre preparation removed by carefully controlled reduction. A reaction centre membrane complex was formed in which the ratio of reaction centre to cytochrome b was near 1 : 2. Illumination caused oxidation of the membrane cytochrome c and reduction of cytochrome b. These changes were enhanced in the presence of antimycin A, suggesting that a cyclic electron flow system had been reconstituted. The implication of these results on the formation of the photosynthetic electron flow system is discussed.     

Growth of Rhodopseudomonas capsulata under anaerobic dark conditions with dimethyl sulfoxide

The photosynthetic bacterium, Rhodopseudomonas capsulata, could be cultured anaerobically in the absence of light on a synthetic medium with glucose as the carbon source only when dimethyl sulfoxide (DMSO) was added. The extent of growth was proportional to both DMSO and glucose concentrations. Optimal growth was achieved with 20 mm DMSO and 0.25% glucose. Under the best conditions, cells divided with a doubling time of 12 h. Pyruvate also supported the anaerobic dark growth of R. capsulata when DMSO was present. R. capsulata, R. sphaeroides, and R. palustris strains were all able to grow under anaerobic dark conditions with DMSO. Experiments using [¹⁴C]DMSO showed that more than 95% of the ¹⁴C was converted by cultures of R. capsulata to a volatile compound, identified as dimethyl sulfide (DMS) by gas chromatography, thus demonstrating that DMSO was being reduced to DMS during growth. These results indicate that R. capsulata requires a terminal electron acceptor for anaerobic dark growth and that DMSO can serve that function.     

Cytochrome and Alternative Pathway Respiration during Transient Ammonium Assimilation by N-Limited Chlamydomonas reinhardtii

Mass spectrometric analysis of gas exchange in light and dark by N-limited cells of Chlamydomonas reinhardtii indicated that ammonium assimilation was accompanied by an increase in respiratory carbon flow to provide carbon skeletons for amino acid synthesis. Tricarboxylic acid (TCA) cycle carbon flow was maintained by the oxidation of TCA cycle reductant via the mitochondrial electron transport chain. In wild-type cells, inhibitor studies and ¹⁸O₂ discrimination experiments indicated that respiratory electron flow was mediated entirely via the cytochrome pathway in both the light and dark, despite a large capacity for the alternative pathway. In a cytochrome oxidase deficient mutant, or in wild-type cells in the presence of cyanide, the alternative pathway could support the increase in TCA cycle carbon flow. These different mechanisms of oxidation of TCA cycle reductant were reflected by the much greater SHAM sensitivity of ammonium assimilation by cytochrome oxidase-deficient cells as compared to wild type.     

Diazotrophic growth of Rhodopseudomonas acidophila and Rhodopseudomonas capsulata under microaerobic conditions in the dark

Diazotrophy of Rhodopseudomonas acidophila and Rhodopseudomonas capsulata was not obligatorily linked to photosynthesis. In the dark R. acidophila grew with dinitrogen as sole nitrogen source at a dissolved oxygen tension of 15 Torr (= 2.0 kPa); the doubling time was 8 h. Acetylene reduction by whole cells was more sensitive to oxygen in the light than in the dark. 16.5 mg N₂ were fixed per g lactic acid consumed. R. capsulata synthesized nitrogenase and fixed dinitrogen in the dark at a dissolved oxygen tension of less than one Torr (= 0.13 kPa). The doubling time of this bacterium was 16 h and 10.5 mg N₂ were fixed per g lactic acid consumed.Abbreviation kPa kilopascal     

The activities of two pathways of nitrate reduction in Rhodopseudomonas capsulata

