Involvement of the respiratory chain of gram-negative bacteria in the reduction of tellurite

Abstract

The terminal oxidases of the respiratory chain of seven strains of gram-negative bacteria were shown to be involved in the reduction of tellurite. The rate of tellurite reduction correlated with the intensity of respiration. The inhibitors of terminal oxidases, carbon monoxide and cyanide, inhibited the reduction of tellurite. In Pseudomonas aeruginosa PAO ML4262 and P. aeruginosa PAO ML4262 (pBS 10), the respiratory chain was found to contain three types of cytochrome c, one of which (the carbon monoxide-binding cytochrome c) was involved in the reduction of tellurite. Agrobacterium tumefaciens VKM B-1219, P. aeruginosa IBPM B-13, and Escherichia coli G0-102bd++ cells contained oxidases aa3, bb3, and bd, respectively. The respiratory chain of other strains contained two oxidases: E. coli DH5alpha of bb3- and bd-type, and Erwinia carotovora VKM B-567 of bo3- and bd-type. All the strains under study reduced tellurite with the formation of tellurium crystallites. Depending on the position of the active center of terminal oxidases in the plasma membrane, the crystallites appeared either in the periplasmic space [P. aeruginosa PAO ML4262 and P. aeruginosa PAO ML4262 (pBS10)], or on the outer surface of the membrane (A. tumefaciens VKM B-1219 and P. aeruginosa IBPM B-13), its inner surface (E. coli G0-102bd++), or on both surfaces (E. coli DHaalpha and E. carotovora VKM B-567).

The membrane-bound respiratory chain of Pseudomonas pseudoalcaligenes KF707 cells grown in the presence or absence of potassium tellurite This work is dedicated to my friend and colleague Franco Tatò, prematurely deceased on 7 July 2001.

“…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 7n0 (standard reduction potential at basic pHs of the couple Te\TeO# − $ l k0n42 V) ; based on the dissociation constants of tellurous acid (3i10 −$ and 2i10 −) for k " and k # , respectively), potassium tellurite at pH 7n0 should be mainly present in the form of HTeO − $ and TeO# − $ (10%\1 ratio) with no Te% + 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 k0n12 V at pH 7n0) 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.…”

“…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).…”

“…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 FADH # 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 membranebound 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.…”

“…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).…”

An inducible tellurite-resistance operon in Proteus mirabilis

“…The oxyanions of tellurium, tellurite (K 2 TeO 3 ) and tellurate, are highly toxic for most micro-organisms, causing direct oxidation of cellular thiols (Taylor, 1999;Turner et al, 1999) or, following reduction to telluride, is inappropriately incorporated in place of sulfur in amino acids (Garberg et al, 1999;Taylor, 1999). Tellurite can also be reduced to the metal by nitrate reductase (Avazeri et al, 1997) or the terminal oxidases of most Gram-negative bacteria (Trutko et al, 2000;Di Tomaso et al, 2002). Resistant bacteria produce jet-black colonies on solid medium supplemented with K 2 TeO 3 as the result of internal deposition of elemental tellurium (Hill et al, 1993;Whelan et al, 1995).…”