Skip to main content
Log in

Enzyme(s) responsible for tellurite reducing activity in a moderately halophilic bacterium, Salinicoccus iranensis strain QW6

  • Original Paper
  • Published:
Extremophiles Aims and scope Submit manuscript

Abstract

Oxyanions of tellurium, like tellurate (TeO4 2−) and tellurite (TeO3 2−), are highly toxic for most microorganisms. There are a few reports on the bacterial tellurite resistance mechanism(s). Salinicoccus iranensis, a Gram-positive halophilic bacterium, shows high tellurite resistance and NADH-dependent tellurite reduction activity in vitro. Since little is known regarding TeO3 2− resistance mechanisms in halophilic microorganisms, here one of the enzymatic reduction activities presented in this microorganism is investigated. To enhance the enzymatic activity during purification, the effect of different parameters including time, inoculation, different pHs, different tellurite concentrations and different salts were optimized. We also examined the tellurite removal rates by diethyldithiocarbamate (DDTC) during optimization. In the culture medium the optimum conditions obtained showed that at 30 h, 2 % inoculum, pH 7.5, without tellurite and with 5 % NaCl (w/v) the highest enzyme activity and tellurite removal were observed. Results of the purification procedure done by hydroxyapatite batch-mode, ammonium sulfate precipitation, followed by phenyl-Sepharose and Sephadex G-100 column chromatography, showed that the enzyme consisted of three subunits with molecular masses of 135, 63 and 57 kDa. In addition to tellurite reduction activity, the enzyme was able to reduce nitrate too. Our study extends the knowledge regarding this process in halophilic microorganisms. Besides, this approach may suggest an application for the organism or the enzyme itself to be used for bioremediation of polluted areas with different contaminants due to its nitrate reductase activity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Amoozegar MA, Hamedi J, Dadashipour M, Shariatpanahi S (2005) Effect of salinity on the tolerance to toxic metals and oxyanions in native moderately halophilic spore-forming bacilli. World J Microbiol Biotechnol 21:1237–1243

    Article  CAS  Google Scholar 

  • Amoozegar MA, Schumann P, Hajighasemi M, Ashengroph M, Razavi MR (2008a) Salinicoccus iranensis sp. nov., a novel moderate halophile. Int J Syst Evol Microbiol 58:178–183

    Article  PubMed  CAS  Google Scholar 

  • Amoozegar MA, Ashengroph M, Malekzadeh F, Reza Razavi M, Naddaf S, Kabiri M (2008b) Isolation and initial characterization of the tellurite reducing moderately halophilic bacterium, Salinicoccus sp. strain QW6. Microbiol Res 163:456–465

    Article  PubMed  CAS  Google Scholar 

  • Amoozegar MA, Khoshnoodi M, Didari M, Hamedi J, Ventosa A, Baldwin SA (2012) Tellurite removal by a tellurium-tolerant halophilic bacterial strain, Thermoactinomyces sp. QS-2006. Ann Microbiol 62:1031–1037

    Article  CAS  Google Scholar 

  • Avazeri 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  CAS  Google Scholar 

  • Baesman SM, Bullen TD, Dewald J, Zhang D, Curran S, Islam FS, Beveridge TJ, Oremland RS (2007) Formation of tellurium nanocrystals during anaerobic growth of bacteria that use Te oxyanions as respiratory electron acceptors. Appl Environ Microbiol 73:2135–2143

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Baesman SM, Stolz JF, Kulp TR, Oremland RS (2009) Enrichment and isolation of Bacillus beveridgei sp. nov., a facultative anaerobic haloalkaliphile from Mono Lake, California, that respires oxyanions of tellurium, selenium, and arsenic. Extremophiles 13:695–705

    Article  PubMed  CAS  Google Scholar 

  • Barbier GG, Campbell WH (2005) Viscosity effects on eukaryotic nitrate reductase activity. J Biol Chem 280:26049–26054

    Article  PubMed  CAS  Google Scholar 

  • Borghese R, Borsetti F, Foladori P, Ziglio G, Zannoni D (2004) Effects of the metalloid oxyanion tellurite (TeO3 2−) on growth characteristics of the phototrophic bacterium Rhodobacter capsulatus. Appl Environ Microbiol 70:6595–6602

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  PubMed Central  Google Scholar 

  • Etezad SM, Khajeh K, Soudi M, Ghazvini PTM, Dabirmanesh B (2009) Evidence on the presence of two distinct enzymes responsible for the reduction of selenate and tellurite in Bacillus sp. STG-83. Enzyme Microb Tech 45:1–6

    Article  CAS  Google Scholar 

  • Filimonenkov AA, Zvyagilskaya RA, Tikhonova TV, Popov VO (2010) Isolation and characterization of nitrate reductase from the halophilic sulfur-oxidizing bacterium Thioalkalivibrio nitratireducens. Biochemistry (Mosc) 75:744–751