1. The disappearance of nitrate from suspensions of intact, washed cells of Rhodopseudomonas capsulata strain N22DNAR⁺ was measured with an ion selective electrode. In samples taken from phototrophic cultures grown to late exponential phase, nitrate disappearance was partially inhibited by light but was not affected by the presence of ammonium. Nitrate disappearance from samples from low density cultures in the early exponential phase of growth was first inhibited and later stimulated by light. In these cells ammonium ions inhibited the light-dependent but not the dark disappearance of nitrate. It is concluded that cells in the early exponential phase of growth possess both an ammonium-sensitive, assimilatory pathway for nitrate reduction (NRI) and an ammonium-insensitive pathway for nitrate reduction (NRII) which is linked to respiratory electron flow and energy conservation. In cells harvested in late exponential phase only the respiratory pathway for pitrate reduction is detectable.
2. Nitrate reduction, as judged by the oxidation of reduced methyl viologen by anaerobic cell suspensions, was measured at high rates in those strains of R. capsulata (AD2, BK5, N22DNAR⁺) which are believed to possess NRII activity but not in those strains (Kbl, R3, N22) which only manifest the ammonium-sensitive NRI pathway. On this basis we have used nitrate-dependent oxidation of reduced methyl viologen as a diagnostic test for the nitrate reductase of NRII in cells harvested from cultures of R. capsulata strain AD2. The activity was readily detectable in cells from cultures grown aerobically in the dark with ammonium nitrate as source of nitrogen. When the oxygen supply to the culture was withdrawn, the level of methyl viologen-dependent nitrate reductase increased considerably and nitrite accumulated in the culture medium. Upon reconnecting the oxygen supply, methyl viologen-dependent nitrate reductase activity decreased and the reduction of nitrate to nitrite in the culture was inhibited. It is concluded that the respiratory nitrate reductase activity is regulated by the availability of electron transport pathways that are linked to the generation of a proton electrochemical gradient.

     

Photoinduction of electron transport on the acceptor side of PSI in Synechocystis PCC 6803 mutant deficient in flavodiiron proteins Flv1 and Flv3

After transferring the dark-acclimated cyanobacteria to light, flavodiiron proteins Flv1/Flv3 serve as a main electron acceptor for PSI within the first seconds because Calvin cycle enzymes are inactive in the dark. Synechocystis PCC 6803 mutant Δflv1/Δflv3 devoid of Flv1 and Flv3 retained the PSI chlorophyll P700 in the reduced state over 10?s (Helman et al., 2003; Allahverdiyeva et al., 2013). Study of P700 oxidoreduction transients in dark-acclimated Δflv1/Δflv3 mutant under the action of successive white light pulses separated by dark intervals of various durations indicated that the delayed oxidation of P700 was determined by light activation of electron transport on the acceptor side of PSI. We show that the light-induced redox transients of chlorophyll P700 in dark-acclimated Δflv1/Δflv3 proceed within 2?min, as opposed to 1–3?s in the wild type, and comprise a series of kinetic stages. The release of rate-limiting steps was eliminated by iodoacetamide, an inhibitor of Calvin cycle enzymes. Conversely, the creation with methyl viologen of a bypass electron flow to O₂ accelerated P700 oxidation and made its extent comparable to that in the wild-type cells. The lack of major sinks for linear electron flow in iodoacetamide-treated Δflv1/Δflv3 mutant, in which O₂- and CO₂-dependent electron flows were impaired, facilitated cyclic electron flow, which was evident from the decreased steady-state oxidation of P700 and from rapid dark reduction of P700 during and after illumination with far-red light. The results show that the photosynthetic induction in wild-type Synechocystis PCC 6803 is largely hidden due to the flavodiiron proteins whose operation circumvents the rate-limiting electron transport steps controlled by Calvin cycle reactions.     

Chemoautotrophic growth of Rhodopseudomonas species with hydrogen and chemotrophic utilization of methanol and formate

A chemolithoautotrophic type of metabolism, which was hitherto unknown for purple nonsulfur bacteria, was demonstrated by growth experiments using Rhodopseudomonas capsulata Kb1 and Rhodopseudomonas acidophila 10050. These strains were able to grow in a mineral medium in the dark at the expense of H₂, O₂, and CO₂. A minimum doubling time of 9 h was obtained for R. capsulata under an atmosphere containing less than 15% oxygen; higher oxygen concentrations suppressed autotrophic but not chemoorganotrophic growth. Oxygen sensitivity of chemoautotrophically growing cells of R. acidophila was even more pronounced, whereas cells growing chemotrophically on methanol almost tolerated the oxygen concentration of air. Highest oxygen sensitivity of growth of R. acidophila was observed with formate as substrate. The growth yield of cultures grown semiaerobically in the dark on methanol was 0.23 g dry cell material per g methanol consumed.     

