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Reduced pyridine nucleotides NADH or NADPH pro-vide the reducing power: NH4 -ketoglutarate NADPH H⎯⎯→ glutamate NADP H2O 25.6 This reaction provides an important interface between nit

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tase, so it no longer binds to nitrogenase The ADP⬊oxidized nitrogenase reductase

complex dissociates, making way for another ATP⬊reduced nitrogenase reductase

complex to bind to nitrogenase Interestingly, nitrogenase reductase is a member of

the G-protein family; G proteins are molecular switches whose operation is driven

by NTP hydrolysis

Nitrogenase is a rather slow enzyme: Its optimal rate of etransfer is about 12 e

pairs per second per enzyme molecule; that is, it reduces only three molecules of

nitrogen gas per second Because its activity is so weak, nitrogen-fixing cells

main-tain large amounts of nitrogenase so that their requirements for reduced N can be

met As much as 5% of the cellular protein may be nitrogenase

The Regulation of Nitrogen Fixation To a first approximation, two regulatory

controls are paramount (Figure 25.8): (1) ADP inhibits the activity of nitrogenase;

thus, as the ATP/ADP ratio drops, nitrogen fixation is blocked (2) NH4 represses

FIGURE 25.7 Ribbon diagram of nitrogenase reductase (the Fe-protein, blue) ⬊nitrogenase (FeMo protein, green) complex The Fe-protein iron-sulfur cluster is shown in yellow, bound ADP in orange The nitrogenase FeMo cofactor is shown in cyan, the P-cluster in red (pdb id  1N2C).

Nitrogenase

Nitrogenase reductase

N

NH2 C O

Nitrogenase reductase

Arg 101 O

ADP

e –

nif gene expression

N2 + + 10 H+ 2 NH4+ + H2

(c)

(b)

(a)

Nicotinamide

Ribose

ADP–ribosyl group

ATP

NAD+

ADP 8

FIGURE 25.8 Regulation of nitrogen fixation (a) ADP inhibits nitrogenase activity (b) NH4 represses nif gene

expression (c) In some organisms, the nitrogenase

complex is regulated by covalent modification ADP– ribosylation of nitrogenase reductase leads to its inactivation.

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774 Chapter 25 Nitrogen Acquisition and Amino Acid Metabolism

the expression of the nif genes, the genes that encode the proteins of the nitrogen-fixing system To date, some 20 nif genes have been identified with the nitrogen fix-ation process Repression of nif gene expression by ammonium, the primary

prod-uct of nitrogen fixation, is an efficient and effective way of shutting down N2fixation when its end product is not needed In addition, in some systems, covalent modifi-cation of nitrogenase reductase leads to its inactivation Inactivation occurs when Arg101of nitrogenase reductase receives an ADP-ribosyl group donated by NAD

25.2 What Is the Metabolic Fate of Ammonium?

Given the prevalence of N atoms in cellular components, it is surprising that only three enzymatic reactions introduce ammonium into organic molecules Of these

three, glutamate dehydrogenase and glutamine synthetase are responsible for most of the ammonium assimilated into carbon compounds The third, carbamoyl-phosphate syn-thetase I, is a mitochondrial enzyme that participates in the urea cycle.

Glutamate dehydrogenase (GDH) catalyzes the reductive amination of

-keto-glutarate to yield glutamate Reduced pyridine nucleotides (NADH or NADPH) pro-vide the reducing power:

NH4  -ketoglutarate  NADPH  H⎯⎯→

glutamate NADP H2O (25.6) This reaction provides an important interface between nitrogen metabolism and cel-lular pathways of carbon and energy metabolism because -ketoglutarate is a citric acid

cycle intermediate In vertebrates, GDH is an 6-type multimeric enzyme localized in the mitochondrial matrix that uses NADPH as electron donor when operating in the biosynthetic direction (the direction of glutamate synthesis) (Figure 25.9) In contrast, when GDH acts in the catabolic direction to generate -ketoglutarate from glutamate,

NAD, not NADP, is usually the electron acceptor The catabolic activity is allosteri-cally activated by ADP and inhibited by GTP

