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ELSEVIER Biochimicaet Biophysica Acta 1289 (1996) 14-24
BR
Biochi~ie~a
et Biophysica A~ta
NAD-glutamate dehydrogenase from Halobacterium halobium:
inhibition and activation by TCA intermediates and amino acids
Maria Jose Bonete *, Francisco Perez-Pomares, Juan Ferrer, M6nica L. Camacho
Departamento de Agroqufmica-BioqMmica. Facultad de Ciencias. Unicersidad de Alicante, Ap. 99. Alicante, E-03080, Spain
Received 30 May 1995: revised 29 August 1995; accepted 11 September 1995
Abstract
A variety of metabolites have been found to elicit a form of inhibition or activation on an NAD-specific glutamate dehydrogenase
(NAD-GDH, EC 1.4.1.2) from Halobacterium halobium. The purified halophilic enzyme was tested with several compounds known to be
allosteric modifiers of mammalian glutamate dehydrogenases to determine their effects on enzyme activity. GTP, ATP, ADP and AMP
did not affect the enzyme, so these effectors of bovine glutamate dehydrogenase do not play a role in the regulation of the halophilic
enzyme. However, the halophilic enzyme was subject to strong inhibition by TCA intermediates. When measuring the initial rate of the
reaction, the oxidative deamination of L-glutamate was inhibited by TCA metabolites such as: fumarate, oxalacetate, succinate and
malate; by substrate analogues such as: NADP +, D-glutamate and glutarate; and by dicarboxylic compounds such as adipate. On the other
hand, all the amino acids tested were activators of this enzyme, except the D-isomer of the substrate L-glutamate that acted as an inhibitor.
The relative effectiveness of each inhibitor or activator (K~ or K~ values) was correlated with the dipole moment (#), HOMO and
LUMO molecular orbital energies, optimal distance between two carboxyl groups, and hydrophobicity. Compounds with high dipole
moment acted as good activators while compounds with low dipole moment were inhibitors. We have also found that the best activators
were amino acids with no polar lateral chain.
Keywords: Archaea; Halobacterium halobium; NAD-glutamate dehydrogenase: Inhibition: Activation
1. Introduction
Halophilic archaea are obligate halophiles that require
10-20% NaCI for optimal growth [1], and constitute a
fascinating example of biological adaptation. The biochem-
ical machinery of these organisms works at concentrations
of salt at which proteins in non-halophilic cells would be
salted out and cease to function [2,3]. Their proteins have a
strong acidic composition that makes theirs structures salt-
dependent [4,5]. The archaeon H. halobium is an extreme
halophilic microorganism that needs high salt concentra-
tions to grow at optimal conditions. It is chemo-organotroph
and requires amino acids as organic carbon and energy
sources. In its extreme environmental medium, there are
relatively high concentrations of aminoacidic compounds
from the increase of organic matter when water is evapo-
rated.
Corresponding author. Fax: +34 6 5903464: E-mail:
M.J.Bonete@VM.CPD.UA.ES.
0304-4165/96/$15.00 © 1996 Elsevier Science B.V. All rights reserved
SSDI 0304-41 65(95)00134-4
L-glutamate dehydrogenase (EC 1.4.1.2, NAD-GDH)
catalyses the reversible oxidative deamination of L-gluta-
mate to the corresponding keto acid, a-ketoglutarate (a
key carbon intermediate), using NAD ÷ as a coenzyme:
L~ -- glutamate + NAD+ + H20
- ketoglutarate + NADH + NH 4 + H +
This enzyme plays an important role in the catabolism
of L-glutamate [6]. Thus NAD-GDH may represent a key
enzyme in the physiology of the microorganism, enabling
it to convert a number of amino acids into easily utilizable
metabolic intermediates, and it provides a pivotal function
in linking carbon and nitrogen metabolism. It may also be
important in determining the general availability of oxi-
dized and reduced forms of the coenzymes [7].
A great deal is known about the enzymes of halophilic
archaea. Little is known about metabolic control of the
activity and synthesis of their enzymes, though they are
believed to be regulated in patterns similar to enzymes of
eubacteria [8]. The H. halobium uncoloured mutant strain
has two different GDHs, one NADP-dependent that has a