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Microbial Physiology. Albert G. Moat, John W. Foster and Michael P. Spector Copyright¶ 2002 by Wiley-Liss, Inc. ISBN: 0-471-39483-1 CHAPTER 12 PHOTOSYNTHESIS AND INORGANIC METABOLISM Organisms that use C1 compounds (e.g., CO2 or CH4) as their major or sole source of carbon and energy are called autotrophs. Methylotrophs use methane (CH4) or methanol (CH3OH) as their sole source of carbon. Autotrophic organisms that use light as a source of energy are photoautotrophs. The source of utilized energy serves as a physiological distinction, as shown in Table 12-1. CHARACTERISTICS AND METABOLISM OF AUTOTROPHS Photosynthetic Bacteria and Cyanobacteria Most living forms on earth are ultimately dependent on the process of photosynthesis. This process occurs in green plants, algae, cyanobacteria, and photosynthetic bacteria. A large community of marine microorganisms, generally referred to as phytoplankton, contains many species of cyanobacteria (representative examples: Prochlorococcus, Synechococcus,andAnabaena) that comprise the largest population of photosynthetic organisms on the planet. Many plants and microorganisms also conduct nitrogen fixation (see Chapter 14), providing a basis of continuity for all other life. Some reactions in the photosynthetic process are quite slow and inefficient. Therefore, one major aspect of the study of photosynthetic organisms is the improvement of the efficiency of the process through genetic engineering. Photosynthetic bacteria are found in the deeper waters of permanently stratified (meromictic) lakes where the conditions are anaerobic, but light is available. Differentiation between the photosynthetic bacteria and the cyanobacteria (some- times referred to in the past as blue-green algae) is based on the type of photosensitive pigments produced. Prokaryotes such as the cyanobacteria (Anabaena, Synechococcus, Prochlorococcus) that conduct true photosynthesis contain chlorophyll a,whichis common to the eukaryotic algae and green plants. Water serves as the electron 434 CHARACTERISTICS AND METABOLISM OF AUTOTROPHS 435 TABLE 12-1. Principal Groups of Autotrophs Energy Source Group Genera H2 Hydrogen bacteria Ralstonia (formerly Alcaligenes), Nocardia, Xanthobacter, Pseudomonas derxia NH3 Nitrifying bacteria Nitrosolobus, Nitrosomonas, Nitrocystis NO2 Nitrifying bacteria Nitrobacter, Nitrospina, Nitrosococcus N2 Nitrogen-fixing bacteria Azotobacter, Anabaena, Prochlorococcus, Rhizobium 2− H2S, S, S2O3 Sulfur bacteria Thiobacillus, Sulfolobus, Desulfotomaculum, Wolinella, Desulfovibrio, Beggiatoa Fe2+ Iron bacteria Gallionella, Sphaerotilus, Thiobacillus ferrooxidans, Leptothrix, Shewanella oneidensis CH4,CH3OH Methylotrophs Hyphomicrobium, Methylomonas, Methylobacterium, Methylosinus, Paracoccus, Pseudomonas H2,CO2, Methanogens Methanobacterium, Methanobrevibacter, Formate Methanococcus, Methanomicrobium, Methylamine Methogenium, Methanospirillum, Trimethylamine Methanosarcina Acetate Light Phototrophs Rhodobacter, Anabaena, Prochlorococcus, Synechococcus, algae donor and oxygen is generated by photolysis. The purple bacteria (Thiorhodaceae) contain bacteriochlorophyll a or b.TheThiorhodaceae utilize H2S and/or inorganic compounds as electron donors, and their metabolism does not involve molecular oxygen (i.e., it is anaerobic). Green bacteria (Chlorobacteriaceae) contain bacteriochloro- phyll c or d and small amounts of bacteriochlorophyll a,usingH2S and/or organic compounds as electron donors and following anaerobic metabolic pathways. The struc- ture and biosynthesis of bacteriochlorophyll has been studied in detail and is discussed in Chapter 15. Production of light-absorbing carotenoid pigments also represents a differentiating characteristic. All algae and green plants contain β-carotene. The purple sulfur and nonsulfur bacteria contain a variety of carotenoid pigments of both aliphatic and aryl types, whereas the green bacteria contain only aryl carotenoids (Fig. 12-1). The carotenoid pigments absorb light energy and transfer it to the chlorophyll molecules of the antenna. Algae and the cells of higher plants contain chloroplasts. Comparable struc- tures (chromatophores) are observed in the photosynthetic bacteria. The photo- synthetic apparatus of Rhodococcus sphaeroides consists of a series of intracy- toplasmic membranes (ICMs) that appear as vesicular invaginations originating from the cytoplasmic membrane. R. sphaeroides carries out anoxigenic photosyn- thesis but is also capable of both aerobic and anaerobic respiration as well as fermentation. 