Electron Donor For Anoxygenic Photosynthesis Research Articles

Venus' Mass Spectra Show Signs of Disequilibria in the Middle Clouds.

We present a re‐examination of mass spectral data obtained from the Pioneer Venus Large Probe Neutral Mass Spectrometer. Our interpretations of differing trace chemical species are suggestive of redox disequilibria in Venus' middle clouds. Assignments to the data (at 51.3 km) include phosphine, hydrogen sulfide, nitrous acid, nitric acid, carbon monoxide, hydrochloric acid, hydrogen cyanide, ethane, and potentially ammonia, chlorous acid, and several tentative PxOy species. All parent ions were predicated upon assignment of corresponding fragmentation products, isotopologues, and atomic species. The data reveal parent ions at varying oxidation states, implying the presence of reducing power in the clouds, and illuminating the potential for chemistries yet to be discovered. When considering the hypothetical habitability of Venus' clouds, the assignments reveal a potential signature of anaerobic phosphorus metabolism (phosphine), an electron donor for anoxygenic photosynthesis (nitrite), and major constituents of the nitrogen cycle (nitrate, nitrite, ammonia, and N2).

Arsenite as an Electron Donor for Anoxygenic Photosynthesis: Description of Three Strains of Ectothiorhodospira from Mono Lake, California and Big Soda Lake, Nevada.

Three novel strains of photosynthetic bacteria from the family Ectothiorhodospiraceae were isolated from soda lakes of the Great Basin Desert, USA by employing arsenite (As(III)) as the sole electron donor in the enrichment/isolation process. Strain PHS-1 was previously isolated from a hot spring in Mono Lake, while strain MLW-1 was obtained from Mono Lake sediment, and strain BSL-9 was isolated from Big Soda Lake. Strains PHS-1, MLW-1, and BSL-9 were all capable of As(III)-dependent growth via anoxygenic photosynthesis and contained homologs of arxA, but displayed different phenotypes. Comparisons were made with three related species: Ectothiorhodospira shaposhnikovii DSM 2111, Ectothiorhodospira shaposhnikovii DSM 243T, and Halorhodospira halophila DSM 244. All three type cultures oxidized arsenite to arsenate but did not grow with As(III) as the sole electron donor. DNA–DNA hybridization indicated that strain PHS-1 belongs to the same species as Ect. shaposhnikovii DSM 2111 (81.1% sequence similarity), distinct from Ect. shaposhnikovii DSM 243T (58.1% sequence similarity). These results suggest that the capacity for light-driven As(III) oxidation is a common phenomenon among purple photosynthetic bacteria in soda lakes. However, the use of As(III) as a sole electron donor to sustain growth via anoxygenic photosynthesis is confined to novel isolates that were screened for by this selective cultivation criterion.

The genetic basis of anoxygenic photosynthetic arsenite oxidation.

'Photoarsenotrophy', the use of arsenite as an electron donor for anoxygenic photosynthesis, is thought to be an ancient form of phototrophy along with the photosynthetic oxidation of Fe(II), H2 S, H2 and NO2-. Photoarsenotrophy was recently identified from Paoha Island's (Mono Lake, CA) arsenic-rich hot springs. The genomes of several photoarsenotrophs revealed a gene cluster, arxB2AB1CD, where arxA is predicted to encode for the sole arsenite oxidase. The role of arxA in photosynthetic arsenite oxidation was confirmed by disrupting the gene in a representative photoarsenotrophic bacterium, resulting in the loss of light-dependent arsenite oxidation. In situ evidence of active photoarsenotrophic microbes was supported by arxA mRNA detection for the first time, in red-pigmented microbial mats within the hot springs of Paoha Island. This work expands on the genetics for photosynthesis coupled to new electron donors and elaborates on known mechanisms for arsenic metabolism, thereby highlighting the complexities of arsenic biogeochemical cycling.

Transformation of monothioarsenate by haloalkaliphilic, anoxygenic photosynthetic purple sulfur bacteria.

Thioarsenates are the dominant arsenic species in arsenic-rich, alkaline, and sulfidic waters, but bacterial interactions with these compounds have only recently been examined. Previous studies have shown that microorganisms play a role in the transformation of monothioarsenate to arsenate, including use of monothioarsenate as a chemolithotrophic electron donor coupled with oxygen as an electron acceptor. We obtained enrichment cultures from two saline, alkaline lakes (Mono Lake, CA and Big Soda Lake, NV) that are able to use monothioarsenate as the sole electron donor for anoxygenic photosynthesis. These anoxic cultures were able to convert a 1 mM mixture of thioarsenates completely to arsenate in c. 13 days and 4 mM monothioarsenate to arsenate in c. 17 days. This conversion was light dependent; thus, monothioarsenate can be used as the sole electron donor for anoxygenic photosynthesis. Both of the Mono Lake and Big Soda Lake enrichment cultures were dominated by an organism closely related to Ectothiorhodospira species. We tested additional strains of purple sulfur bacteria and found widespread ability to use monothioarsenate as an electron donor. The ability of bacteria to transform thioarsenates directly via anoxygenic photosynthesis adds a new perspective to the well-studied arsenic and sulfur cycles.

