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The highly toxic oxyanion tellurite (TeO 2−3 ) enters the phototrophic bacterium Rhodobacter capsulatus via an as yet uncharacterized monocarboxylate transport system

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Abstract

The facultative phototroph Rhodobacter capsulatus takes up the highly toxic oxyanion tellurite when grown under both photosynthetic and respiratory growth conditions. Previous works on Escherichia coli and R. capsulatus suggested that tellurite uptake occurred through a phosphate transporter. Here we present evidences indicating that tellurite enters R. capsulatus cells via a monocarboxylate transport system. Indeed, intracellular accumulation of tellurite was inhibited by the addition of monocarboxylates such as pyruvate, lactate and acetate, but not by dicarboxylates like malate or succinate. Acetate was the strongest tellurite uptake antagonist and this effect was concentration dependent, being already evident at 1 μM acetate. Conversely, tellurite at 100 μM was able to restrict the acetate entry into the cells. Both tellurite and acetate uptakes were energy dependent processes, since they were abolished by the protonophore FCCP and by the respiratory electron transport inhibitor KCN. Interestingly, cells grown on acetate, lactate or pyruvate showed a high level resistance to tellurite, whereas cells grown on malate or succinate proved to be very sensitive to the oxyanion. Taking these data together, we propose that: (a) tellurite enters R. capsulatus cells via an as yet uncharacterized monocarboxylate(s) transporter, (b) competition between acetate and tellurite results in a much higher level of tolerance against the oxyanion and (c) the toxic action of tellurite at the cytosolic level is significantly restricted by preventing tellurite uptake.

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Abbreviations

ROS:

Reactive oxygen species

DDTC:

Diethyldithiocarbamate

NEM:

N-ethylmaleimide

FCCP:

Carbonyl cyanide-p-trifluoromethoxyphenyl-hydrazone

References

  • Avazéri C, Turner RJ, Pommier J, Weiner JH, Giordano G, Verméglio A (1997) Tellurite reductase activity of nitrate reductase is responsible for the basal resistance of Escherichia coli to tellurite. Microbiology 143:1181–1189

    Article  PubMed  Google Scholar 

  • Borghese R, Borsetti F, Foladori P, Ziglio G, Zannoni D (2004) Effects of the metalloid oxyanion tellurite (TeO 2−3 ) on growth characteristics of the phototrophic bacterium Rhodobacter capsulatus. Appl Environ Microbiol 70:6595–6602

    Article  PubMed  CAS  Google Scholar 

  • Borsetti F, Borghese R, Francia F, Randi MR, Fedi S, Zannoni D (2003a) Reduction of potassium telurite to elemental tellurium and its effect on the plasma membrane redox components of the facultative phototroph Rhodobacter capsulatus. Protoplasma 221:153–161

    Article  PubMed  CAS  Google Scholar 

  • Borsetti F, Toninello A, Zannoni D (2003b) Tellurite uptake by cells of the facultative phototroph Rhodobacter capsulatus is a ΔpH-dependent process. FEBS Lett 554:315–318

    Article  PubMed  CAS  Google Scholar 

  • Borsetti F, Tremaroli V, Michelacci F, Borghese R, Winterstein C, Daldal F, Zannoni D (2005) Tellurite effects on Rhodobacter capsulatus cell viability and superoxide dismutase activity under oxidative stress conditions. Res Microbiol 156:807–813

    Article  PubMed  CAS  Google Scholar 

  • Cadenas E (1989) Biochemistry of oxygen toxicity. Annu Rev Biochem 58:79–110

    Article  PubMed  CAS  Google Scholar 

  • Chiong M, González E, Barra R, Vásquez C (1988) Purification and biochemical characterization of tellurite-reducing activities from Thermus thermophilus HB8. J Bacteriol 170:3269–3273

    PubMed  CAS  Google Scholar 

  • Di Tomaso G, Fedi S, Carnevali M, Manegatti M, Taddei C, Zannoni D (2002) The membrane-bound respiratory chain of Pseudomonas pseudoalcaligenes KF707 cells grown in the presence or absence of potassium tellurite. Microbiology 148:1699–1708

    PubMed  CAS  Google Scholar 

  • Fridovich L (1995) Superoxide radical and superoxide dismutases. Annu Rev Biochem 64:97–112

    Article  PubMed  CAS  Google Scholar 

  • Hosie AHF, Allaway D, Poole PS (2002) A monocarboxylate permease of Rhizobium leguminosarum is the first member of a new subfamily of transporters. J Bacteriol 184:5436–5448

    Article  PubMed  CAS  Google Scholar 

  • Imlay JA, Linn S (1988) DNA damage and oxygen radical toxicity. Science 240:1302–1309

    Article  PubMed  CAS  Google Scholar 

  • Ingham CJ, Armitage JP (1987) Involvement of transport in Rhodobacter sphaeroides chemotaxis. J Bacteriol 169:5801–5807

    PubMed  CAS  Google Scholar 

  • Kessi J, Ramuz M, Wehrli E, Spycher M, Bachofen R (1999) Reduction of selenite and detoxification of elemental selenium by the phototrophic bacterium Rhodospirillum rubrum. Appl Environ Microbiol 65:4734–4740

    PubMed  CAS  Google Scholar 

  • Lloyd JR, Mabbett AN, Williams DR, Macaskie LE (2001) Metal reduction by sulphate-reducing bacteria: physiological diversity and metal specificity. Hydrometallurgy 59:327–337