Rhodopseudomonas adriatica sp. nov., a new species of the Rhodospirillaceae,dependent on reduced sulfur compounds

A new purple nonsulfur bacterium was isolated from enrichment cultures of a sulfide-containing marine lagoon. The bacterium is similar to Rhodopseudomonas capsulata and is described as a new species of the genus Rhodopseudomonas: Rhodopseudomonas adriatica. Cells are non-motile, 0.5–0.8 m by 1.3–1.8 m, and multiply by binary fission. Intracytoplasmic membranes are of the vesicular type. The photosynthetic pigments are bacteriochlorophyll a and carotenoids of the spheroidene group. Growth is possible anaerobically in the light and at low pO₂ in the dark. Biotin and thiamine are required as growth factors. A wide variety of organic compounds, as well as sulfide and thiosulfate, are used as photosynthetic electron donors. Sulfide is oxidized to elemental sulfur, which is subsequently converted to sulfate, whereas thiosulfate oxidation occurs without measurable intermediate. Rhodopseudomonas adriatica is unable to assimilate sulfate, growth is only possible in the presence of a reduced sulfur compound.     

The role of PGR5 in the redox poising of photosynthetic electron transport

The pgr5 mutant of Arabidopsis thaliana has been described as being deficient in cyclic electron flow around photosystem I, however, the precise role of the PGR5 protein remains unknown. To address this issue, photosynthetic electron transport was examined in intact leaves of pgr5 and wild type A. thaliana. Based on measurements of the kinetics of P700 oxidation in far red light and re-reduction following oxidation in the presence of DCMU, we conclude that this mutant is able to perform cyclic electron flow at a rate similar to the wild type. The PGR5 protein is therefore not essential for cyclic flow. However, cyclic flow is affected by the pgr5 mutation under conditions where this process is normally enhanced in wild type leaves, i.e. high light or low CO₂ concentrations resulted in enhancement of cyclic electron flow. This suggests a different capacity to regulate cyclic flow in response to environmental stimuli in the mutant. We also show that the pgr5 mutant is affected in the redox poising of the chloroplast, with the electron transport chain being substantially reduced under most conditions. This may result in defective feedback regulation of photosynthetic electron transport under some conditions, thus providing a rationale for the reduced efficiency of cyclic electron flow.     

Composition of the cell wall of the phage resistant mutantRhodopseudomonas capsulata St. Louis RC1-

A mutant ofRhodopseudomonas capsulata St. Louis (R. capsulata St. Louis RC1^-), resistant against the bacteriophage RC1, was isolated and its cytoplasmic membrane and cell wall fractions (buoyant densities on sucrose density gradient centrifugation: 1.123 and 1.222 g/cm³, respectively) were obtained. Different from the wild type strain, the cell wall fraction of the mutant lacked galactose. Galactose is a characteristic component of the capsule polysaccharide ofR. capsulata St. Louis. There were no differences in lipopolysaccharide and peptidoglycan compositions as well as in polypeptide patterns of the cell wall fractions between mutant and wild-type cells. Thus, the lack of a firmly bound capsule inR. capsulata St. Louis RC1^- was the only difference found.     

