Department of Biology, University of Bologna, 42 Irnerio, 40126 Bologna I, Italy1
Author for correspondence: Davide Zannoni. Tel: +39 051 209 1285/86. Fax+39 051 24 25 76. e-mail: zannoni{at}alma.unibo.it
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ABSTRACT |
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Keywords: cytochromes, tellurite uptake, tellurium crystallites
Abbreviations: cyt, cytochrome; TMBZ, 3,3',5,5'-tetramethylbenzidine
This work is dedicated to my friend and colleague Franco Tatò, prematurely deceased on 7 July 2001.
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INTRODUCTION |
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The role assumed by the respiratory chain of bacterial cells resistant to potassium tellurite remains elusive, although several reports suggest that plasma-membrane redox enzymes might be involved in at least one of the two enzymic steps required to generate tellurium from tellurite (Moore & Kaplan, 1992 ). The extent of tellurite reduction in R. sphaeroides was inversely related to the oxidation state of the carbon source and it has also been shown to be dependent on FADH2 oxidation activity (Moore & Kaplan, 1992
, 1994
). Chiong et al. (1988)
purified a protein fraction from Thermus thermophilus which contained an NADH/NADPH-dependent tellurite-reducing activity, while Terai et al. (1958)
demonstrated tellurite reduction in cell extracts of Mycobacterium avium. Tellurite reductase activity encoded by a large conjugative plasmid of the IncHI-2 incompatibility group has also been observed in Alcaligenes sp. (Jobling & Ritchie, 1988
). The membrane-bound nitrate reductases (NarG and NarZ) have been found to reduce tellurite and contribute to the basal level of resistance in Escherichia coli (Avazeri et al., 1997
). Additionally, the periplasmically located nitrate reductase (Nap) also exhibits tellurite reductase activity (R. J. Turner, personal communication). Recently, the electron-transport activity catalysed by the branched respiratory chain of Pseudomonas aeruginosa (Matsushita et al., 1980
; Zannoni, 1989
; Cunningham & Williams, 1995
) has been correlated with reduction of potassium tellurite, although at a rate which is three orders of magnitude lower than the rate of oxygen reduction (Trutko et al., 2000
).
Strain KF707 of Pseudomonas pseudoalcaligenes has been extensively described in the past for its capacity to cometabolize polychlorinated biphenyls (PCBs) under aerobic conditions (Taira et al., 1992 ; Fedi et al., 2001
). Notably, during a selection procedure for the isolation of TeR strains from a PCB-contaminated soil, we have recently observed that P. pseudoalcaligenes KF707 can also grow in media containing up to 100 µg ml-1 (0·4 mM) of potassium tellurite (unpublished results). This observation, in addition to the fact that to the best of our knowledge no data are presently available on the arrangement of the respiratory pathway of P. pseudoalcaligenes, prompted us to investigate the effect of potassium tellurite on the type and composition of the plasma-membrane respiratory redox components along with the uptake and reduction of potassium tellurite linked to accumulation of intracellular crystals of elemental tellurium. We demonstrate that P. pseudoalcaligenes KF707 cells have a branched respiratory chain which is functionally and structurally affected by tellurite; we also conclude that tellurite-dependent modifications of the respiratory chain and tellurite reduction to elemental tellurium are unrelated phenomena.
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METHODS |
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Preparation of membranes.
P. pseudoalcaligenes KF707 membrane fragments from washed cells grown aerobically in LB medium in the presence or absence of potassium tellurite were prepared using a French pressure cell and ultracentrifugation as described previously (Zannoni et al., 1978 ) either in 50 mM MOPS buffer (pH 7·0) containing 1 mM KCl, EDTA and PMSF for PAGE analyses or in 50 mM Tricine buffer (pH 7·5) containing 5 mM MgCl2 for spectroscopic studies. Membrane fragments were suspended at a known protein concentration in the same buffer, and used immediately for electron-transport measurements or stored frozen at -80 °C for PAGE analyses.
Protein determination.
Protein content of samples was determined by the method of Bradford (1976) , using bovine serum albumin as a standard.