    Article  CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    PubMed  CAS  Google Scholar 

  • Moore MD, Kaplan S (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

    PubMed  CAS  Google Scholar 

  • Moore MD, Kaplan S (1994) Members of the family Rhodospirillaceae reduce heavy metal oxyanions to maintain redox poise during photosynthetic growth: these metal-reducing bacteria may help to remediate environmental pollution. ASM News 60:17–23

    Google Scholar 

  • O’Gara JP, Gomelsky M, Kaplan S (1997) Identification and molecular genetic analysis of multiple loci contributing to high-level tellurite resistance in Rhodobacter sphaeroides 2.4.1. Appl Environ Microbiol 63:4713–4720

    PubMed  CAS  Google Scholar 

  • Pearion CT, Jablonski PE (1999) High level, intrinsic resistance of Natronococcus occultus to potassium tellurite. FEMS Microbiol Lett 174:19–23

    Article  CAS  Google Scholar 

  • Rojas DM, Vásquez CC (2005) Sensitivity to potassium tellurite of Escherichia coli cells deficient in CSD, CsdB and IscS cysteine desulfurases. Res Microbiol 156:465–471

    Article  PubMed  CAS  Google Scholar 

  • Summers AO, Jacoby GA (1977) Plasmid-determined resistance to tellurium compounds. J Bacteriol 128:276–281

    Google Scholar 

  • Tantaleán JC, Araya MA, Saavedra CP, Fuentes DE, Pérez JM, Calderón IL, Youderian P, Vásquez CC (2003) The Geobacillus stearothermophilus V iscS gene, encoding cysteine desulfurase, confers resistance to potassium tellurite in Escherichia coli K-12. J Bacteriol 185:5831–5837

    Article  PubMed  CAS  Google Scholar 

  • Taylor DE (1999) Bacterial tellurite resistance. Trends Microbiol 7:111–115

    Article  PubMed  CAS  Google Scholar 

  • Tomás JM, Kay WW (1986) Tellurite susceptibility and non-plasmid-mediated resistance in Escherichia coli. Antimicrob Agents Chemother 30:127–131

    PubMed  Google Scholar 

  • Turner RJ (2001) Tellurite toxicity and resistance in Gram-negative bacteria. Rec Res Dev Microbiol 5:69–77

    CAS  Google Scholar 

  • Turner RJ, Weiner JH, Taylor DE (1992) Use of diethyldithiocarbamate for quantitative determination of tellurite uptake by bacteria. Anal Biochem 204:292–295

    Article  PubMed  CAS  Google Scholar 

  • Turner RJ, Weiner JH, Taylor DE (1995) The tellurite-resistance determinants tehAtehB and klaAklaBtelB have different biochemical requirements. Microbiology 141:3133–3140

    PubMed  CAS  Google Scholar 

  • Turner RJ, Weiner JH, Taylor DE (1999) Tellurite-mediated thiol oxidation in Escherichia coli. Microbiology 145:2549–2557

    PubMed  CAS  Google Scholar 

  • Vásquez CC, Saavedra CP, Loyola CA, Araya MA, Pichuantes S (2001) The product of the cysK gene of Bacillus stearothermophilus V mediates potassium tellurite resistance in Escherichia coli. Curr Microbiol 43:418–423

    Article  PubMed  CAS  Google Scholar 

  • Walter EG, Taylor DE (1992) Plasmid-mediated resistance to tellurite: expressed and cryptic. Plasmid 27:52–64

    Article  PubMed  CAS  Google Scholar 

  • Weaver PF, Wall JD, Gest H (1975) Characterization of Rhodopseudomonas capsulata. Arch Microbiol 105:207–216

    Article  PubMed  CAS  Google Scholar 

  • Willison JC (1988) Pyruvate and acetate metabolism in the photosynthetic bacterium Rhodobacter capsulatus. J Gen Microbiol 134:2429–2439

    CAS  Google Scholar 

  • Yurkov V, Jappé J, Verméglio A (1996) Tellurite resistance and reduction by obligately aerobic photosynthetic bacteria. Appl Environ Microbiol 62:4195–4198

    PubMed  CAS  Google Scholar 

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Acknowledgments

We thank the Ministero Istruzione Università e Ricerca (MIUR) for supporting this work (Grant: PRIN 2005–2006). D.M. is a recipient of a PhD fellowship from the University of Bologna (PhD School of Biological Sciences, Biomedicine and Biotechnology; XXI program: 2006–2008).

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Authors and Affiliations

  1. Department of Biology, University of Bologna, Via Irnerio 42, 40126, Bologna, Italy

    Roberto Borghese, Daniele Marchetti & Davide Zannoni

  2. Interdepartmental Center of Research in Environmental Sciences (CIRSA), University of Bologna, 48100, Ravenna, Italy

    Roberto Borghese

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  1. Roberto Borghese
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  2. Daniele Marchetti
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  3. Davide Zannoni
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Correspondence to Roberto Borghese.

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Communicated by Jörg Overmann.

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Borghese, R., Marchetti, D. & Zannoni, D. The highly toxic oxyanion tellurite (TeO 2−3 ) enters the phototrophic bacterium Rhodobacter capsulatus via an as yet uncharacterized monocarboxylate transport system. Arch Microbiol 189, 93–100 (2008). https://doi.org/10.1007/s00203-007-0297-7

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  • DOI: https://doi.org/10.1007/s00203-007-0297-7

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