Redox chain and energy transduction in chromatophores from Rhodopseudomonas capsulata cells grown anaerobically in the dark on glucose and dimethyl sulfoxide

Membranes from cells of Rhodopseudomonas capsulata grown anaerobically in the dark on glucose plus dimethyl sulfoxide differ from those obtained from photoheterotrophically grown cells in several ways: (a) there are qualitative and quantitative variations in the cytochrome composition; (b) electron-transport rates are unusually low in the cytochrome b to cytochrome c region; (c) light-induced ATP synthesis is dependent on the ability of the alternate respiratory pathway to maintain the Q₁₀-cytochrome b complex in a partially oxidized state; (d) a non-energy-conserving NADH-dehydrogenase activity dominates the respiratory activity. In addition, data obtained with both wild-type and mutant cells that contain altered electron-transport systems tend to exclude a role of the redox chain as ATP-producing machinery during anaerobic/dark growth.     

Bacteriochlorophyll Synthesis and the Ultrastructure of Wild Type and Mutant Strains of Rhodopseudomonas spheroides

The ultrastructure of sectioned cells of mutant and wild type Rhodopseudomonas spheroides has been examined by electron microscopy. The characteristic vesicles associated with the presence of bacteriochlorophyll were found in wild type cells grown with low aeration. These were also found in mutant TA-R which forms bacteriochlorophyll under high aeration. None of the mutants with blocks in bacteriochlorophyll synthesis contained intracytoplasmic membrane. These included mutant 8-17 which accumulates bacteriochlorophyllide but fails at the phytolation step. We conclude that the intact bacteriochlorophyll molecule, or some particular membrane protein associated with it, is needed for the development of the characteristic intracytoplasmic membrane system in R. spheroides.     

An Investigation of Electron Spin Resonance in Wild Type Chlamydomonas reinhardi and Mutant Strains Having Impaired Photosynthesis

The electron spin resonance signals of wild type Chlamydomonas reinhardi and three mutant strains having impaired photosynthesis have been investigated. The wild type strain generates two different electron spin resonance signals. Signal I is obtained without illumination (i.e., dark signal) whereas signal II is generated preferentially only by red light. Signal I is missing from wild type cells that have been cultured in the dark, but it returns after these dark-grown cells have been illuminated. Chloroplast fragments obtained from the three mutant strains cannot photoreduce TPN. Two of the strains lack the dark signal I while the third strain has both signal I and signal II. Other studies have revealed that the two mutant strains which lack signal I give no Hill reaction but that they can photoreduce TPN if supplied with an artificial reductant. The mutant strain which has both electron spin resonance signals can carry out the Hill reaction, yet it too will not photoreduce TPN unless reductant is supplied. The electron spin resonance signals generated by the wild type and mutant strains are discussed in terms of the pathway of TPN photoreduction, and it is suggested that signal I is associated with one of the two light-dependent phases of this pathway.     

Evidence for a Block between Plastoquinone and Cytochrome f in a Photosynthetic Mutant of Lemna with Abnormal Flowering Behavior

Mutant strain 1073 of Lemna perpusilla is concluded to be blocked between plastoquinone and cytochrome f in the photosynthetic electron transport system. The location of the block is based on the following observations of activities in chloroplasts isolated from the mutant and wild-type plants. (a) Relative to wild type, electron flow rates from water to ferricyanide, 2,6-dichlorophenol indophenol or NADP were very low in the mutant, but rates of photosystem I-dependent electron flow and cyclic phosphorylation were high. (b) Chlorophyll a fluorescence induction curves for mutant and wild type were similar. (c) Silicomolybdate and lipophilic acceptors in the mutant were photoreduced at rates comparable to wild type. (d) Cytochrome f of the mutant chloroplasts was not reduced by red light, but was oxidized by red or far red light. (e) Reduction of the primary electron acceptor of photosystem II (Q) by ATP-driven reverse electron flow was not observed in the mutant.     

Asymmetry of an energy transducing membrane. The location of cytochrome c2 in Rhodopseudomonas spheroides and Rhodopseudomonas capsulata

Monospecific antibodies have been prepared against cytochrome c₂ from Rhodopseudomonas spheroides and Rhodopseudomonas capsulata, and against cytochrome c′ from Rps. capsulata. These antibodies precipitated their respective antigens, but did not cross react with a wide range of procaryotic or eucaryotic cytochromes, or with other bacterial proteins. The cytochromes produced during aerobic growth were immunologically indistinguishable from those produced during photosynthetic growth.Cytochrome c₂ is located in vivo in the periplasmic space between the cell wall and the cell membrane, and when chromatophores are prepared from whole cells the cytochrome becomes trapped inside these vesicles. The implications of these results to energy coupling in the photosynthetic bacteria are discussed.     