Measurement of oxygen uptake and inhibitor titrations.
Respiratory activities in membrane fragments were determined by monitoring oxygen consumption with a Clark-type oxygen electrode YSI 53 (Yellow Springs Instruments) as detailed elsewhere (Daldal et al., 2001 ).
Spectral analysis of cytochrome content of membranes.
The amounts of cytochromes in membrane fragments and soluble fractions were estimated by recording reduced (with sodium ascorbate or dithionite)-minus-oxidized (with potassium ferricyanide) optical difference spectra at room temperature with a Jasco 7800 spectrophotometer. Absorption coefficients 604630 of 23 mM-1 cm-1,
561575 of 22 mM-1 cm-1 and
551540 of 19 mM-1 cm-1 were used for a-, b- and c-type cytochromes, respectively.
Equilibrium redox titrations.
Dark equilibrium redox titrations were performed in a self-made glass cuvette kept anoxic by means of a stream of argon. A platinum electrode was fitted into the cuvette and the redox potentials were measured against an external calomel electrode connected via a salt bridge. The following redox mediators, at a concentration of 2·5 µM, were used: N-ethyldibenzopyrazine ethyl sulphate, N-methyldibenzopyrazine methyl sulfate, 2,3,5,6-tetramethyl-1,4-benzoquinone, p-benzoquinone, 1,2-naphthoquinone and 1,4-naphthoquinone. Sodium ascorbate and sodium dithionite were used as reductants; potassium ferricyanide was the oxidant. Membranes equivalent to 3 mg ml-1 were suspended in MES/TES/Tricine (30 mM each) buffer with 50 mM KCl (pH 7·09·0).
Determination of potassium tellurite in liquid media.
The quantitative determination of tellurite was done using the reagent diethyldithiocarbamate (DDTC) as described by Turner et al. (1992) .
Electron micrographs of bacterial cells.
To determine the presence of tellurium (Te0) in bacterial cells, potassium tellurite (35 µg ml-1) was added to the liquid culture during the mid-exponential growth phase. Two hours later, when the bacterial cultures became black, they were harvested and processed for electron-microscopy analysis as follows. Cell pellets were fixed for 2 h in 0·05 M cacodylate, 1·5% (w/v) glutaraldehyde (pH 7·2); the same buffer was used for overnight washing of the samples followed by 2 h fixation with 2% (w/v) osmium tetroxide and dehydration with ethanol. Samples were finally embedded in Durcopan. Thin sections obtained by an LKB Ultratome Nova were double-stained with uranyl acetate and lead citrate (Reynolds, 1963 ). Specimens were examined with a Philips CM-100 transmission electron microscope.
TMBZ-SDS-PAGE gels.
SDS-PAGE was performed using 16·5% (w/v) acrylamide Tris-Tricine gels as described by Shägger & von Jagow (1987) . Samples were denatured for 5 min at 37 °C in SDS loading buffer prior to electrophoresis, and gels were stained with Coomassie brilliant blue to visualize the polypeptides. The c-type cytochromes were revealed via intrinsic peroxidase activity of their haem group, using 3,3',5,5'-tetramethylbenzidine (TMBZ) and H2O2 (Thomas et al., 1976
).
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RESULTS |
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Difference spectra and redox potentiometry
Reduced-minus-oxidized difference spectra recorded under different redox conditions (ascorbate and dithionite as reducing agents) of membranes from KF707 grown in LB broth and harvested at OD6602 are in Fig. 4(a)
. The spectra were recorded from samples with identical protein concentrations (1 mg ml-1) and are thus directly comparable. The presence of c- and b-type haems with
-bands in their reduced form at 552 nm (peak) and 560 nm (shoulder), respectively, is apparent. In none of the spectra were signals observed which would have indicated the presence of aa3-type haems (
-band in their reduced form at 602605 nm). As shown in Fig. 4(b)
, the reduced-minus-oxidized difference spectra of membranes isolated from cells grown in the presence of 35 µg potassium tellurite ml-1 (OD660
2·4) were qualitatively different from the controls (Fig. 4a
). In particular, the
-band of c-type haems at 552 nm was considerably decreased compared to that of b-type haems (560 nm): the cyt c/b ratio [based on nmol haem (mg protein)-1] was 0·9, as against a ratio of 1·65 in membranes from control cells (Fig. 4a
).
