Carbon Metabolism of Phototrophic Prokaryotes

In the natural environment, the principal carbon source of phototrophic bacteria in many instances is CO2 (Madigan et al., 1989; Sinninghe Damste et al., 1993; Takahashi et al., 1990). In Cyanobacteria, Chromatiaceae, Ectothiorho-dospiraceae and purple nonsulfur bacteria, CO2 is assimilated by the reductive pentose phosphate or Calvin cycle. Employing this cycle, the formation of one molecule of glyceraldehyde-3-phosphate requires 6 NAD(P)H+H+ and 9 ATP. By comparison, the reductive tricarboxylic acid cycle used for CO2-assimilation by green sulfur bacteria requires 4 NADH+H+, 2 reduced ferre-doxins, and only 5 ATP. As two of the reactions of the reductive tricarboxylic acid cycle (the a-oxoglutarate synthase and pyruvate synthase rea ctions) require reduced ferredoxin as electron donor, this pathway of CO2 fixation can only proceed under strongly reducing conditions. Furthermore, reduced ferredoxin is a primary product of the light reaction only in FeS-type reaction centers. Ultimately, the lower demand for ATP is possible because of the adapatation of green sulfur bacteria to the strongly reducing conditions of their natural environment. CO2-fixation by the hydroxypropionate cycle in Chloroflexus aurantiacus requires 8 ATP per glyceraldehyde-3-phosphate and therefore is energetically less favorable than in green sulfur bacteria.

Organic carbon as it is present in canonical microbial biomass (<C4H8O2N>; Harder and van Dijken, 1976) is considerably more reduced than CO2. Given the high energy demand of autotrophic growth, the capability for assimilation of organic carbon compounds is of selective advantage especially if natural populations are limited by light or by low concentrations of electron-donating substrates, as is typically the case for phototrophic sulfur bacteria. At limiting concentrations of sulfide or thiosulfate, the cell yield of green sulfur bacteria is increased three times if acetate is available as an additional carbon source (Overmann and Pfennig, 1989b). Acetate represents one of the most important intermediates of anaerobic degradation of organic matter (Wu et al., 1997). That almost all anoxygenic phototrophic bacteria (with the exception of Rhodopila globiformis; Imhoff and Truper, 1989) are capable of acetate assimilation is therefore not surprising. In most phototrophic Proteobacteria, acetate is assimilated by acetyl-CoA synthetase and the enzymes of the glyoxylate cycle. In green sulfur bacteria, the ferredoxin-dependent pyruvate synthetase, PEP synthetase, and reactions of the reductive tricar-boxylic acid cycle serve this purpose. The capacity for organotrophic growth seems to correlate with the presence of a-oxoglutarate dehydroge-nase. The latter is a key enzyme for the complete oxidation of the carbon substrates in the tricarboxylic acid cycle (Kondratieva, 1979), whereas a complete cycle is not needed for the photoassimilation during the presence of inorganic electron donors. The range of carbon substrates utilized and the capacity for photoorganotrophy or chemoorganotrophy varies considerably among the different groups of phototrophic pr okaryotes (Pfennig and Truper, 1989).

Organic carbon compounds not only are assimilated but also can serve as photosynthetic electron donors in purple nonsulfur bacteria, some Chromatiaceae and Ectothiorhodospi-raceae, all Heliobacteriaceae, and members of the Chloroflexus subdivision.

Green sulfur bacteria are the least versatile of all phototrophic prokaryotes. All known species are obligately photolithotrophic and assimilate only very few simple organic carbon compounds (acetate, propionate, pyruvate). Few strains have been shown to assimilate fructose or glutamate. Whereas green sulfur bacteria have a higher growth affinity for sulfide than purple sulfur bacteria, acetate seems to be used by purple sulfur bacteria at an affinity 30 times higher than in green sulfur bacteria (Veldhuis and van Gemer-den, 1986). In addition, uptake of acetate in Chlorobium phaeobacteroides is inhibited by light (Hofman et al., 1985).

