Fumarate respiration

The adaptation to an anaerobic lifestyle with the aid of hydrogenosomes required the acquisition of an (oxygen-sensitive) hydrogenase. The evolution of fumarate respiration in N. ovalis shows that an adaptation to life in anaerobic environments can occur in steps - by evolutionary tinkering. 

Such a metabolism ( fumarate respiration ) is well known from anaerobic mitochondria (Tielens et al. 2002 Tielens and van Hellemond, Chap. 6 in this volume), but is unique in combination with a hydrogenase that might compete with the fumarate reductase for the same substrates. This hydrogenase of N. ovalis represents a novel type of [Fe]-only or [FeFe]-hydrogenase that allows H2 formation to be coupled directly to the reoxidation of NADH. The [Fe]-hydrogenase is linked covalently with a protein, which possesses NAD and FMN binding sites, and a ferredoxin-like FeS module that allows transfer... 

Cells of W. succinogenes catalyzing Reactions (6) or (7) were found to take up tetraphenylphosphonium (TPP" ) form the external medium [20,21]. TPP uptake was prevented by the presence of a protonophore. From the amount of TPP" " taken up, the (0.17 V) was calculated to be approximately the same as that generated by fumarate respiration with formate [Reaction (8)] (Table 2). 

The values of and Ap were nearly the same, since the ApH across the membrane was negligible. The H"7e and the ATP/e ratios were determined for fumarate respiration but not for polysulfide sulfur respiration. 

Table 2 Bioenergetic Data of the Polysulfide Sulfur Respiration with Formate of W. succinogenes [2], The Data are Compared to Those of Fumarate Respiration...

However, the values for polysulfide respiration can be estimated from the growth yields (Y) of W. succinogenes growing at the expense of Reactions (7) and (8). The growth yield of poly sulfide sulfur respiration was measured to be approximately half that of fumarate respiration, suggesting that the and... 

ATP/e ratio of polysulfide sulfur respiration was also half that of fumarate respiration [1]. This view is confirmed by the redox potential differences (AE) between formate and each of the two electron acceptors under the growth conditions of the bacteria. The AE of polysulfide sulfur respiration is approximately half that of fumarate respiration. The firee energy required for ATP synthesis calculated from AE and the ATP/e ratios are 116 and 127 kJ mol in anaerobic respiration with polysulfide sulfur and fumarate, respectively. Both values are consistent with the general observation that phosphorylation requires about 100 kJ moP ATP in growing bacteria in most instances. 

Proteoliposomes containing polysulfide reductase and either hydrogenase or formate dehydrogenase isolated from W. succinogenes do not catalyze polysulfide sulfur respiration unless 8-methyl-menaquinone is present (Table 3). Menaquinone with a side chain consisting of six or four isoprene units, or vitamin Ki served in reconstituting fumarate respiration, but did not replace 8-methyl-menaquinone in polysulfide sulfur respiration. The low activities of polysulfide sulfur respiration observed without added 8-methyl-menaquinone were probably due to the small amounts of this quinone associated with the enzyme preparations used. Maximum activity of polysulfide sulfur respiration required 10 p.mol 8-methyl-menaquinone per gram phospholipid [O. Klimmek and W. Dietrich, unpublished results]. 

Kroger A, Biel S, Simon J, Gross R, Unden G, Lancaster CRD. Fumarate respiration of Wolinella succinogenes, enzymology, energetics, and coupling mechanism. Biochim Biophys Acta 2002 1553 23-38. 

Escherichia coli kl2 (fumarate-respiring) glycerol carbon tetrachloride [79]... 

Figure 18.2 Summary of respiratory energy flows. Foods ate converted into the reduced form of nicotinamide adenine dinucleotide (NADH), a strong reductant, which is the most reducing of the respiratory electron carriers (donors). Respiration can he based on a variety of terminal oxidants, such as O2, nitrate, or fumarate. Of those, O2 is the strongest, so that aerobic respiration extracts the largest amount of free energy from a given amount of food. In aerobic respiration, NADH is not oxidized directly by O2 rather, the reaction proceeds through intermediate electron carriers, such as the quinone/quinol couple and cytochrome c. The most efficient respiratory pathway is based on oxidation of ferrocytochrome c (Fe ) with O2 catalyzed by cytochrome c oxidase (CcO). Of the 550 mV difference between the standard potentials of c)Tochrome c and O2, CcO converts 450 mV into proton-motive force (see the text for further details).

