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Volume 167, Issue 2

The putative phosphate transporter PitB (PP1373) is involved in tellurite uptake in KT2440 Free

Abstract

Tellurium oxyanions are chemical species of great toxicity and their presence in the environment has increased because of mining industries and photovoltaic and electronic waste. Recovery strategies for this metalloid that are based on micro-organisms are of interest, but further studies of the transport systems and enzymes responsible for implementing tellurium transformations are required because many mechanisms remain unknown. Here, we investigated the involvement in tellurite uptake of the putative phosphate transporter PitB (PP1373) in soil bacterium KT2440. For this purpose, through a method based on the CRISPR/Cas9 system, we generated a strain deficient in the gene and characterized its phenotype on exposing it to varied concentrations of tellurite. Growth curves and transmission electronic microscopy experiments for the wild-type and Δ strains showed that both were able to internalize tellurite into the cytoplasm and reduce the oxyanion to black nano-sized and rod-shaped tellurium particles, although the Δ strain showed an increased resistance to the tellurite toxic effects. At a concentration of 100 μM tellurite, where the biomass formation of the wild-type strain decreased by half, we observed a greater ability of Δ to reduce this oxyanion with respect to the wild-type strain (~38 vs ~16 %), which is related to the greater biomass production of Δ and not to a greater consumption of tellurite per cell. The phenotype of the mutant was restored on over-expressing . In summary, our results indicate that PitB is one of several transporters responsible for tellurite uptake in KT2440.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): phosphate transporter , pitB , Pseudomonas putida , tellurite and tellurium nanostructures
Funding
This study was supported by the:
  • Vicerrectoría de Investigación, Universidad de Costa Rica (Award 809-B7-A43)
    • Principle Award Recipient: MaxChavarría
© 2021 The Authors
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2020-12-21
2024-04-24
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References

  1. Cucchiella F, D’Adamo I, Lenny Koh SC, Rosa P. Recycling of WEEEs: an economic assessment of present and future e-waste streams. Renew Sustain Energy Rev 2015; 51:263–272 [View Article]
     [Google Scholar]
  2. Chasteen TG, Fuentes DE, Tantaleán JC, Vásquez CC. Tellurite: history, oxidative stress, and molecular mechanisms of resistance. FEMS Microbiol Rev 2009; 33:820–832 [View Article][PubMed]
     [Google Scholar]
  3. Maltman C, Yurkov V. Extreme environments and high-level bacterial tellurite resistance. Microorganisms 2019; 7:601–624 [View Article][PubMed]
     [Google Scholar]
  4. Presentato A, Turner RJ, Vásquez CC, Yurkov V, Zannoni D. Tellurite-dependent blackening of bacteria emerges from the dark ages. Environ Chem 2019; 16:266–288 [View Article]
     [Google Scholar]
  5. Di Tomaso G, Fedi S, Carnevali M, Manegatti M, Taddei C et al. The membrane-bound respiratory chain of Pseudomonas pseudoalcaligenes KF707 cells grown in the presence or absence of potassium tellurite. Microbiology 2002; 148:1699–1708 [View Article][PubMed]
     [Google Scholar]
  6. Basnayake RST, Bius JH, Akpolat OM, Chasteen TG. Production of dimethyl telluride and elemental tellurium by bacteria amended with tellurite or tellurate. Appl Organomet Chem 2001; 15:499–510 [View Article]
     [Google Scholar]
  7. Moore MD, Kaplan S. 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 1992; 174:1505–1514 [View Article][PubMed]
     [Google Scholar]
  8. Forootanfar H, Amirpour-Rostami S, Jafari M, Forootanfar A, Yousefizadeh Z et al. Microbial-assisted synthesis and evaluation the cytotoxic effect of tellurium nanorods. Mater Sci Eng C Mater Biol Appl 2015; 49:183–189 [View Article][PubMed]