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Analyses at pH 7·0 (552540 nm) of the spectra obtained at controlled ambient potentials in membranes from cells grown in the presence of tellurite indicated the presence of components with Em,7 of +380±4 and +297±2 mV and relative contributions of 22% and 78%, respectively (data not shown). Notably, the amount of these two high-potential components was 50% lower than the equivalent components of membranes from control cells (see also Fig. 4a, b
and Table 2
below). Analogously, the number of b-type haems resolved at 560575 nm (pH 7·0) in membranes from tellurite-grown cells (Fig. 6
, filled circles) was similar to the number seen in control membranes (Em,7 of +420±8, +280±4 and+74±1, with contributions of 9, 25, 65%, respectively) with some significant quantitative variation, i.e. the amount of the highest-potential b-type haems [0·9 nmol (mg protein)-1] was lower than the amount of the equivalent components in control membranes [1·2 nmol (mg protein)-1]. Additionally, redox titrations at pH 9·0 (Fig. 6
, open circles) revealed the presence of an extra b-type haem along with minor variations of the two high-potential haems (Em,9 of +390±10 and +310±15 mV) and a further resolution of the signal titrated at +74 mV into two components (Em,9 of +40±5 and -8±3 mV); indeed a b-type species with Em of +203±5 mV was evident at pH 9·0 due to a shift to lower potentials (30 mV slope per pH unit) of components at +40±5 and -8±3 mV (pH 9·0). Thus, membranes from KF707 cells grown in the presence of potassium tellurite show at least two major specific features: (i) the presence of a new high-potential b-type haem (cyt b203 at pH 9·0), and (ii) a consistent reduction of the amount of the highest-potential b-type haems and of the c-type haem complement (see also Table 2
and Fig. 7
).
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Redox chain of membranes from cultures harvested in the early exponential growth phase in LB medium plus tellurite
The functional, spectroscopic and thermodynamic data presented in the preceding paragraphs were obtained in membranes from KF707 cells harvested in the late exponential or stationary growth phase (OD660 2). To test whether the changes of the respiratory chain were due to tellurite reduction activity occurring from mid-exponential phase onwards or were the result of a metabolic cell adaptation from the beginning of growth, membranes from cells grown in the presence or absence of tellurite were harvested at the beginning of the exponential growth phase (OD660 0·5) and analysed. Interestingly, most of the features seen in membranes from cells harvested at the stationary growth phase (OD660 2) were already apparent at the beginning of the exponential phase. The data in Table 2 summarize some of our results. In particular, tellurite-grown cells have a strong cyanide-resistant oxidative activity (59% and 64% of activity with 10 µM KCN and/or 5 µM antimycin A, respectively) while most of the NADH-dependent respiration in control cells is catalysed by the cyt c oxidase (only 22% of activity with 10 µM KCN); in line with this, the cyt c oxidase activity is almost three times lower in membranes from tellurite-grown cells than in the control, in parallel with a consistent decrease (7075%) of both soluble and membrane-bound cytochromes c.
Further studies indicated that changes of the redox-chain components in membranes from cells grown in LB medium supplemented with tellurite can be reversed by transfer of cells into LB medium without tellurite. This conclusion was obtained by re-inoculating cells grown in LB+tellurite (35 µg ml-1), and harvested at the stationary growth phase, into LB liquid medium without tellurite. Membranes isolated from the latter type of cultures during either the early- or late-exponential growth phase showed respiratory activities, inhibitor sensitivities, difference redox spectra, and redox titrations identical to those reported for those from cultures re-inoculated several times into LB media without tellurite (data not shown). These results were interpreted as showing that the effects induced by tellurite on the functional and structural organization of the KF707 redox chain are likely to be the result of a metabolic pressure and not the result of mutations generated by tellurite, although this possibility, at present, cannot be excluded a priori.