Cyclic photophosphorylation by chromatophores of the facultative phototroph,Rhodopseudomonas capsulata

Summary Cyclic photophosphorylation catalyzed by chromatophores derived from the facultative phototroph, Rhodopseudomonas capsulata was investigated. In the absence of an external electron donor such as succinate, cyclic photophosphorylation is strongly inhibited by O₂. Maximal phosphorylation rates are obtained in the presence of molecular hydrogen. Cytochrome c and bovine serum albumin have no significant effects on the reaction. However, dichlorophenolindophenol and phenazonium methosulfate are inhibitory to cyclic photophosphorylation. Cyclic photophosphorylation is sensitive to antimycin A, but highly resistant to heptylhydroxy-quinoline-N-oxide. Neither phenazonium methosulfate, nor dichlorophenolindophenol or tetramethyl-p-phenylenediamine can effect antimycin-insensitive cyclic photophosphorylation. Oligomycin strongly inhibits the phosphorylation. Overreduction caused by the ascorbate-dichlorophenolindophenol couple results in strong inhibition of phosphorylation. Addition of fumarate decreases the inhibition caused by overreduction. However, the fumarate mediated phosphorylation is nearly completely inhibited by antimycin A. Atebrine is a strong inhibitor for cyclic photophosphorylation, whereas dinitrophenol is only a weak inhibitor.

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Zusammenfassung Die durch Chromatophoren aus dem fakultativ phototrophen Rhodopseudomonas capsulata katalysierte cyclische Photophosphorylierung wurde untersucht. In der Abwesenheit eines zusätzlichen Elektronendonators wie Succinat wird die cyclische Photophosphorylierung durch O₂ stark gehemmt. Maximale Phosphorylierungsraten werden unter H₂-Atmosphäre erzielt. Cytochrom c und Rinderserumalbumin haben keinen deutlichen Effekt auf die Reaktion. Demgegenüber haben Dichlorphenolindophenol und Phenazinmethosulfat eine hemmende Wirkung auf die cyclische Photophosphorylierung. Die cyclische Photophosphorylierung wird durch Antimycin A stark gehemmt, ist aber gegenüber Heptyl-hydroxy-chinolin-N-oxyd auffallend resistent. Weder Phenazinmethosulfat noch Dichlorphenolindophenol oder Tetramethyl-p-phenylendiamin bewirken eine antimycin-resistente Phosphorylierung. Oligomycin hemmt die Photophosphorylierung stark. Eine durch Ascorbat-Dichlorphenolindophenol verursachte Überreduktion wirkt sich stark hemmend auf die Phosphorylierung aus. In Gegenwart von Fumarat ist die durch Überreduktion bedingte Hemmung stark verringert. Diese vom Fumarat abhängige Photophosphorylierung wird jedoch durch Antimycin A beinahe vollständig gehemmt. Atebrin ist ein starker Hemmstoff für die cyclische Photophosphorylierung. Demgegenüber ist die durch Dinitrophenol bewirkte Hemmung der cyclischen Photophosphorylierung gering.

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Abbreviations ADP adenosine diphosphate - ATP adenosine triphosphate - BChl bacteriochlorophyll - DNP 2,4-dinitrophenol - DCPIP dichlorophenolindophenol - FAD flavinadenine dinucleotide - FMN flavin mononucleotide - G-6-P glucose-6-phosphate - HOQNO heptylhydroxy-quinoline-N-oxide - NAD(P) nicotinamid-adenine-dinucleotide (phosphate) - PMS phenazonium methosulfate - Rh. Rhodospirillum - Rhps. Rhodopseudomonas - TMPD tetramethyl-p-phenylenediamine