     [Google Scholar]
  9. Bao H, Lu Z, Cui X, Qiao Y, Guo J et al. Extracellular microbial synthesis of biocompatible CdTe quantum dots. Acta Biomater 2010; 6:3534–3541 [View Article][PubMed]
     [Google Scholar]
  10. Turner RJ, Borghese R, Zannoni D. Microbial processing of tellurium as a tool in biotechnology. Biotechnol Adv 2012; 30:954–963 [View Article][PubMed]
     [Google Scholar]
  11. Trutko SM, Akimenko VK, Suzina NE, Anisimova LA, Shlyapnikov MG et al. Involvement of the respiratory chain of gram-negative bacteria in the reduction of tellurite. Arch Microbiol 2000; 173:178–186 [View Article][PubMed]
     [Google Scholar]
  12. Pérez JM, Calderón IL, Arenas FA, Fuentes DE, Pradenas GA et al. Bacterial toxicity of potassium tellurite: unveiling an ancient enigma. PLoS One 2007; 2:e211 [View Article][PubMed]
     [Google Scholar]
  13. Borsetti F, Francia F, Turner RJ, Zannoni D. The thiol:disulfide oxidoreductase DsbB mediates the oxidizing effects of the toxic metalloid tellurite (TeO3 2-) on the plasma membrane redox system of the facultative phototroph Rhodobacter capsulatus . J Bacteriol 2007; 189:851–859 [View Article][PubMed]
     [Google Scholar]
  14. Taylor DE. Bacterial tellurite resistance. Trends Microbiol 1999; 7:111–115 [View Article][PubMed]
     [Google Scholar]
  15. Turner RJ. Bacterial tellurite resistance. In Kretsinger RH, Uversky VN, Permyakov EA. (editors) Encyclopedia of Metalloproteins New York, NY: Springer; 2013
     [Google Scholar]
  16. Maltman C, Yurkov V. Bioremediation potential of bacteria able to reduce high levels of selenium and tellurium oxyanions. Arch Microbiol 2018; 200:1411–1417 [View Article][PubMed]
     [Google Scholar]
  17. Yurkov VV, Beatty JT. Aerobic anoxygenic phototrophic bacteria. Microbiol Mol Biol Rev 1998; 62:695–724 [View Article][PubMed]
     [Google Scholar]
  18. Elías AO, Abarca MJ, Montes RA, Chasteen TG, Pérez-Donoso JM et al. Tellurite enters Escherichia coli mainly through the PitA phosphate transporter. Microbiologyopen 2012; 1:259–267 [View Article][PubMed]
     [Google Scholar]
  19. Borghese R, Marchetti D, Zannoni D. The highly toxic oxyanion tellurite (TeO3 2-) enters the phototrophic bacterium Rhodobacter capsulatus via an as yet uncharacterized monocarboxylate transport system. Arch Microbiol 2008; 189:93–100 [View Article][PubMed]
     [Google Scholar]
  20. Borghese R, Zannoni D. Acetate permease (ActP) is responsible for tellurite (TeO3 -2) uptake and resistance in cells of the facultative phototroph Rhodobacter capsulatus . Appl Environ Microbiol 2010; 76:942–944 [View Article][PubMed]
     [Google Scholar]
  21. Turner MS, Tan YP, Giffard PM. Inactivation of an iron transporter in Lactococcus lactis results in resistance to tellurite and oxidative stress. Appl Environ Microbiol 2007; 73:6144–6149 [View Article][PubMed]
     [Google Scholar]
  22. Elías A, Díaz-Vásquez W, Abarca-Lagunas MJ, Chasteen TG, Arenas F et al. The ActP acetate transporter acts prior to the PitA phosphate carrier in tellurite uptake by Escherichia coli . Microbiol Res 2015; 177:15–21 [View Article][PubMed]
     [Google Scholar]
  23. Nikel PI, Chavarría M, Danchin A, de Lorenzo V. From dirt to industrial applications: Pseudomonas putida as a synthetic biology chassis for hosting harsh biochemical reactions. Curr Opin Chem Biol 2016; 34:20–29 [View Article][PubMed]
     [Google Scholar]
  24. Nikel PI, Martínez-García E, de Lorenzo V. Biotechnological domestication of Pseudomonads using synthetic biology. Nat Rev Microbiol 2014; 12:368–379 [View Article][PubMed]
     [Google Scholar]
  25. Avendaño R, Chaves N, Fuentes P, Sánchez E, Jiménez JI et al. Production of selenium nanoparticles in Pseudomonas putida KT2440. Sci Rep 2016; 6:1–9 [View Article]
     [Google Scholar]
