Coupled Oxidative Phosphorylation

A . Y I E L D OP " E N E R G Y - R I C H " PHOSPHATE ( ~ P )

I n order t o serve t h e energy requirements of t h e cell, energy released in oxidative reactions must be conserved in some biologically available form.

E q u a t i o n (23) is a general formulation for t h e coupling between oxidation a n d energy-trapping reactions. I n this reaction, the free energy of

theoxida-A H² + Β + wADP + wP0⁴ —• A + B H² + nATP + n H²0 (23) tion, or a portion of it, is conserved in the "high-energy" bond of adenosine triphosphate ( A T P ) . * T h e mechanisms of A T P utilization cannot be re­

viewed here. T h e reader is referred t o t h e review of Krebs and Kornberg.^{2 2} T h e yield of ~ P in equation (23) depends upon t h e AF of t h e reaction (voltage span between A H² and B) and upon t h e number of energy con­

servation steps t h a t m a y be available between A H² a n d B . W h e n Β is 0², results are usually reported as P / O ratios, t h a t is, equivalents of phosphate esterified per a t o m of oxygen taken u p (i.e., per 2 H oxidized). T h e integral value of t h e ratio is sometimes taken as t h e number of points a t which mechanisms for phosphate esterification exist. Figure 8 shows t h e probable yield of ~ P , based on experiments with animal mitochondria,^{2 2}* ^{1 7 9} for electron transport between various members of the respiratory chain [vari­

ous pairs of A H² and Β in equation (23)]. Comparison of the respiratory chain sequence with the dehydrogenation potentials of various substrate

* The term "high-energy bond" has been criticized as being misleading.^{1 7 8} The free energy released on hydrolysis of a "high-energy" compound is not contained in any one bond, but is a statistical property of the system, being defined by equa­

tion 18. In the text, the symbol ~ P is used for convenience. At pH 7, AF' for the hydrolysis of ATP is approximately — 7900 cal., whereas under the conditions used in oxidative phosphorylation studies, the best approximation for AF' at pH 7 is probably

-12,000 cal.^{1 7 8 a}

356 Μ . I . D O L I N

systems indicates t h e total a m o u n t of phosphate esterification t h a t m a y theoretically be expected for t h e one-step oxidation (one pair of hydrogens transferred) of typical substrates. Oxidation of carbonyl groups t o carboxyl groups, with D P N as electron acceptor, can be coupled with the formation of a n energy-rich bond (without need for further hydrogen transfer reac­

tions). During glucose oxidation via t h e glycolytic p a t h w a y a n d the tri­

carboxylic acid cycle, this reaction occurs upon t h e reduction of D P N b y glyceraldehyde-3-phosphate, pyruvate, a n d α-ketoglutarate.^{2 2} T h e oxidation of p y r u v a t e and α-ketoglutarate b y various bacteria^{1 1 0} and of acetaldehyde b y C. kluyveri¹*⁰ offer further examples of this energy-coupled oxidation.

This reaction is usually termed "substrate-linked phosphorylation," to distinguish it from t h e respiratory chain phosphorylation t h a t accompanies t h e reoxidation of D P N H . Substrate-linked phosphorylation is not sensitive t o dinitrophenol, whereas respiratory chain phosphorylation is uncoupled b y this reagent (i.e., phosphorylation is abolished, b u t oxygen u p t a k e is either not affected or somewhat stimulated). T h e mechanism of substrate-linked phosphorylation is reasonably well understood; several acyl esters m a y occur as intermediates.^{2 2}

Phosphate esterification coupled to true electron transport through the respiratory chain is a characteristic property of mitochondria.³ W i t h ani­

mal mitochondrial systems, t h e reoxidation of D P N H , with oxygen as ac­

ceptor yields, experimentally, 3 ~ Ρ for a two-electron transfer (Fig. 8).

Two of the phosphorylations can be obtained with cytochrome c as ac­

ceptor and one in t h e reoxidation of cytochrome c b y o x y g e n .^{2 2}-^{1 7 9} T h e ­ oretically, one might expect t h a t t h e step from D P N H t o cytochrome c would yield one ^ P between D P N H a n d flavoprotein, and a second ~ P in the reoxidation of reduced flavoprotein b y cytochrome c. Such partial reactions have not been demonstrated to date. T h e oxidation of succinate b y O2 yields two ~ P , in keeping with the predictions t h a t would be m a d e from schemes such as t h a t of Figure 8. I n spite of much work, t h e intimate mechanism of respiratory chain phosphorylation is still not understood.