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DISCUSSION |
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The main conclusions concerning the functional aspects of the respiratory chain of cells grown in the absence of tellurite can be summarized as follows: (a) the respiratory chain of KF707 is branched because three oxidative pathways can be distinguished by their cyanide sensitivities; (b) a first branch occurs before the antimycin-A-sensitive site (cyt bc1 complex) because the NADH-dependent respiration is not completely blocked (75% inhibition) by this inhibitor; (c) the second branch is at the level of cytochromes c (most likely soluble cyt c+membrane-bound cyt cy; see below) because two cyt c oxidases can be distinguished by their cyanide sensitivities; (d) the most cyanide-sensitive cyt c oxidase contributes only 20% of the total respiratory activity of cells harvested at the stationary growth phase.
The thermodynamic and SDS-PAGE analyses of membrane fragments from KF707 revealed a cyt c composition similar to that observed in other species of Pseudomonas and Rhodobacter (Zannoni, 1989 , 1995
; Hochkoeppler et al., 1995
). Indeed, at least four membrane-bound c-type cytochromes (operationally defined as c1, cp, co and cy) of Mr 33000, 32000, 27500 and 24000 can be distinguished by TMBZ-SDS-PAGE analysis along with a soluble c-type species with its
band in the reduced form at 551·5 nm isolated from the soluble fraction (Em,7 +291 mV, Mr 10000) and a membrane-bound c-type haem of unknown function and Mr 17000. Unfortunately, only one membrane-bound c-type haem is thermodynamically resolvable [Em,7 +379±6 mV, 0·3 nmol (mg protein)-1] whereas all the rest of the cyt c type complement titrates as a single unresolved component at pH 7·0 with Em of +300±1 mV (n=2) contributing about 80% of the total signal at 552540 nm. The b-type complement of strain KF707 contains at least five haems with Em,7 of +395±4, +318±3,+203±6, +124±8 and +64±2 mV. These latter two Em,7 values are extrapolated from data obtained at pH 9·0 (30 mV slope per pH unit from 7·0 to 9·0) while the b-type haem at +203 mV can only be seen at pH 9·0 in cells grown in the presence of tellurite (see below) thanks to a 60 mV shift to lower values of haems at +124 and +64 mV (pH 7·0). By analogy with previously published data on b-type species present in the respiratory chain of R. capsulatus and R. sphaeroides (Zannoni, 1995
) the two high-potential haems at +395 and +318 mV are likely to be involved in oxygen dioxide reducing activities, although it is difficult to state whether they belong to the same redox complex, i.e. the cbb3-type cyt oxidase, or they are part of two different oxidases. Indeed, an interesting but still unexplained result of this study concerns the presence of two cyt c oxidase activities, this conclusion being based on the cyanide titration patterns of NADH- and reduced cyt c-dependent oxidation activities. Thus, the actual features of the b-type haems catalysing these two oxidases remain at present elusive.