Glutamine synthetase (GS) catalyzes the ATP-dependent amidation of the

-carboxyl group of glutamate to form glutamine (Figure 25.10) The reaction

pro-ceeds via a -glutamyl-phosphate intermediate, and GS activity depends on the

presence of divalent cations such as Mg2 Glutamine is a major N donor in the

biosynthesis of many organic N compounds such as purines, pyrimidines, and other amino acids, and GS activity is tightly regulated, as we shall soon see The amide-N of glutamine provides the nitrogen atom in these biosyntheses

Carbamoyl-phosphate synthetase I, the third enzyme capable of using ammo-nium to form an N-containing organic compound, catalyzes an early step in the urea cycle Two ATPs are consumed, one in the activation of HCO3 for reaction with ammonium and the other in the phosphorylation of the carbamate formed (see also Figure 25.22):

(25.7)

N-acetylglutamate is an essential allosteric activator for this enzyme.

NH4  HCO3   2 ATP H2N C O PO3 2 ADP  Pi 2 H

O

NH3+

C

CH2

CH2

C

+

C

CH2

CH2

C

HC

NH4+

Glu

H2O

-KG

FIGURE 25.9 The glutamate dehydrogenase reaction.

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The Major Pathways of Ammonium Assimilation Lead

to Glutamine Synthesis

In organisms that enjoy environments rich in nitrogen, GDH and GS acting in

se-quence furnish the principal route of NH4 incorporation (Figure 25.11) However,

GDH has a significantly higher Kmfor NH4 than does GS Consequently, in

organ-isms such as green plants that grow under conditions where little NH4 is available,

GDH is not effective and GS is the only NH4 -assimilative reaction Such a situation

creates the need for an alternative mode of glutamate synthesis to replenish the

glu-tamate consumed by the GS reaction This need is filled by gluglu-tamate synthase (also

known as GOGAT, the acronym for the other name of this enzyme—glutamate⬊

o xo-glutarate amino-transferase) Glutamate synthase catalyzes the reductive

amina-tion of -ketoglutarate using the amide-N of glutamine as the N donor:

Reductant -KG  Gln ⎯⎯→ 2 Glu  oxidized reductant (25.8)

Two glutamates are formed—one from amination of -ketoglutarate and the other

from deamidation of Gln (Figure 25.12) These glutamates can now serve as

am-monium acceptors for glutamine synthesis by GS Organisms variously use NADH,

NADPH, or reduced ferredoxin as reductant Glutamate synthases are typically

large, complex proteins; in Escherichia coli, GOGAT is an 800-kD flavoprotein

con-taining both FMN and FAD, as well as [4Fe-4S] clusters

NH3+

C

CH2

CH2

C

C

O C

CH2

CH2 C C

+

H

NH4+

NH3+ H

NH2

C

CH2

CH2

C

C

+

NH3+

O

CH2

CH2 C C

C

H

O–

O P O–

+

O–

O P OH

O C

CH2

CH2 C C

H

NH2

ATP

Gln

(a) Glu

Mg2+

(b)

Gln

ADP

(a)

(b)

FIGURE 25.10 (a) The enzymatic reaction catalyzed by

glutamine synthetase (b) The reaction proceeds by (a)

activation of the -carboxyl group of Glu by ATP,

fol-lowed by (b) amidation by NH 4 

(a) NH4++-ketoglutarate+ NADPH glutamate GDH + NADP++H2O

(b) Glutamate + NH4++ ATP glutamine GS + ADP +Pi

SUM: 2 NH4++-ketoglutarate+ NADPH + ATP glutamine + NADP++ADP+Pi+H2O

FIGURE 25.11 The GDH/GS pathway of ammo-nium assimilation The sum of these reactions

is the conversion of 1 -ketoglutarate to 1

glu-tamine at the expense of 2 NH 4  , 1 ATP, and

1 NADPH.

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776 Chapter 25 Nitrogen Acquisition and Amino Acid Metabolism

Together, GS and GOGAT constitute a second pathway of ammonium assimilation,

in which GS is the only NH4 -fixing step; the role of GOGAT is to regenerate gluta-mate (Figure 25.13) Note that this pathway consumes 2 equivalents of ATP and

1 NADPH (or similar reductant) per pair of N atoms introduced into Gln, in contrast

to the GDH/GS pathway, in which only 1 ATP and 1 NADPH are consumed per pair

of NH4 fixed Clearly, coping with a nitrogen-limited environment has its cost

25.3 What Regulatory Mechanisms Act on Escherichia coli

Glutamine Synthetase?