436 PHOTOSYNTHESIS AND INORGANIC METABOLISM Alicyclic, b-carotene, algae, green plants Aliphatic, lycopene, purple bacteria Aryl, isorenieratene, green bacteria Fig. 12-1. Examples of carotenoid pigments produced by plants, algae, and photosynthetic bacteria. Although there are many variations, all carotenoids are of one of these three basic types. The Chlorobacteriaceae (green bacteria) contain vesicles enclosed within a thin nonunit membrane that is not directly associated with the cell membrane. Metabolically, the green bacteria are strict anaerobic organisms that are obligately photosynthetic. They utilize H2S, thiosulfate, or H2 as an electron donor and CO2 as the carbon source: CO2 + 2H2S + light −−−→ (CH2O) + H2O + 2S 2CO2 + 2Na2S2O3 + 3H2O + light −−−→ 2(CH2O) + 2NaHSO4 CO2 + 2H2 + light −−−→ (CH2O) + H2O The purple bacteria contain two groups: the purple sulfur bacteria (Thiorhodaceae) that use H2S as an electron donor and the purple nonsulfur bacteria (Athiorhodaceae) that depend on organic compounds such as short-chain fatty acids for photosynthetic metabolism. Poly-β-hydroxybutyrate is the end product: CO2 + 2CH3CHOHCH3 + light −−−→ (CH2O) + H2O + 2CH3COCH3 2CH3COOH + 2CoASH −−−→ 2CH3COSCoA 2CH3COSCoA −−−→ CH3COCH2COSCoA + CoASH nCH3CHOHCH2COSCoA −−−→ (CH3CHOHCH2COOH)n + CoASH Poly-β-hydroxybutyrate serves as a major storage reserve material in these organisms. It is also an important reserve energy source in many other organisms. The cyanobacteria are considered to be very early evolutionary forms because of their lack of dependence on oxygen and on the basis of molecular evidence derived from 16S rRNA sequencing. Phylogenetic analysis of c-type cytochromes and rRNA sequences CHARACTERISTICS AND METABOLISM OF AUTOTROPHS 437 has established a relationship between cyanobacteria and the chloroplasts of green algae and higher plants. These lines of evidence provide support for the concept of prokaryotic origins of chloroplasts along similar lines of development attributed to mitochondria. Autotrophic CO2 Fixation and Mechanisms of Photosynthesis Photoautotrophs and chemoautotrophs, in which CO2 servesasthesoleorprincipal source of cellular carbohydrate, fix CO2 via either the reductive pentose phosphate pathway (Calvin) cycle or the reductive C4-dicarboxylic acid pathway. These systems were first discovered in green plants. Originally, all green plants were thought to assimilate atmospheric CO2 via the reductive pentose pathway (Fig. 12-2) in which phosphoglyceric acid (PGA) is the first stable product (hence the designation C3 plants). Subsequently, an alternative pathway of CO2 fixation was discovered in which C4 dicarboxylic acids (oxaloacetate and malate) were found as the primary products of photosynthesis. Within a taxonomic category, plants with C3 photosynthesis are considered to be ancestral to those with C4 primary photosynthetic products. In photosynthetic and autotrophic bacteria, CO2 fixation occurs primarily via the reductive pentose phosphate pathway (Fig. 12-2). In this system reduction of 1 mol of CO2 to the oxidation level of carbohydrate involves the oxidation of 2 mol of NADPH and the hydrolysis of 3 mol of ATP. Only two of the reactions, phosphoribulokinase and ribulose bisphosphate carboxylase (RuBisCO), are specific to photosynthetic or chemoautotrophic organisms. The other reactions are held in common with the carbohydrate metabolism of nonphotosynthetic organisms. The reductive pentose cycle constitutes the dark reaction of photosynthesis. Six turns of the cycle result in the synthesis of 1 mol of hexose (F-6-P): + 6CO2 + 6H2O + 18ATP + 12NADPH + 12H + −−−→ F-6-P + 18ADP + 12NADP + 17Pi The remainder is recycled through the reductive pathway as shown in Figure 12-2. The reductive C4-dicarboxylic acid pathway (Fig. 12-3) is present in a number of photosynthetic bacteria. In some organisms, such as the Chlorobium, it is the only cyclic pathway for CO2 assimilation. Organisms that use the C4 pathway possess the enzyme pyruvate-orthophosphate dikinase, which synthesizes phosphoenolpyruvate (PEP): ++ pyruvate + ATP + Pi + Mg −−−→ PEP + AMP + PPi This enzyme differs from the PEP synthase of E. coli and other bacteria that can utilize C4 acids in that it produces orthophosphate rather than monophosphate. Chlorobium thiosulfatophilum, a member of the green sulfur bacteria, requires Pi in addition to Mg++ and ATP for the formation of PEP from pyruvate, supporting the fact that in photosynthetic bacteria, such as C4 plants, pyruvate-orthophosphate dikinase rather than PEP synthase is used to form PEP in the photosynthetic assimilation of CO2.The reductive carboxylic acid cycle is essentially a reverse of the TCA cycle in which pyruvate oxidase and α-ketoglutarate oxidase systems are replaced by ferredoxin- dependent pyruvate synthetase and α-ketoglutarate synthetase. This system is also of major importance in the metabolism of anaerobic bacteria. 438 PHOTOSYNTHESIS AND INORGANIC METABOLISM COOH 6 CO2 2 HCOH | H COPO H 2 3 2
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