There is, however, increasing evidence t h a t vitamin Ki functions in both electron transport and oxidative phosphorylation in b a c t e r i a l^{1 2 , 8 9} and m a m ­ malian s y s t e m s .^{1 0 , 1 1} ·^{8 5} I t has also been suggested t h a t α-tocopherol m a y function in oxidative phosphorylation.^{1 4} Mechanisms for t h e mediation of phosphate transfer to A D P via vitamin Κ ι^{1 8 1}·^{1 8 2} and α-tocopherol^{1 4} h a v e been suggested.

T h e free energy of D P N H oxidation, with oxygen as acceptor, is —52,000 cal. Since, under t h e experimental conditions used for P / O determinations, t h e AF for A T P hydrolysis (pH 7) is approximately - 1 2 , 0 0 0 cal.,^{1 7 8} t h e efficiency of D P N H oxidation, as carried out b y animal mitochrondria, is approximately 70 %.

6. MICROBIAL ELECTRON TRANSPORT MECHANISMS 357

B . BACTERIAL SYSTEMS

Respiratory particles capable of catalyzing coupled oxidative phosphoryl­

ation have been isolated from several bacterial species including Alcaligenes faecalis*** M. phlei¹²'¹⁸⁸ and Azotobacter vinelandii.^{Ut 1 8 4} ·^{1 8 6} T h e Azotobacter and A. faecalis systems differ somewhat from mammalian mitochondria in

(1) being less sensitive to dinitrophenol and (2) exhibiting lower P / O ratios for t h e oxidation of typical substrates. With M. phlei succinate oxidation results in P / O ratios approaching those found for mammalian systems and the phosphorylation is sensitive to typical uncoupling agents. D P N H oxida­

tion b y preparations from Azotobacter^y A. faecalis, or M. phlei yields P / O ratios approaching 1, whereas with mammalian mitochondria t h e probable ratio is 3 a n d directly observed values as high as 2.6 have been obtained.^{1 7 9} I t is not clear whether this situation reflects a real difference between bac­

terial a n d mammalian systems (i.e., whether some bacterial respiratory particles h a v e fewer loci for coupled oxidative phosphorylation) or whether optimum conditions have not as y e t been found for the demonstration of oxidative phosphorylation with D P N H as substrate in bacterial systems.

A promising feature of several of t h e bacterial systems is t h e finding t h a t oxidative phosphorylation can be shown to require soluble proteins in ad­

dition to the respiratory particles.

I n Μ. phlei, a soluble protein seems t o be t h e dinitrophenol-sensitive component of t h e phosphorylation system.^{1 8 6}* T h e over-all reaction has also been shown t o require a naphthoquinone.^{1 2} Irradiation of particles and soluble supernatant components a t 3600 A. leads t o inactivation of both oxidation and phosphorylation; these activities are restored to t h e normal level b y the physiologically occurring naphthoquinone t h a t has been iso­

lated from Μ. pAfei.^{1 8 e b} Vitamin Ki is less effective.^{1 2} F M N can restore the oxidation b u t not t h e ability to couple oxidation to phosphorylation. Similar ultraviolet inactivations, reversible b y vitamin Κ ι, have been demonstrated for animal mitochondria.^{1 1} Stimulation of oxidation a n d phosphorylation b y soluble proteins has also been demonstrated for A. vinelandii^u a n d A.

faecalis.*** I n t h e latter system, there appears t o be a n additional require­

m e n t for a polynucleotide of t h e R N A type. Little information is available concerning phosphorylation coupled t o electron transport in bacteria which use inorganic electron donors or acceptors. With intact cells, phosphate turnover studies suggest t h a t oxidative phosphorylation m a y occur when nitrate is t h e electron acceptor for formate oxidation b y E. colt¹*⁷ or when oxygen serves as acceptor for t h e oxidation of sulfur compounds b y thio-bacilli.^{1 8 8}

I n several bacteria, high-molecular weight polyphosphates (metaphos-phate) previously identified histologically as metachromatic granules or volutin g r a n u l e s¹-^{1 8 9} appear to be storage forms for "high-energy"

phos-358 Μ. I . DOLIN

p h a t e generated in oxidative phosphorylation. Chemical identification of t h e volutin granules as polyphosphate h a s been m a d e in A. aerogenes, C.

diphtheriae, mycobacteria, a n d S. cerevisias.1 T h e formation of m e t a p h o s -p h a t e from A T P in E. coli190 a n d probably C. diphtheriae190 a n d y e a s t1 9 1

takes place as follows:

nATP <=± wADP + ( P 08- > (24)

T h e E. coli enzyme h a s been purified and, with substrate concentration of reactants, h a s been shown t o catalyze reaction (24) in a reversible m a n n e r . Polyphosphate is formed solely from t h e terminal phosphate of A T P .

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In document Survey of Microbial Electron Transport Mechanisms (Pldal 37-45)