As indicated earlier, glutamine plays a pivotal role in nitrogen metabolism by donating its amide nitrogen to the biosynthesis of many important organic N com-pounds Consistent with its metabolic importance, in prokaryotic cells such as

E coli, GS is regulated at three different levels:

1 Its activity is regulated allosterically by feedback inhibition.

2 GS is interconverted between active and inactive forms by covalent modification.

3 Cellular amounts of GS are carefully controlled at the level of gene expression and protein synthesis.

Eukaryotic versions of glutamine synthetase show none of these regulatory features

E coli GS is a 600-kD dodecamer (12-type subunit organization) of identical 52-kD monomers (each monomer contains 468 amino acid residues) These monomers are arranged as a stack of two hexagons (Figure 25.14) The active sites are located at subunit interfaces within the hexagons; these active sites are recognizable in the X-ray crystallographic structure by the pair of divalent

-KG

NH3+

C

CH2

CH2

C

+

C

CH2

CH2 C C

H

Gln

NH3+

O C

CH2

CH2 C C

H

NH2

NADH (yeast, N crassa)+ H+

NADPH (E coli)+ H + or

2 H++ 2 reduced ferredoxin (plants)

+-KG + Gln 2 Glu + NAD

+ NADP + or

2 oxidized ferredoxin

NH3+

C

CH2

CH2 C C

H +

(a) 2 NH4++ 2 ATP + 2 glutamate 2 glutamine GS + 2 ADP +2 Pi

(b) NADPH +-ketoglutarate+ glutamine 2 glutamate GOGAT + NADP+

SUM: 2 NH4++-ketoglutarate+ NADPH + 2 ATP glutamine + NADP++2 ADP+2 Pi

FIGURE 25.12 The glutamate synthase reaction (left), showing the reductants exploited by different organisms

in this reductive amination reaction Structure of glutamate synthase (right) (pdb id  1LM1) FAD is shown in blue, the Fe-S cluster in yellow.

FIGURE 25.13 The GS/GOGAT pathway of

ammonium assimilation The sum of these

reactions results in the conversion of 1

-ketoglutarate to 1 glutamine at the expense

of 2 ATP and 1 NADPH.

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cations that occupy them Adjacent subunits contribute to each active site, thus

accounting for the fact that GS monomers are catalytically inactive

Glutamine Synthetase Is Allosterically Regulated

Nine distinct feedback inhibitors (Gly, Ala, Ser, His, Trp, CTP, AMP, carbamoyl-P, and

glucosamine-6-P) act on GS Gly, Ala, and Ser are key indicators of amino acid

me-tabolism in the cell; each of the other six compounds represents an end product of a

biosynthetic pathway dependent on Gln (Figure 25.15) AMP competes with ATP for

binding at the ATP substrate site Gly, Ala, and Ser compete with Glu for binding at

the active site Carbamoyl-P binds at a site that overlaps both the Glu site and the site

occupied by the -PO4of ATP

Glutamine Synthetase Is Regulated by Covalent Modification

Each GS subunit can be adenylylated at a specific tyrosine residue (Tyr397) in an

ATP-dependent reaction (Figure 25.16) Adenylylation inactivates GS If we

de-fine n as the average number of adenylyl groups per GS molecule, GS activity is

inversely proportional to n The number n varies from 0 (no adenylyl groups) to

12 (every subunit in each GS molecule is adenylylated) Adenylylation of GS is

catalyzed by the converter enzyme ATP ⬊GS⬊adenylyl transferase, or simply adenylyl

transferase (AT) However, whether or not this covalent modification occurs is

de-termined by a highly regulated cycle (Figure 26.17) AT not only catalyzes

adeny-lylation of GS, it also catalyzes deadenyadeny-lylation—the phosphorolytic removal of

the Tyr-linked adenylyl groups as ADP The direction in which AT operates

de-pends on the nature of a regulatory protein, PII, associated with it P IIis a 44-kD

protein (tetramer of 11-kD subunits): The state of PII controls the direction in

FIGURE 25.14 The subunit organization of bacterial

glutamine synthetase (a) Schematic; (b) molecular

structure (note the pairs of metal ions [dark blue] that define the active sites) (pdb id  1FPY).

