Appl Microbiol Biotechnol (1987) 26:277--282 Applied
Microbiology
Biotechnology
© Springer-Verlag 1987
Assimilatory reduction of trimethylamine N-oxide
in the yeast Sporopachydermia cereana
David Whitfield* and Peter J. Large
Department of Biochemistry, University of Hull, Hull HU6 7RX, U. K.
Summary. Washed microsomal preparations
(100000 xg sediment) from the yeast Sporopachy-
dermia cereana that had been grown on trimethyl-
amine N-oxide as sole nitrogen source catalysed
the NAD(P)H-dependent reduction of trimethyl-
amine N-oxide to trimethylamine. Under an-
aerobic conditions, this was the sole reaction prod-
uct, but under aerobic conditions only small
amounts of trimethylamine accumulated, most be-
ing further metabolized to methylamine and for-
maldehyde (no detectable dimethylamine accu-
mulated due to its rapid turnover). In the absence
of NAD(P)H, no formation of amines or formal-
dehyde from trimethylamine N-oxide was de-
tected. The trimethylamine N-oxide reductase ac-
tivity was inhibited by quinacrine, Cu 2+ ions, tri-
ethylamine N-oxide (apparent Ki 0.43 mM) and di-
methyl sulphoxide (Ki 0.94 mM). Chlorate and ni-
trate failed to inhibit the enzyme. The Km for tri-
methylamine N-oxide was 29 IxM. Triethylamine
N-oxide was also reduced by the microsomal pre-
paration with the formation of acetaldehyde, and
this reduction was sensitive to the same inhibitors
as trimethylamine N-oxide, suggesting that both
amine oxides are metabolized by the same en-
zyme(s). It is concluded that trimethylamine N-
oxide is metabolized in this yeast via an
NAD(P)H-dependent reductase.
* Present address: Biology Division, Chemical Defence Estab-
lishment, Porton Down, Salisbury, Wilts. SP4 0JQ, U.K.
Offprint requests to: P. J. Large
Abbreviations: TMAO, trimethylamine N-oxide
Introduction
Trimethylamine N-oxide (TMAO) is an abundant
constituent of the muscle and body fluids of ma-
rine fish, and during bacterial decay under rela-
tively anaerobic conditions, the odourless, non-
volatile N-oxide is reduced to trimethylamine
with its characteristic fishy smell (Barrett and
Kwan 1985). The putrefactive bacteria are using
TMAO as a terminal electron acceptor with the
concomitant electron transport-dependent forma-
tion of ATP. The enzymic nature of this dissimila-
tory TMAO reduction has been well characterized
in a wide range of bacteria (e. g. Salmonella typhi-
murium, Kwan and Barrett 1983; Escherichia coli,
Shimokawa and Ishimoto 1979; Yamamoto et al.
1986; and Rhodopseudomonas eapsulata, McEwan
et al. 1985). The same enzyme system is also al-
most certainly responsible for the reduction of di-
methyl sulphoxide (Styrvold and Strom 1984;
McEwan et al. 1985). The trimethylamine formed
from TMAO under these conditions is not meta-
bolized further.
TMAO however can also function as a ni-
trogen or carbon source for the growth of some
bacteria (Large 1981 ; Large and Green 1984), and
as a nitrogen source for yeasts (Yamada et al.
1976; Green and Large 1984), and in this situation
is playing an assimilatory role rather than a dis-
similatory role. Utilization of TMAO by methylo-
trophic bacteria does not normally involve reduc-
tion, but a non-oxidative cleavage of the N-oxide
to dimethylamine and formaldehyde catalysed by
TMAO aldolase (E. C. 4.1.2.32) (Large 1971;
Myers and Zatman 1971) (Eq. 1).
(CH3)3NO ~ (CH3)2NH + HCHO (1)
As a preliminary to investigating the possible ap-