Enzymic systems proposed to be involved in the dissimilatory reduction of selenite in the purple non-sulfur bacteria Rhodospirillum rubrum and Rhodobacter capsulatus
Various enzymic systems, such as nitrite reductase, sulfite reductase and glutathione reductase, have been proposed for, or suspected to be involved in, the reduction of selenite in bacteria. As alphaproteobacteria have been shown to be highly tolerant to transition metal oxyanions, it seemed interesting to investigate the hypothetical involvement of these different enzymes in the reduction of selenite in the purple non-sulfur bacteria Rhodospirillum rubrum and Rhodobacter capsulatus. The hypothetical involvement of nitrite reductase and sulfite reductase in the reduction of selenite in these bacteria was investigated by analysing the effects of nitrite and sulfite amendments on the growth and kinetics of selenite reduction. The reduction of selenite was not concomitant with that of either sulfite or nitrite in Rs. rubrum, suggesting that the reduction pathways operate independently. In Rb. capsulatus, strong interactions were observed between the nitrite reduction and selenite reduction pathways. However, in both organisms, selenite reduction took place during both the growth phase and the stationary phase, indicating that selenite metabolism is constitutively expressed. In contrast, neither nitrite nor sulfite was transformed during stationary phase, suggesting that the metabolism of both ions is induced, which implies that identical reduction pathways for selenite and nitrite or selenite and sulfite are excluded. Buthionine sulfoximine (BSO, S-n-butyl homocysteine sulfoximine), a specific inhibitor of glutathione synthesis, was used to depress the intracellular glutathione level. In stationary-phase cultures of both Rs. rubrum and Rb. capsulatus amended with BSO, the rate of reduction of selenite was slowed, indicating that glutathione may be involved in the dissimilatory reduction of selenite in these organisms. The analysis of the headspace gases of the cultures indicated that the synthesis of methylated selenium compounds was prevented in the presence of 3·0 mM BSO in both organisms, implying that glutathione is also involved in the transformation of selenite to volatile selenium compounds.
AkerboomT. P. M, SiesH.
1981; Assay of glutathione, glutathione disulfide, and glutathione mixed disulfides in biological samples. Methods Enzymol 77:373–382
BébienM,
ChauvinJ.-P, AdrianoJ.-M, GrosseS, VerméglioA.
2001; Effect of selenite on growth and protein synthesis in the phototrophic bacterium Rhodobacter sphaeroides . Appl Environ Microbiol 67:4440–4447[CrossRef]
BébienM,
LagnielG, GarinJ, TouatiD, VerméglioA,
LabarreJ.
2002; Involvement of superoxide dismutases in the response of Escherichia coli to selenium oxides. J Bacteriol 184:1556–1564[CrossRef]
BjörnstedtM,
KumarS, HolmgrenA.
1992; Selenodiglutathione is a highly efficient oxidant of reduced thioredoxin and a substrate for mammalian thioredoxin reductase. J Biol Chem 267:8030–8034
Carmel-HarelO, StorzG.
2000; Roles of the glutathione- and thioredoxin-dependent reduction systems in the Escherichia coli and Saccharomyces cerevisiae responses to oxidative stress. Annu Rev Microbiol 54:439–461[CrossRef]
DeMoll-DeckerH, MacyJ. M.
1993; The periplasmic nitrite reductase of Thauera selenatis may catalyze the reduction of selenite to elemental selenium. Arch Microbiol 160:241–247
DunganR. S, YatesS. R, FrankenbergerW. TJr.
2003; Transformations of selenate and selenite by Stenotrophomonas maltophilia isolated from a seleniferous agricultural drainage pond sediment. Environ Microbiol 5:287–295[CrossRef]
EtchebehereC, TiedjeJ.
2005; Presence of two different active nir S nitrite reductase genes in a denitrifying Thauera sp. from a high-nitrate-removal-rate reactor. Appl Environ Microbiol 71:5642–5645[CrossRef]
FergusonS. J, JacksonJ. B, McEwanA. G.
1987; Anaerobic respiration in the Rhodospirillaceae: characterisation of pathways and evaluation of roles in redox balancing during photosynthesis. FEMS Microbiol Rev 46:117–143[CrossRef]
GantherH. E.
1971; Reduction of the selenotrisulfide derivative of glutathione to a persulfide analog by glutathione reductase. Biochemistry 10:4089–4098[CrossRef]
GriffithO. W, MeisterA.
1979; Potent and specific inhibition of glutathione synthesis by buthionine sulfoximine (S -n-butyl homocysteine sulfoximine). J Biol Chem 254:7558–7560
HarrisonG. I, LaishleyE. J, KrouseH. R.