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778 Chapter 25 Nitrogen Acquisition and Amino Acid Metabolism

P

R

O

O–

+H3N

Mg2+

C H

H C

O

O–

+H3N C

CH3

H C

Glutamine

O

O–

+H3N C

CH2 OH

O

O–

CH2 N N H

N H

O

O–

C

CH2 +NH3

O

NH2

CH2

P

P P

R N N

NH2 N

N

N N

NH2

O–

O P O–

O

O C +H3N

P

+NH3

O

ATP

P

Glutamate +

NH4+

+

Glycine

Alanine

Glutamine synthetase

Serine

Histidine

Tryptophan

Glucosamine-6-P

CTP

Carbamoyl-P

ADP

AMP

FIGURE 25.15 The allosteric regulation of glutamine synthetase activity by feedback inhibition.

CH2

P P

OH

CH2

O

OCH2

N

N N

NH2

ATP

12 + Tyr397in GS

monomer

Glutamine synthetase monomer

Adenylyl transferase

Glutamine synthetase monomer

12

12 Adenylylated Tyr 397 in GS monomer

FIGURE 25.16 Covalent modification of GS: Adenylylation of Tyr 397 in the glutamine synthetase polypeptide via

an ATP-dependent reaction catalyzed by the converter enzyme adenylyl transferase.

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which AT acts If PII is in its so-called PIIA form, the AT⬊PIIA complex acts to

adenylylate GS When PII is in its so-called PIID form, the AT⬊PIID complex

cat-alyzes the deadenylylation of GS The active sites of AT⬊PIIAand AT⬊PIIDare

dif-ferent, consistent with the difference in their catalytic roles In addition, the

AT⬊PIIA and AT⬊PIID complexes are allosterically regulated in a reciprocal

fash-ion by the effectors -KG and Gln Gln activates AT⬊PIIA activity and inhibits

AT⬊PIIDactivity; the effect of -KG on the activities of these two complexes is

di-ametrically opposite (Figure 25.17) Further, Gln favors conversion of PIIDto PIIA,

whereas-ketoglutarate favors the PIIDover the PIIAform

Clearly, the determining factor regarding the degree of adenylylation, n, and

hence the relative activity of GS, is the [Gln]/[-KG] ratio A high [Gln] level

sig-nals cellular nitrogen sufficiency, and GS becomes adenylylated and inactivated In

contrast, a high [-KG] level is an indication of nitrogen limitation and a need for

ammonium fixation by GS

Glutamine Synthetase Is Regulated Through Gene Expression

The gene that encodes the GS subunit in E coli is designated GlnA The GlnA gene

is actively transcribed to yield GS mRNA for translation and synthesis of GS protein

only if a specific transcriptional enhancer, NRI ,is in its phosphorylated form, NRI-P In

turn, NRIis phosphorylated in an ATP-dependent reaction catalyzed by NR II ,a

pro-tein kinase (Figure 25.18) However, if NRIIis complexed with PIIA, it acts not as a

kinase but as a phosphatase, and the transcriptionally active form of NRI, namely

NRI-P, is converted back to NRIwith the result that GlnA transcription halts Recall

from the foregoing discussion that a high [Gln]/[-KG] ratio favors PIIAat the

ex-pense of PIID Under such conditions, GS gene expression is not necessary

25.4 How Do Organisms Synthesize Amino Acids?

Organisms show substantial differences in their capacity to synthesize the

20 amino acids common to proteins Typically, plants and microorganisms can

form all of their nitrogenous metabolites, including all of the amino acids, from

P P

P

+

+

ATP

12

Adenylyl transferase:

PIIA complex

Adenylyl transferase:

PIID complex

12 ADP

Less active GS:

Tyr397–O– AMP adenylylated

-KG Gln

-KG Gln

Active GS:

Tyr397 unadenylylated

Highly sensitive

to feedback inhibition

*State of PII controls adenylyl transferase direction

FIGURE 25.17 The cyclic cascade system regulating the covalent modification of GS.

