Characterization of Aspergillus niger phosphoglucose isomerase.
Use for quantitative determination of erythrose 4-phosphate
George J.G. Ruijter*, Jaap Visser
Section Molecular Genetics of Industrial Microorganisms, Wageningen Agricultural University,
Dreijenlaan 2, 6703 HA Wageningen, the Netherlands
(Received 17 September 1998; accepted 19 November 1998)
Abstract — Phosphoglucose isomerase (PGI) was purified from Aspergillus niger and the in vitro kinetic properties of the enzyme
were related to its functioning in vivo. A new assay method was developed to study the forward reaction making use of mannitol 1-P
dehydrogenase as the coupling enzyme. In this simple assay system mannitol 1-P dehydrogenase converts fructose 6-P and NADH to
mannitol 1-P and NAD
+
, respectively. At pH 7.5 the K
m
for glucose 6-P was 0.48 mM, whereas the K
m
for fructose 6-P was 0.32 mM.
The pentose phosphate pathway intermediates 6-phosphogluconate and erythrose 4-P (E4P) were competitive inhibitors of PGI with
K
i
values of approximately 0.2 mM and 1 μM respectively. In citric acid producing A. niger mycelium inhibition by 6-phospho-
gluconate is of minor physiological significance (10% inhibition). Since E4P could not be detected by an existing procedure, a novel
assay was developed based on the strong inhibition of PGI by E4P. Although the new assay is very sensitive (detection limit 25 pmol),
E4P could still not be detected in metabolite extracts indicating that a very low level of E4P is present in the cells. Using in vitro
kinetics and concentrations of intracellular metabolites the in vivo activity of PGI was calculated and closely matched the steady state
glycolytic flux observed during citric acid production. © Société française de biochimie et biologie moléculaire / Elsevier, Paris
phosphoglucose isomerase / kinetics / Aspergillus niger / erythrose 4-phosphate / 6-phosphogluconate
1. Introduction
Phosphoglucose isomerase (PGI) catalyses interconver-
sion of glucose 6-P (G6P) and fructose 6-P (F6P) which is
the second step in glycolysis [1]. PGI has a strategic
position in metabolism as several metabolic pathways
branch off from the glycolytic/gluconeogenic pathway
both at G6P (biosynthesis of cell wall components, oxi-
dative part of pentose phosphate pathway) and F6P
(mannitol biosynthesis, non-oxidative part of pentose
phosphate pathway). PGI has been purified from a number
of sources. The best characterized enzymes include PGI
from rabbit skeletal muscle [2] and yeast [3]. Some as-
pects of A. niger PGI have been studied by Singh [4], but
we are not aware of any reports on PGI from other fungi.
Yeast PGI is a dimeric enzyme with a subunit molecular
mass of about 60 kDa [5]. PGI from most sources is
inhibited by several compounds which are intermediates
of central metabolism (e.g., 6-phosphogluconate, eryth-
rose 4-P, ATP)[1]. In particular inhibition by erythrose
4-P (E4P) is strong, e.g., the K
i
value for yeast PGI is 2
μM [6]. The physiological significance of inhibition by
E4P is, however, questionable, since E4P has never been
detected unequivocally in metabolite extracts [7, 8].
Paoletti et al. [7] developed a sensitive assay for determi-
nation of E4P, but failed to detect it in tissue extracts. One
explanation could be that the level of E4P in cells is too
low to be detected by this method [7, 8].
A. niger is able to accumulate a high level of citric acid
from hexoses under particular conditions. The sugar
substrate is metabolized mainly via glycolysis resulting in
formation of pyruvate, which is then converted in a few
steps to citric acid [9]. Recently, several attempts have
been made to construct a model of A. niger carbohydrate
metabolism in relation to citric acid production by this
organism [10–12]. With such models in hand flux control
analysis can be performed enabling design of a strategy to
improve citric acid biosynthesis by genetic engineer-
ing [11]. To support these models with reliable data we
purified and characterised PGI from A. niger. Like PGI
from other sources A. niger PGI is strongly inhibited by
E4P. To investigate the relevance of E4P inhibition in vivo
we attempted to determine E4P levels in metabolite
extracts. However, since E4P could not be detected in A.
niger metabolite extracts by the method of Paoletti et
al. [7], we developed a novel assay for quantitative
determination of E4P, based on the strong inhibition of
PGI by E4P. * Correspondence and reprints
Biochimie 81 (1999), 267-272
© Société française de biochimie et biologie moléculaire / Elsevier, Paris