1980; Stable isotope fractionation by Clostridium pasteurianum . 3.Effect of SeO32– on the physiology and associated sulfur isotope fractionation during SeO32– and SeO42– reductions. Can J Microbiol 26:952–958[CrossRef]
HarrisonG, CurleC, LaishleyE. J.
1984; Purification and characterization of an inducible dissimilatory type sulfite reductase from Clostridium pasteurianum . Arch Microbiol 138:72–78[CrossRef]
KarrE. A, SattleyW. M, JungD. O, MadiganM. T, AchenbachL. A.
2003; Remarkable diversity of phototrophic purple bacteria in a permanently frozen antarctic lake. Appl Environ Microbiol 69:4910–4914[CrossRef]
KellyB. S, AntholineW. E, GriffithO. W.
2002; Escherichia coli γ -glutamylcysteine synthetase. Two active site metal ions affect substrate and inhibitor binding. J Biol Chem 277:50–58[CrossRef]
KessiJ, HanselmannK. W.
2004; Similarities between the abiotic reduction of selenite with glutathione and the dissimilatory reaction mediated by Rhodospirillum rubrum and Escherichia coli . J Biol Chem 279:50662–50669[CrossRef]
KessiJ, RamuzM, WehrliE, SpycherM, BachofenR.
1999; Reduction of selenite and detoxification of elemental selenium by the phototrophic bacterium Rhodospirillum rubrum . Appl Environ Microbiol 65:4734–4740
Libreros-MinottaC. A, PardoJ. P, Mendoza-HernándezG, RendónJ. L.
1992; Purification and characterization of glutathione reductase from Rhodospirillum rubrum . Arch Biochem Biophys 298:247–253[CrossRef]
LosiM. E, FrankenbergerW. TJr.
1997; Reduction of selenium oxyanions by Enterobacter cloacae SLD1a-1: isolation and growth of the bacterium and its expulsion of selenium particles. Appl Environ Microbiol 63:3079–3084
MooreM. D, KaplanS.
1992; Identification of intrinsic high-level resistance to rare-earth oxides and oxyanions in members of the class Proteobacteria : characterization of tellurite, selenite, and rhodium sesquioxide reduction in Rhodobacter sphaeroides . J Bacteriol 174:1505–1514
NewtonG. L, FaheyR. C.
1989; Glutathione in prokaryotes. In Glutathione: Metabolism and Physiological Functions pp 69–77 Edited by
ViñaJ.
Boca Raton: CRC Press;
OhlendorfH. M.
1989; Bioaccumulation and effects of selenium in wildlife. In Selenium in Agriculture and the Environment pp 133–177 Edited by
JacobsL. W.
Madison, WI: American Society of Agronomy;
O'TooleD, RaisbeckM. F.
1998; Magic numbers, elusive lesions: comparative pathology and toxicology of selenosis in waterfowl and mammalian species. In Environmental Chemistry of Selenium pp 355–395 Edited by
FrankenbergerW. T.,
EngbergR. A.Jr
New York: Marcel Dekker;
PeckH. D, TedroS, KamenM. DJr. 1974; Sulfite reductase activity in extracts of various photosynthetic bacteria. Proc Natl Acad Sci U S A 71:2404–2406[CrossRef]
PreussM, KlemmeJ.-H.
1983; Purification and characterization of a dissimilatory nitrite reductase from the phototrophic bacterium Rhodopseudomonas palustris . Z Naturforsch (C) 38:933–938
SchwintnerC, SabatyM, BernaB, CahorsS, RichaudP.
1998; Plasmid content and localization of the genes encoding the denitrification enzymes in two strains of Rhodobacter sphaeroides . FEMS Microbiol Lett 165:313–321[CrossRef]
TomeiF. A, BartonL. L, LemanskiC. L, ZoccoT. G.
1992; Reduction of selenate and selenite to elemental selenium by Wolinella succinogenes . Can J Microbiol 38:1328–1333[CrossRef]
TomeiF. A, BartonL. L, LemanskiC. L, ZoccoT. G, FinkN. H, SillerudL. O.
1995; Transformation of selenate and selenite to elemental selenium by Desulfovibrio desulfuricans . J Ind Microbiol 14:329–336[CrossRef]
Van Fleet-StalderV, GürleyükH, BachofenR, ChasteenT. G.
1997; Effects of growth conditions on production of methyl selenides in cultures of Rhodobacter sphaeroides . J Ind Microbiol Biotechnol 19:98–103[CrossRef]
WoeseC. R, StackebrandtE, WeisburgW. G. 8 other authors1984; The phylogeny of purple bacteria: the alpha subdivision. Syst Appl Microbiol 5:315–326[CrossRef]
Enzymic systems proposed to be involved in the dissimilatory reduction of selenite in the purple non-sulfur bacteria Rhodospirillum rubrum and Rhodobacter capsulatus