  26. Belda E, van Heck RGA, José Lopez-Sanchez M, Cruveiller S, Barbe V et al. The revisited genome of Pseudomonas putida KT2440 enlightens its value as a robust metabolic chassis. Environ Microbiol 2016; 18:3403–3424 [View Article][PubMed]
     [Google Scholar]
  27. Nikel P, Chavarría M. Quantitative physiology approaches to understand and optimize reducing power availability in environmental bacteria. Hydrocarbon and Lipid Microbiology Protocols - Springer Protocols Handbooks Berlin, Heidelberg: Springer P; 2015 pp 39–70
     [Google Scholar]
  28. Nikel PI, Chavarría M, Fuhrer T, Sauer U, de Lorenzo V. Pseudomonas putida KT2440 strain metabolizes glucose through a cycle formed by enzymes of the Entner-Doudoroff, Embden-Meyerhof-Parnas, and pentose phosphate pathways. J Biol Chem 2015; 290:25920–25932 [View Article][PubMed]
     [Google Scholar]
  29. Nikel PI, Fuhrer T, Chavarría M, Sanchez-Pascuala A, Sauer U et al. Redox stress reshapes carbon fluxes of Pseudomonas putida for cytosolic glucose oxidation and NADPH generation. bioRxiv. 2020; 2020.06.13:149542
     [Google Scholar]
  30. Sánchez-Romero JM, Díaz-Orejas R, De Lorenzo V. Resistance to tellurite as a selection marker for genetic manipulations of Pseudomonas strains. Appl Environ Microbiol 1998; 64:4040–4046 [View Article][PubMed]
     [Google Scholar]
  31. Rajwade JM, Paknikar KM. Bioreduction of tellurite to elemental tellurium by Pseudomonas mendocina MCM B-180 and its practical application. Hydrometallurgy 2003; 71:243–248 [View Article]
     [Google Scholar]
  32. Aparicio T, de Lorenzo V, Martínez-García E. CRISPR/Cas9-Based counterselection boosts recombineering efficiency in Pseudomonas putida . Biotechnol J 2018; 13:1700161–10 [View Article][PubMed]
     [Google Scholar]
  33. Sambrook J, Russell D. Molecular Cloning: a laboratory manual. , 3rd ed. Cold Spring Harbor; 2001 p Isbn: 978-087969577-4
  34. Silva-Rocha R, Martínez-García E, Calles B, Chavarría M, Arce-Rodríguez A et al. The standard European vector architecture (SEVA): a coherent platform for the analysis and deployment of complex prokaryotic phenotypes. Nucleic Acids Res 2013; 41:D666–D675 [View Article][PubMed]
     [Google Scholar]
  35. Jackson RJ, Binet MRB, Lee LJ, Ma R, Graham AI et al. Expression of the PitA phosphate/metal transporter of Escherichia coli is responsive to zinc and inorganic phosphate levels. FEMS Microbiol Lett 2008; 289:219–224 [View Article][PubMed]
     [Google Scholar]
  36. Turner RJ, Weiner JH, Taylor DE. Tellurite-mediated thiol oxidation in Escherichia coli . Microbiology 1999; 145 (Pt 9:2549–2557 [View Article][PubMed]
     [Google Scholar]
  37. Turner RJ, Aharonowitz Y, Weiner JH, Taylor DE. Glutathione is a target in tellurite toxicity and is protected by tellurite resistance determinants in Escherichia coli . Can J Microbiol 2001; 47:33–40 [View Article][PubMed]
     [Google Scholar]
  38. Chavarría M, Nikel PI, Pérez-Pantoja D, de Lorenzo V. The Entner-Doudoroff pathway empowers Pseudomonas putida KT2440 with a high tolerance to oxidative stress. Environ Microbiol 2013; 15:1772–1785 [View Article][PubMed]
     [Google Scholar]
  39. Presentato A, Piacenza E, Anikovskiy M, Cappelletti M, Zannoni D et al. Rhodococcus aetherivorans BCP1 as cell factory for the production of intracellular tellurium nanorods under aerobic conditions. Microb Cell Fact 2016; 15:1–14 [View Article]
     [Google Scholar]
  40. Lohmeier-Vogel EM, Ung S, Turner RJ. In vivo 31P nuclear magnetic resonance investigation of tellurite toxicity in Escherichia coli . Appl Environ Microbiol 2004; 70:7342–7347 [View Article][PubMed]
     [Google Scholar]
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The putative phosphate transporter PitB (PP1373) is involved in tellurite uptake in Pseudomonas putida KT2440
Microbiology 167, 001002 (2021); https://doi.org/10.1099/mic.0.001002
/content/journal/micro/10.1099/mic.0.001002
/content/journal/micro/10.1099/mic.0.001002
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