The detailed mechanism of tellurite reduction by bacterial cells (a four-electron reaction) is as yet unknown (Turner, 2001 ). Early work by Moore & Kaplan (1994)
indicated that the extent of reduction in R. sphaeroides was inversely related to the oxidation state of the carbon source and it was also dependent on FADH2 oxidation activity, while recent work on several tellurite-resistant Gram-negative bacteria (genera Pseudomonas, Agrobacterium, Erwinia and Escherichia) suggested an active role of the respiratory electron-transport chain in the accumulation of elemental tellurium and that the position of the catalytic centres of terminal membrane-bound oxidases correlates with the periplasmic or cytoplasmic location of tellurium crystallite granules (Trutko et al., 2000
). On the other hand, the authors of the latter study also reported that specific activation of cyt c activity in cells of P. aeruginosa lowers the tellurium content of cells, which clearly indicates that reduction of tellurite and oxygen dioxide compete for the same pool of reducing equivalents before the cyt c oxidase level. This reasoning is also consistent with the expected electrochemical properties of tellurite in aqueous solution at pH 7·0 (standard reduction potential at basic pHs of the couple Te/
=-0·42 V); based on the dissociation constants of tellurous acid (3x10-3 and 2x10-8 for k1 and k2, respectively), potassium tellurite at pH 7·0 should be mainly present in the form of
and
(104/1 ratio) with no Te4+ present due to its instability in water; this means that the standard potentials of the redox couples free to react with the respiratory components would be too low (estimated at -0·12 V at pH 7·0) to be reduced by the catalytic centres of membrane-bound oxidases (Poole, 1988
) as also previously suggested by others (Trutko et al., 2000
). On the other hand, it is reasonable to presume that the periplasmic pH of growing cells would be acidic (at least two pH units lower than cytosolic pH) due to proton extrusion. This local pH might therefore affect the equilibrium of the different forms of tellurium, shifting to more positive values the potentials of the redox couples present so as to be suitable oxidants for the redox-chain components. Keeping these considerations in mind, it is therefore particularly difficult to predict the interaction of
with the respiratory redox complexes. At the present experimental stage we are therefore tempted to suggest that the most likely thermodynamic interaction, if any (see also below) would be at the quinone pool level (Em,7 of the redox couples Q·-/Q and Q/QH2 of -200 and +90 mV, respectively) in the light of the following results obtained with membranes from KF707 cells grown in the presence of tellurite, namely: (a) the cyt c oxidase activity is drastically decreased (50%) while the cyanide-resistant oxidase activity is enhanced, catalysing most (6065%) of the NADH-dependent respiration; (b) cyt c- and b-type components linked to the upper part of the redox chain are 75% and 50% decreased, respectively; SDS-PAGE analysis shows that this drastic decrease involves specifically the soluble cyt c-type subunit (Mr 10000), and the membrane-bound subunits with molecular masses of 33 and 17 kDa; (c) the amount of cyt b395 plus b318 is reduced while a new cyt b (Em,9=+203 mV) is present; this suggests that the haems with the highest potential are involved in cyt c oxidase activity while cyt b203 would play a role in the cyanide-resistant oxidase. In addition to these specific effects on the respiratory components we have also shown that: (a) tellurite is accumulated by cells of KF707 as granules of elemental tellurium, (b) tellurite reduction to tellurium and cytoplasmic accumulation of tellurium are phenomena restricted to the midlate-exponential and stationary growth phases although functional and structural modifications of the respiratory chain are already evident in membranes from cells harvested at the beginning of the exponential growth phase (OD660 0·5), and (c) the changes observed in membranes from cells grown in the presence of tellurite can be reversed by transferring cells into LB medium without tellurite. These observations, taken together, tend to indicate that the functional and structural variations of the respiratory chain of P. pseudoalcaligenes KF707 cells grown in the presence of tellurite and the accumulation of elemental tellurium are separate events. This raises the question whether the modifications observed are specifically required for survival in the presence of tellurite or simply reflect toxic effects of the oxyanion on metabolic pathways not directly related to the respiratory system. We have observed that KF707 cells pre-adapted to grow in the presence of tellurite start growing immediately when transferred into media containing tellurite; conversely, KF707 cells grown in media with no tellurite show a lag period of about 20 h before they start growing. On the other hand, KF707 cells pre-adapted to grow in the presence of tellurite do not show any initial lag period in LB broth and they have an orthodox redox chain after growth in LB broth for a few generations (OD660
0·5). This suggests that the variations observed at the level of the respiratory chain in KF707 cells grown in the presence of tellurite are the result of its direct and/or indirect effect on respiratory genes, a phenomenon not necessarily linked with the capacity to grow in the presence of tellurite. In this respect, it is difficult to explain the general decrease of the haem complement in terms of specific metabolic requirements for survival in the presence of tellurite. Further studies are therefore necessary to establish whether modifications of the redox-chain complement are indicative of an active role of respiration in tellurite reduction, as suggested by Trutko et al. (2000)
, or they constitute, as the present study suggests, a secondary effect of tellurite on metabolic functions such as the thiol-redox buffering system (Turner et al., 1995
).
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ACKNOWLEDGEMENTS |
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Received 12 December 2001;
revised 11 February 2002;
accepted 21 February 2002.