Comp. Biochem. Physiol. Vol. 74B, No. 3, pp. 567 to 571, 1983 0305-0491/83/030567-05503.00/0
Printed in Great Britain. © 1983PergamonPress Ltd
ADAPTATION OF TERMINAL RESPIRATION PATHWAYS
OF TETRAHYMENA PYRIFORMIS ST TO GROWTH WITH
ADDED IRON OR CARBONYL CYANIDE
m-CHLOROPHENYLHYDRAZONE
MARK D. UN1TT*, ROBERTI. SCOTTand DAVID LLOYD
Department of Microbiology, University College, Newport Road, Cardiff CF2 1TA, Wales, UK
Abstract--1. Tetrahymena pyriformis grown in medium which contained 0.6/~g/ml iron possesses at least
three pathways of terminal respiration which are inhibited by cyanide, azide and salicylhydroxamicacid
respectively.
2. Mid-exponential phase cultures grown in the presence of 5.6/~g/ml iron and glucose showed the
same respiratory properties in terms of respiration rate and inhibitor sensitivity as cultures grown in the
absence of added iron and glucose.
3. The respiration of mid-exponential phase cultures adapted to growth in the presence of 2.5/~M-
carbonyl cyanide m-chlorophenylhydrazone was incompletely inhibited by a combination of cyanide,
azide and salicylhydroxamic acid.
4. The residual respiration accounted for between 25 and 35~o of the total, indicating synthesis of a
novel terminal oxidase or gross modification of existing terminal respiratory pathways in the presence of
the uncoupler of energy conservation.
5. The sole functional cytochrome oxidase present in organisms grown in the absence or presence of
added iron and glucose or after adaptation to uncoupler was cytochrome a6zo; no other CO-reacting
haemoprotein was detected in photochemical action spectra.
INTRODUCTION
Many eukaryotic micro-organisms show a residual
respiration in the presence of cyanide, azide or carbon
monoxide, even when these inhibitors are present in
sufficiently high concentrations to inhibit cytochrome
c oxidase completely (Lloyd, 1974). Such inhibitor
studies on protozoa have demonstrated the presence
of at least two terminal oxidases, apart from cyto-
chrome c oxidase, in the trypanosome Trypanosoma
mega (Hill & Degn, 1977) and in the soil amoeba
Acanthamoeba castellanii (Lloyd et al., 1979).
Respiration of the ciliated protozoon Tetrahymena
pyriformis has several unusual features and has been
the subject of study since Baker & Baumberger (1941)
noted its atypical a-type cytochromes. Studies of the
effects of respiratory inhibitors on intact T. pyriformis
have shown that the process of terminal oxidation in
this protozoon can be resolved into five distinct path-
ways, terminating in at least three oxidases (Lloyd et
al., 1980). Pathway 1 is inhibited by azide, cyanide,
CO and H2S. A second major pathway is inhibited by
much higher cyanide concentrations and by H2S.
Pathway 3 is H2S-sensitive but cyanide-insensitive,
while a fourth pathway is inhibited only by high con-
centrations of cyanide (1-2 mM). Cytochrome %20 is
kinetically competent to act as a terminal oxidase
(Turner et al., 1971), reacts with cyanide and CO
(Lloyd & Chance, 1972), and is probably the terminal
oxidase for pathway 1. Pathways 2, 3 and 4 may ter-
minate at novel alternative oxidases or involve modi-
* Present address: Department of Biochemistry, Univer-
sity College, Cathays Park, Cardiff CF1 1XL, Wales, UK
Abbreviations: CCCP, Carbonyl cyanide m-chlorophe-
nylhydrazone; SHAM, Salicylhydroxamicacid.
fled forms of component 1. Pathway 5 is unaffected by
azide, cyanide, CO or H2S but is sensitive to inhi-
bition by salicylhydroxamic acid (SHAM). The oxi-
dase sensitive to inhibition by SHAM has recently
been demonstrated in T. pyriformis by Eichel &
Stearns (1977), and it has been suggested that it is
extremely active in media supplemented with metal
ions (Stearns et al., 1978).
T. pyriformis can become physiologically adapted to
grow in medium containing 10 - 4 M cyanide
(McCashland, 1955). Euglena gracilis, adapted to
growth in the presence of 10-SM 2,4-dinitrophenol
(Kahn, 1974), becomes resistant to other uncouplers
of energy conservation. Crithidia fasciculata has also
been adapted to growth in the presence of carbonyl-
cyanide m-chlorophenylhydrazone (CCCP) (Kutzman
& Roberts, 1978). The resistance reported in these
organisms is apparently not a result of mutant selec-
tion. In both T. pyriformis (McCashland & Andresen,
1963) and E. gracilis (Kahn, 1973), resistance is readily
reversible by culturing the cells in the absence of the
stressing agent.
In the present paper, we describe the effects of
azide, cyanide and SHAM on the respiration of intact
organisms cultured in media supplemented with iron
and in the presence of CCCP, and show that cyto-
chrome a620 is the sole cytochrome oxidase irrespec-
tive of growth conditions.
EXPERIMENTAL METHOD
Maintenance and 9rowth of oroanisms
Tetrahymena pyriformis ST was maintained and grown
axenically on a basal medium composed of: 2% (w/v) pro-
teose peptone (Difco) and 0.1% (w/v) liver digest (Oxoid)
with shaking at 30°C, exactly as described previously
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