    Article  CAS  Google Scholar 

  • Fthenakis VM, Kim HC, Alsema E (2008) Emissions from photovoltaic life cycles. Environ SciTechnol 42:2168–2174

    Article  CAS  Google Scholar 

  • Kabiri M, Amoozegar MA, Tabebordbar M, Gilany K, Salekdeh GH (2009) Effects of selenite and tellurite on growth, physiology, and proteome of a moderately halophilic bacterium. J Proteome Res 8:3098–3108

    Article  PubMed  CAS  Google Scholar 

  • Kinkle BK, Sadowsky MJ, Johnstone K, Koskinen WC (1994) Tellurium and selenium resistance in Rhizobia and its potential use for direct isolation of Rhizobium meliloti from soil. Appl Environ Microbiol 60:1674–1677

    PubMed  CAS  PubMed Central  Google Scholar 

  • Klonowska A, Heulin T, vermeglio A (2005) Selenite and tellurite reduction by Shewanella oneidensis. Appl Environ Microbiol 71:5607–5609

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  • Lefebvre O, Moletta R (2006) Treatment of organic pollution in industrial saline wastewater: a literature review. Water Res 40:3671–3682

    Article  PubMed  CAS  Google Scholar 

  • Lund K, DeMossJ A (1976) Association–dissociation behavior and subunit structure of heat-released nitrate reductase from Escherichia coli. J Biol Chem 251:2207–2216

    PubMed  CAS  Google Scholar 

  • Moreno-Vivián C, Cabello P, Manuel Marti´nez-Luque M, Blasco R, Castillo F (1999) Prokaryotic nitrate reduction: molecular properties and functional distinction among bacterial nitrate reductases. J Bacteriol 181:6573–6584

    PubMed  PubMed Central  Google Scholar 

  • Moscoso H, Saavedra C, Loyola C, Pichuantes S, Vasquez C (1998) Biochemical characterization of tellurite-reducing activities of Bacillus stearothermopilus V. Res microbial 149:389–397

    Article  CAS  Google Scholar 

  • Pérez JM, Caldeŕon IL, Arenas FA, Fuentes DE, Pradenas GA, Fuentes EL, Sandoval JM, Castro ME, Eĺıas AO, V´asquez CC (2007) Bacterial toxicity of potassium tellurite: unveiling an ancient enigma. PLoS One 2:e211

    Article  PubMed  PubMed Central  Google Scholar 

  • Sabaty M, Avazeri C, Pignol D, Vermeglio A (2001) Characterization of the reduction of selenate and tellurite by nitrate reductase. Appl Environ Microbiol 67:5122–5126

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Terai T, Kamahora T, Yamamura Y (1958) Tellurite reductase from Mycobacterium avium. J Bacteriol 75:535–539

    PubMed  CAS  PubMed Central  Google Scholar 

  • Theisen J, Zylstra GJ, Yee N (2013) Genetic evidence for a molybdopterin-containing tellurate reductase. Appl Environ Microbiol 79:3171–3175

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Tremaroli V, Fedi S, Zannoni D (2007) Evidence for a tellurite-dependent generation of reactive oxygen species and absence of a tellurite-mediated adaptive response to oxidative stress in cells of Pseudomonas pseudoalcaligenes KF707. Arch Microbiol 187:127–135

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Turner RJ, Pommie J, Weiner JH, Giordano G, Vermeglio 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 

  • Wilson CM (1983) Staining of proteins on gels: comparison of dyes and procedures. Methods Enzymol 91:236–247

    Article  PubMed  CAS  Google Scholar 

  • Yurkov VV, Thomas BJ (1998) Aerobic anoxygenic phototrophic bacteria. Microbiol MolBiol Rev 62:695–724

    CAS  Google Scholar 

  • Zannoni D, Borsetti F, Harrison JJ, Turner RJ (2007) The bacterial response to the chalcogen metalloids Se and Te. Adv Microb Physiol 53:1–71

    Article  Google Scholar 

  • Zhuang X, Han Z, Bai Z, Zhuang G, Shim H (2010) Progress in decontamination by halophilic microorganisms in saline wastewater and soil. Environ Pollut 158:1119–1126

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to express their gratitude to the research council of University of Tehran and Tarbiat Modares University.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Mohammad Ali Amoozegar or Khosro Khajeh.

Additional information

Communicated by A. Oren.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Alavi, S., Amoozegar, M.A. & Khajeh, K. Enzyme(s) responsible for tellurite reducing activity in a moderately halophilic bacterium, Salinicoccus iranensis strain QW6. Extremophiles 18, 953–961 (2014). https://doi.org/10.1007/s00792-014-0665-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00792-014-0665-6

Keywords

Navigation