Effect of FCH2COONa (3-3 mM) on lddney homogenate respiring in presence of sodium fumarate (Mg and A.T.P. added)... 

The first suggestion that substrates in carbohydrate oxidation might exert catalytic effects on the oxidation of other intermediates (cf.earlier demonstration of such action in the urea cycle by Krebs and Henseleit, 1932 see Chapter 6) arose from the work of Szent-Gyorgi (1936). He demonstrated that succinate and its 4C oxidation products catalytically stimulated the rate of respiration by muscle tissues. He also observed that reactions between the 4C intermediates were reversible and that if muscle was incubated with oxaloacetate, fumarate and malate made up 50-75% of the products, 2-oxoglutarate 10-25% and, significantly, 1-2% of the C was converted to citrate. These observations were... 

In the next 2 to 3 years further experiments, particularly by Eggleston, who had joined Krebs in January 1936, confirmed and extended the observations. Careful quantitative evaluation of the data indicated that citrate like fumarate (Szent-Gyorgi) and like ornithine in the urea cycle exerted a catalytic effect on muscle metabolism. If arsenite, which blocks 2-oxoglutarate oxidation, was added with citrate to a respiring pigeon-muscle preparation, 2-oxoglutarate accumulated. 

Fumarate is able to serve as an electron acceptor in anaerobic respiration, as it may be reduced reversibly to succinate in a two-electron process. The succinate-fumarate couple may therefore be utilized as an oxidant or reductant in the respiratory chain, and so differs from the other examples given in this section. These two reactions are catalyzed by succinate dehydrogenase and fumarate reductase, which have many similarities in subunit structure. These are shown in Table 29. Although they are different enzymes, the fumarate reductase can substitute for succinate dehydrogenase under certain conditions. The synthesis of succinate dehydrogenase is induced... 

Organisms with anaerobic mitochondria can be divided into two different types those which perform anaerobic respiration and use an alternative electron acceptor present in the environment, such as nitrate or nitrite, and those which perform fermentation reactions using an endogenously produced, organic electron acceptor, such as fumarate (Martin et al. 2001 Tielens et al. 2002). An example of the first type is the nitrate respiration that occurs in several ciliates (Finlay et al. 1983), and fungi (Kobayashi et al. 1996 Takaya et al. 2003), which use nitrate and/or nitrite as the terminal electron acceptor of their mitochondrial electron-transport chain, producing nitrous oxide as... 

The vast majority of mitochondria use oxygen as a terminal acceptor of electrons. Along with aerobically respiring mitochondria, versatile mitochondria exist in which both oxygen and other oxidized compounds, e.g. fumarate and nitrate, serve as electron acceptors. Such sophisticated mitochondria were reported in several ciliates, fungi, and even lower animals (Tielens et al. 2002). The yield of ATP is, however, much lower in the cases of anaerobic respiration, as compared with 32-36 mol per mole of glucose produced by aerobic respiration (Saraste 1999). 

Fumaric acid is a naturally occurring sour-tasting compound found in many plants such as Fumaria officinalis L. (Fumariaceae), Boletus scaber Bull. (Boletaceae), and Fames igniaries (Fries) Kickx. (Pluporaceae). It is an essential component for respiration in plant and animal tissues. It is produced by fermentation with mold, such as Rhizopus nigricans, or by chemical synthesis. It is also used in soft drinks and ice cream and as an acidulant along with citric acid. 

SQR (respiratory complex II) is involved in aerobic metabolism as part of the citric acid cycle and of the aerobic respiratory chain (Saraste, 1999). QFR participates in anaerobic respiration with fumarate as the terminal electron acceptor (Kroger, 1978 Kroger etal., 2002) and is part of the electron transport chain catalyzing the oxidation ofvarious donor substrates (e.g., H2 or formate) by fumarate. These reactions are coupled via an electrochemical proton potential (Ap) to ADP phosphorylation with inorganic phosphate by ATP synthase (Mitchell, 1979). 

Fig. 9. The coupling of electron and proton flow in succinate iquinone oxidoreduc-tases in aerobic (a,c) and anaerobic respiration (b,d), respectively. Positive and negative sides of the membrane are as described for Fig. 1. (a) and (b) Electroneutral reactions as catalyzed by C-type SQR enzymes (a) and D-type E. coli QFR (b). (c) Utilization of a transmembrane electrochemical potential Ap as possibly catalyzed by A-type and B-type enzymes, (d) Electroneutral fumarate reduction by B-type QFR enzymes with a proposed compensatory E-pathway. ...

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