Utilization of 'elemental' sulfur by different phototrophic sulfur bacteria (Chromatiaceae, Ectothiorhodospiraceae): A sulfur K-edge XANES spectroscopy study

Phototrophic sulfur bacteria are generally able to use elemental sulfur as an electron donor for anoxygenic photosynthesis. Elemental sulfur is mainly a mixture of cyclo-octasulfur and polymeric sulfur. The purple sulfur bacterium Allochromatium vinosum strongly prefers the polymeric sulfur fraction showing that sulfur speciation has a strong influence on availability of elemental sulfur. X-ray absorption near edge structure (XANES) spectroscopy was used to investigate whether polymeric sulfur is also the preferred sulfur species in other purple sulfur bacteria belonging to the families Chromatiaceae and Ecothiorodospiraceae. The cultures were fed with 50 mM of elemental sulfur consisting of 68% polymeric sulfur and 30% cyclo-octasulfur. In all cultures, elemental sulfur was converted into intra- or extracellular sulfur globules, respectively, and further oxidized to sulfate. Sulfate concentrations were determined by HPLC and turbidometric assays, respectively. However, the added elemental sulfur was only partly used by the bacteria, one part of the 'elemental sulfur' remained in the cultures and was not taken up. XANES spectroscopy revealed that only the polymeric sulfur fraction was taken up by all cultures investigated. This strongly indicates that polymeric 'chain-like' sulfur is the form preferably used by phototrophic sulfur bacteria.

Nitrite, an Electron Donor for Anoxygenic Photosynthesis

We report a previously unknown process in which anoxygenic phototrophic bacteria use nitrite as an electron donor for photosynthesis. We isolated a purple sulfur bacterium 98% identical to Thiocapsa species that stoichiometrically oxidizes nitrite to nitrate in the light. Growth and nitrate production strictly depended on both light and nitrite. This is the first known microbial mechanism for the stoichiometric oxidation of nitrite to nitrate in the absence of oxygen and the only known photosynthetic oxidation in the nitrogen cycle. This work demonstrates nitrite as the highest-potential electron donor for anoxygenic photosynthesis known so far.

Utilization of solid ‘elemental’ sulfur by the phototrophic purple sulfur bacterium Allochromatium vinosum: a sulfur K-edge X-ray absorption spectroscopy study

The purple sulfur bacterium Allochromatium vinosum can use elemental sulfur as an electron donor for anoxygenic photosynthesis. The elemental sulfur is taken up, transformed into intracellular sulfur globules and oxidized to sulfate. Commercially available "elemental" sulfur usually consists of the two species cyclo-octasulfur and polymeric sulfur. The authors investigated whether only one sulfur species is used or at least preferred when Alc. vinosum takes up elemental sulfur and forms globules. To this end, Alc. vinosum was cultivated photolithoautotrophically with two types of elemental sulfur that differed in their cyclo-octasulfur : polymeric sulfur ratio, as well as with pure polymeric sulfur. Sulfur speciation was analysed using X-ray absorption spectroscopy, and sulfate contents were determined by HPLC to quantify the amount of elemental sulfur being taken up and oxidized by Alc. vinosum. The results show that Alc. vinosum uses only the polymeric sulfur (sulfur chain) fraction of elemental sulfur and is probably unable to take up and form sulfur globules from cyclo-octasulfur. Furthermore, direct cell-sulfur contact appears to be necessary for uptake of elemental sulfur by Alc. vinosum.

Rhodovulum iodosum sp. nov. and Rhodovulum robiginosum sp. nov., two new marine phototrophic ferrous-iron-oxidizing purple bacteria.