Based on their metabolic flexibility, two groups can be distinguished among the Chromatiaceae. Several species (Chromatium okenii, Chr. weissii, Chr. warmingii, Chr. buderi, Chr. tepidum, Thiospirillum jenense, Lamprocystis roseopersic-ina, Thiodictyon elegans, Thiodictyon bacillo-sum, Thiocapsa pfennigii, Thiopedia rosea) are obligately phototrophic, strictly anaerobic and photoassimilate acetate and pyruvate only in the presence of CO2 and sulfide. Assimilatory sulfate reduction is absent in these species (Pfennig and Truper, 1989). However, particularly those species with limited metabolic flexibility form dense blooms under natural conditions (see Coexistence of Phototrophic Sulfur Bacteria in this Chapter). The second physiological group within the Chromatiaceae comprises the small Chroma-tium species (Chr. gracile, Chr. minus, Chr. minutissimum), Allochromatium vinosum, Lamprobacter modestohalophilus, as well as Thiocystis spp., Thiocapsa. Most of these species use thiosulfate as electron donor and a wide range of organic carbon compounds including glucose, fructose, glycerol, fumarate, malate, succinate, formate, propionate, and butyrate for photoassimilation, and often are capable of assimilatory sulfate reduction. In some species (especially Allochromatium vinosum), these organic carbon substrates also serve as electron-donor for phototrophic or chemotrophic growth.

Most Ectothiorhodospiraceae species are capable of photoorganotrophic growth, with Ectothiorhodospira halophila and Ectothiorho-dospira halochloris being the exceptions. The spectrum of electron-donating carbon substrates for photoorganotrophic growth resembles that found in the versatile Chromatium species (Pfennig and Truper, 1989). Assimilation of acetate and propionate proceeds by carboxylation and therefore depends on the presence of CO2.

Chloroflexus aurantiacus grows preferably by photoorganoheterotrophy (Pierson and Casten-holz, 1995). The carbon substrates utilized comprise acetate, pyruvate, lactate, butyrate, C4-dicarboxylic acids, some alcohols, sugars and amino acids (glutamate, aspartate). This versatility has been seen as the major cause for the profuse growth of Chloroflexus in microbial mats where accompanying microorganisms, especially cyanobacteria, may provide the required carbon substrates (Sirevag, 1995). However, high rates of formation of low-molecular-weight organic carbon substrates by the anaerobic food chain have also been observed in other stratified systems, where the dominating anoxygenic pho-totrophs could utilize only a narrow range of carbon substrates (Overmann, 1997; Overmann et al., 1996). The refore, the presence of low-molecular-weight organic carbon substrates is not necessarily the most selective factor in the natural environment.

Slow photolithoautotrophic growth with H2S or H2 as electron-donating substrates has been shown in laboratory cultures of Chloroflexus aurantiacus and in hot spring populations (Pier-son and Castenholz, 1995). Carbon fixation proceeds by carboxylation of acetyl-CoA and via hydroxypropionyl-CoA as an intermediate and yields glyoxylate as the net product (hydroxypro-pionate cycle; Holo, 1989; Strauß and Fuchs, 1993; Eisenreich et al., 1993). So far this cycle has not been found in any other member of the Bacteria. Glyoxylate is further assimilated into cell material with tartronate semialdehyde and 3-phosphoglycerate as intermediates (Menendez et al., 1999).

The highest metabolic versatility is found in phototrophic a- and ß-Proteobacteria (purple nonsulfur bacteria). All representatives grow photoorganoheterotrophically and (with the exception of Blastochloris viridis) photolithoau-totrophically with H2 in the light. In addition to the substrates used by versatile purple sulfur bacteria, the spectrum of substrates that can serve as electron donors comprise long-chain fatty acids (like pelargonate), amino acids (aspartate, arginine, glutamate), sugar alcohols (sorbitol, mannitol), or aromatic compounds (benzoate; Imhoff and Trüper, 1989). With the exception of Rubrivivax gelatinosus, none of the purple non-sulfur bacteria is capable of degradation of polymers and therefore depends on the anaerobic food chain for the supply of electron-donating substrates required for growth. This dependence and the competition with chemotrophs for the carbon substr ates might be the major reason why dense blooms of purple nonsulfur bacteria do not occur under natural conditions (see Habitats of Phototrophic Prokaryotes in this Chapter). Some species are capable of also using reduced sulfur compounds as electron donors. However, most species oxidize sulfide to elemental sulfur only (Hansen and van Gemerden, 1972).

In Heliobacteriaceae, only a limited number of carbon substrates can serve as photosynthetic electron donor including pyruvate, ethanol, lac-tate, acetate, and butyrate. High levels of sulfide are inhibitory (Madigan, 1992; Madigan and Ormerod, 1995).

Cyanobacteria are obligate autotrophs par excellence; however, small molecular weight organic compounds such as acetate, sugars and amino acids are assimilated. In the case of amino acids, the presence of various efficient uptake systems has been interpreted as a means of recovery of leaked organic nitrogen, rather than a true chemotrophic capability (Montesinos et al., 1997). Certain strains of cyanobacteria can grow facultatively as chemoheterotrophs in the dark (Rippka et al., 1979), but even under these conditions all of the photosynthetic machinery is synthesized. This lack of regulation implies that chemotrophy has played no significant evolutionary role in these organisms.

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