+

NRII

H2O

P

NRII:PIIA

P

activates GlnA

transcription; GS

is synthesized

FIGURE 25.18 Transcriptional regulation of GlnA

expres-sion through the reversible phosphorylation of NR I

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780 Chapter 25 Nitrogen Acquisition and Amino Acid Metabolism

inorganic forms of N such as NH4 and NO3  In these organisms, the -amino

group for all amino acids is derived from glutamate, usually via transamination of the corresponding -keto acid analog of the amino acid (Figure 25.19) In many

cases, amino acid biosynthesis is thus a matter of synthesizing the appropriate

-keto acid carbon skeleton, followed by transamination with Glu The amino

acids can be classified according to the source of intermediates for the -keto acid

biosynthesis (Table 25.1) For example, the amino acids Glu, Gln, Pro, and Arg

CH2

C COO–

NH3+ COO–

COO–

COO–

COO–

COO–

COO–

COO–

COO–

CH2

CH2 C H

+

R O

CH2

CH2

C COO– +

R

NH3+

CH2

CH2 C H

+ C COO–

O

CH2

CH2

+ C COO–

CH2

Glutamate -Keto acid -KG -Amino acid

Glutamate Oxaloacetate -KG Aspartate

Pyridoxal phosphate-dependent aminotransferase

Glutamate-aspartate aminotransferase

ACTIVE FIGURE 25.19

Glutamate-dependent transamination of -keto acid carbon

skele-tons is a primary mechanism for amino acid synthesis.

The transamination of oxaloacetate by glutamate to

yield aspartate and -ketoglutarate is a prime example.

Test yourself on the concepts in this figure at

www.cengage.com/login.

Lysine*

Phosphoenolpyruvate and Erythrose-4-P Family The aromatic amino acids

Phenylalanine Tyrosine Tryptophan

The remaining amino acid, histidine, is derived from PRPP

(5-phosphoribosyl-1-pyrophosphate) and ATP

TABLE 25.1 The Grouping of Amino Acids into Families According to the Metabolic Intermediates

That Serve as Their Progenitors

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(and, in some instances, Lys) are all members of the -ketoglutarate family

be-cause they are all derived from the citric acid cycle intermediate -ketoglutarate.

We return to this classification scheme later when we discuss the individual

biosynthetic pathways

Amino Acids Are Formed from ␣-Keto Acids by Transamination

Transamination involves transfer of an -amino group from an amino acid to the

-keto position of an -keto acid (Figure 25.19) In the process, the amino donor

be-comes an -keto acid while the -keto acid acceptor becomes an -amino acid:

Amino acid  -keto acid ⎯⎯→ -keto acid  amino acid (25.9)

HUMAN BIOCHEMISTRY

Human Dietary Requirements for Amino Acids

Humans can synthesize only 10 of the 20 common amino acids

(see table below); the others must be obtained in the diet Those

that can be synthesized are classified as nonessential, meaning it

is not essential that these amino acids be part of the diet In

ef-fect, humans can synthesize the -keto acid analogs of

nonessen-tial amino acids and form the amino acids by transamination In

contrast, humans are incapable of constructing the carbon

skele-tons of essential amino acids, so they must rely on dietary sources

for these essential metabolites Excess dietary amino acids cannot

be stored for future use, nor are they excreted unused Instead,

they are converted to common metabolic intermediates that can

be either oxidized by the citric acid cycle to generate metabolic

energy or used to form glucose (see Section 25.5)

Since autotrophic cells (and many prokaryotic cells) synthesize

all 20 amino acids, several questions arise regarding human

di-etary requirements for amino acids First, why is it that humans

lack the ability to do what other organisms can do? The answer is

that, over evolutionary time, human diets provided adequate

amounts of those amino acids classified now as “essential.” Thus,

the loss of the metabolic pathways for synthesis of “essential”

amino acids did not impair the fitness of humans That is,

synthe-sizing “essential” amino acids became superfluous, and no

evolu-tionary pressure operated on humans to retain the genes for these

pathways A second question now emerges: Are there significant

differences between synthesis of amino acids human can make

(the so-called “nonessential” amino acids) and those they can’t?