Two new strains of marine purple bacteria, N1T and N2T, were isolated from coastal sediment of the North Sea (Germany) with ferrous iron as the only electron donor for anoxygenic photosynthesis. The isolates are the first salt-dependent, ferrous-iron-oxidizing purple bacteria characterized so far. Analysis of 16S rRNA gene sequences revealed an affiliation with the genus Rhodovulum, which until now comprises only marine species. The sequence similarity of both strains was 95.2%, and their closest relative was Rhodovulum adriaticum. Like all known Rhodovulum species, the new strains had ovoid to rod-shaped cells, contained bacteriochlorophyll a and carotenoids of the spheroidene series, and were able to oxidize sulfide and thiosulfate. Like Rhodovulum adriaticum, both strains were unable to assimilate sulfate; for growth they needed a reduced sulfur source, e.g. thiosulfate. In contrast to the new strains, none of the known Rhodovulum species tested was able to oxidize ferrous iron or iron sulfide. In growth experiments, strains N1T and N2T oxidized 65 and 95%, respectively, of the ferrous iron supplied. Electron diffraction analysis revealed ferrihydrite as the main product of ferrous iron oxidation. In addition, traces of magnetite were formed. Strains N1T (= DSM 12328T) and N2T (= DSM 12329T) are described as Rhodovulum iodosum sp. nov. and Rhodovulum robiginosum sp. nov., respectively.

Ferrous iron oxidation by anoxygenic phototrophic bacteria

NATURAL oxidation of ferrous to ferric iron by bacteria such as Thiobacillus ferrooxidans or Gallionella ferruginea1, or by chemical oxidation2,3 has previously been thought always to involve molecular oxygen as the electron acceptor. Anoxic photochemical reactions4–6 or a photobiological process involving two photosystems7–9 have also been discussed as mechanisms of ferrous iron oxidation. The knowledge of such processes has implications that bear on our understanding of the origin of Precambrian banded iron formations10–14. The reducing power of ferrous iron increases dramatically at pH values higher than 2–3 owing to the formation of ferric hydroxy and oxyhydroxy compounds1,2,15 (Fig. 1). The standard redox potential of Fe3+/Fe2+ (E0 = +0.77 V) is relevant only under acidic conditions. At pH 7.0, the couples Fe(OH)3/Fe2+ (E′0 = -0.236V) or Fe(OH)3 + HCO−3FeCO3 (E′0 = +0.200 V) prevail, matching redox potentials measured in natural sediments9,16,17. It should thus be possible for Fe(n) around pH 7.0 to function as an electron donor for anoxygenic photosynthesis. The midpoint potential of the reaction centre in purple bacteria is around +0.45 V (ref. 18). Here we describe purple, non-sulphur bacteria that can indeed oxidize colourless Fe(u) to brown Fe(in) and reduce CO2 to cell material, implying that oxygen-independent biological iron oxidation was possible before the evolution of oxygenic photosynthesis.

Sulfide-induced sulfide-quinone reductase activity in thylakoids of Oscillatoria limnetica.

Sulfide-dependent partial electron-transport reactions were studied in thylakoids isolated from cells of the cyanobacterium Oscillatoria limnetica, which had been induced to perform sulfide-driven anoxygenic photosynthesis. It was found that these thylakoids have the capacity to catalyze electron transfer, from sulfide to externally added quinones, in the dark. Assay conditions were developed to measure the reaction either as quinone-dependent sulfide oxidation (colorimetrically) or as sulfide-dependent quinone reduction (by UV dual-wavelength spectrophotometry). The main features of this reaction are as follows. (i) It is exclusively catalyzed by thylakoids of sulfide-induced cells. Noninduced thylakoids lack this reaction. (ii) Plastoquinone-1 or -2 are equally good substrates. Ubiquinone-1 and duroquinone yield somewhat slower rates. (iii) The apparent Km for plastoquinone-1 was 32 microM and for sulfide about 4 microM. Maximal rates (at 25 degrees C) were about 75 mumol of quinone reduced per mg of chlorophyll.h. (iv) The reaction was not affected by extensive washes of the membranes. (v) Unlike sulfide-dependent NADP photoreduction activity of these thylakoids, which is sensitive to all the specific inhibitors of the cytochrome b6f complex, the new dark reaction exhibited differential sensitivity to these inhibitors. 2-n-Nonyl-4-hydroxyquinoline-N-oxide was the most potent inhibitor of both light and dark reactions, working at submicromolar concentrations. 5-n-Undecyl-6-hydroxy-4,7-dioxobenzothiazole also inhibited the two reactions to a similar extent, but at 10 times higher concentrations than 2-n-nonyl-4-hydroxyquinoline-N-oxide. 2,5-Dibromo-3-methyl-6-isopropyl-p-benzoquinone, 2-iodo-6-isopropyl-3-methyl-2',4,4'-trinitrodiphenyl ether, and stigmatellin had no effect on the dark reaction at concentrations sufficient to fully inhibit the light reaction from sulfide. We propose that the sulfide-induced factor which enables the use of sulfide as the electron donor for anoxygenic photosynthesis in Oscillatria limnetica is a membrane-bound sulfide-quinone reductase. Its site of interaction is suggested to be either the cytochrome b6 (at the Qc quinone binding site or the bH site) or the plastoquinone pool. The analogy to other anoxygenic photosynthetic systems is discussed.