FEMS Microbiology Letters 58 (1989) 229-232 229
Published by Elsevier
FEM 03505
Nitrogen-limited behaviour of micro-organisms growing
in the presence of large concentrations of ammonium ions
Ed T. Buurman, M. Joost Teixeira de Mattos and Oense M. Neijssel
Department of Microbiology, Biotechnology Centre, University of A msterdam, Amsterdam, The Netherlands
Received 24 November 1988
Accepted 26 November 1988
Key words: Klebsiella pneumoniae; Ammonia assimilation; Glutamate dehydrogenase;
Glutamate synthase; pH; Chemostat culture
1. SUMMARY
Cells of Klebsiella pneumoniae NCTC 418
grown at low culture pH values (4.5-5) in a glu-
cose-limited chemostat culture contained elevated
levels of glutamate synthase (EC 2.6.1.53). This
can be taken as an indication that these cells show
the physiology of nitrogen-limited cells, in spite of
the fact that high concentrations (about 80 mM)
of ammonium ions were present in the culture
extracellular fluids. This phenomenon can be ex-
plained by the rapid diffusion of ammonia (NH3)
through the cell membrane, leading to very low
cytoplasmic ammonium (NH~-) and NH 3 levels in
cells that possess an almost neutral cytoplasmic
pH value, but are growing at low culture pH
values.
2. INTRODUCTION
Ammonium salts are frequently used as a
nitrogen source in microbiological media. An in-
Correspondence to: Dr. O.M. Neijssel, Department of Microbi-
ology, Biotechnology Centre, University of Amsterdam, Nieuwe
Achtergracht 127, 1018 WS Amsterdam, The Netherlands.
teresting problem is how ammonia (NH3) or am-
monium ions (NH~-) enter the cell. Kleiner [1]
estimated that the permeability coefficient for NH 3
through the cell membrane of KlebsieUa pneumo-
niae is high (2 × 10 3 cm. s-l), which indicates
that this compound will diffuse rapidly through
the cell membrane. On the other hand it has been
shown that micro-organisms contain NH~- trans-
port systems which are derepressed when the
medium contains nitrogen sources other than am-
monium salts (for review, see [21). In addition,
there is uncertainty about which chemical species
(NH 3 or NH4~) is the substrate for the two main
assimilatory enzymes: glutamate dehydrogenase
and glutamine synthetase [3].
If NH 3 can indeed diffuse very quickly through
the cell membrane, this will lead to serious conse-
quences when neutrophilic organisms such as K.
pneumoniae or Escherichia coli, possessing a cyto-
plasmic pH value of 7.5-8 [4], are growing at low
medium pH values. Since the NH 3 gradient across
the membrane will be close to zero and the ex-
tracellular NH 3 concentration will be vanishingly
small at such low extracellular pH values, the
intracellular NH 3 and NH~- concentrations can-
not be large. Thus, on the basis of this hypothesis
one could predict that when Klebsiella pneumoniae
is growing in a nominally glucose-limited chemo-
0378-1097/89/$03.50 © 1989 Federation of European Microbiological Societies