The big table summarizes amino acid biosynthesis from citric acid cycle intermediates in terms of the number of reactions needed to make an amino acid from a TCA cycle intermediate.* Nonessen-tial amino acids are shown in blue; essenNonessen-tial amino acids in red Two conclusions stand out: Nonessential amino acids require fewer reaction steps for synthesis than essential amino acids, and nonessential amino acids tend to be more abundantly represented

in proteins than essential amino acids Thus, evolutionary loss was not random: The biosynthetic pathways lost were those for amino acids requiring the most reaction steps

*From Srinivasan, V., Morowitz, H., and Smith, E., 2007 Essential amino

acids, from LUCA to LUCY Complexity 13:8–9.

Histidine* Asparagine

Phenylalanine Glycine

*Arginine and histidine are essential in the diets of juveniles, not adults.

†Tyrosine is classified as nonessential only because it is readily formed from essential

phenylalanine.

Essential and Nonessential Amino Acids in Humans

Amino Acid Reaction Steps Mole % in Proteins†

†Mole percentages are taken from amino acid representations among proteins in the Swiss-Prot protein knowledgebase: ca.expasy.org/sprot.

‡Note that “nonessential” tyrosine can only be made from “essential” phenylanine.

Nonessential Amino Acids Require Fewer Reactions for Synthesis

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782 Chapter 25 Nitrogen Acquisition and Amino Acid Metabolism

The predominant amino acid/-keto acid pair in these reactions is glutamate/

-ketoglutarate, with the net effect that glutamate is the primary amino donor

for the synthesis of amino acids Transamination reactions are catalyzed by

aminotransferases (the preferred name for enzymes formerly termed transami-nases) Aminotransferases are named according to their amino acid substrates, as in

glutamate–aspartate aminotransferase. Aminotransferases are prime examples of enzymes that catalyze double displacement (ping-pong)–type bisubstrate reactions (see Figure 13.23)

The Pathways of Amino Acid Biosynthesis Can Be Organized into Families

As indicated in Table 25.1, the amino acids can be grouped into families on the basis of the metabolic intermediates that serve as their precursors

A DEEPER LOOK

The Mechanism of the Aminotransferase (Transamination) Reaction

The aminotransferase (transamination) reaction is a workhorse in

biological systems It provides a general means for exchange of

nitrogen between amino acids and -keto acids This vital reaction

is catalyzed by pyridoxal phosphate (PLP) The mechanism

in-volves loss of the C proton, followed by an aldimine–ketimine

tautomerization—literally a “flip-flop” of the Schiff base double

bond from the pyridoxal aldehyde carbon to the -carbon of the

amino acid substrate This is followed by hydrolysis of the ketimine intermediate to yield the product -keto acid Left in the active

site is a pyridoxamine phosphate intermediate, which combines with another (substrate) -keto acid to form a second ketimine,

which rearranges to form an aldamine, followed by release as an amino acid Transaldiminization with a lysine at the active site completes the reaction

+

H

NH3+

N HC +

CH3 N

H +

2 –O3PO

N

O

+ –

N H +

2 –O3PO

O

NH2

H2C

O–

CH3 N

H +

2 –O3PO

O

N

H2C +

CH3 N

H +

2 –O3PO +

H

NH3+

H

N HC +

CH3 N

H +

2 –O3PO

H

CH3

H

O–

H +

H +

H2O

H2O

C

2– O3PO

OH

CH3 N

H +

Lysine

H

O–

H

O–

Ketimine Aldimine

Transamination intermediate

Pyridoxamine

E•PLP complex

E-PLP complex

䊱 The mechanism of PLP-catalyzed transamination reactions.

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