Skip to main content

Advertisement

Log in

Reduction of selenite and tellurite by a highly metal-tolerant marine bacterium

  • Research
  • Published:
International Microbiology Aims and scope Submit manuscript

Abstract

Selenium (Se) and tellurium (Te) contaminations in soils and water bodies have been widely reported in recent years. Se(IV) and Te(IV) were regarded as their most dangerous forms. Microbial treatments of Se(IV)- and Te(IV)-containing wastes are promising approaches because of their environmentally friendly and sustainable advantages. However, the salt-tolerant microbial resources that can be used for selenium/tellurium pollution control are still limited since industrial wastewaters usually contain a large number of salts. In this study, a marine Shewanella sp. FDA-1 (FDA-1) was reported for efficient Se(IV) and Te(IV) reduction under saline conditions. Process and product analyses were performed to investigate the bioreduction processes of Se(IV) and Te(IV). The results showed that FDA-1 can effectively reduce Se(IV) and Te(IV) to Se0 and Te0 Se(IV)/Te(IV) to Se0/Te0 in 72 h, which were further confirmed by XRD and XPS analyses. In addition, enzymatic and RT‒qPCR assays showed that flavin-related proteins, reductases, dehydrogenases, etc., could be involved in the bioreduction of Se(IV)/Te(IV). Overall, our results demonstrate the ability of FDA-1 to reduce high concentrations of Se(IV)/or Te(IV) to Se0/or Te0 under saline conditions and thus provide efficient microbial candidate for controlling Se and Te pollution.

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
Fig. 6

Similar content being viewed by others

Data availability

All data generated or analysed during this study are included in this published article and its supplementary information files. The genome data used in this study has been deposited in Short Read Archive under project number PRJNA967134.

References

  • Abatenh E, Gizaw B, Tsegaye Z, Wassie M (2017) The role of microorganisms in bioremediation-A review. Open J Environ Biol 2:038–046

    Article  Google Scholar 

  • Arenas FA, Díaz WA, Leal CA, Pérez-Donoso JM, Imlay JA, Vásquez CC (2010) The Escherichia coli btuE gene, encodes a glutathione peroxidase that is induced under oxidative stress conditions. Biochem Biophys Res Commun 398:690–694

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arindam S, Manoj K, Rayanee C, Sudeshna S, Kannan P (2022) Simultaneous removal of selenite and heavy metals from wastewater and their recovery as nanoparticles using an inverse fluidized bed bioreactor. J Clean Prod 376:134248

    Article  Google Scholar 

  • Beleneva IA, Efimova KV, Eliseikina MG, Svetashev VI, Orlova TY (2019) The tellurite-reducing bacterium Alteromonas macleodii from a culture of the toxic dinoflagellate Prorocentrum foraminosum. Heliyon 5:e02435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beliaev AS, Saffarini DA, McLaughlin JL, Hunnicutt D (2001) MtrC, an outer membrane decahaem c cytochrome required for metal reduction in Shewanella putrefaciens MR-1. Mol Microbiol 39:722–730

    Article  CAS  PubMed  Google Scholar 

  • Bretschger O, Obraztsova A, Sturm CA, Chang IS, Gorby YA, Reed SB, Culley DE, Reardon CL, Barua S, Romine MF, Zhou J, Beliaev AS, Bouhenni R, Saffarini D, Mansfeld F, Kim B-H, Fredrickson JK, Nealson KH (2008) Current production and metal oxide reduction by shewanella oneidensis mr-1 wild type and mutants. Appl Environ Microbiol 73:7003–7012

    Article  Google Scholar 

  • Brutinel ED, Gralnick JA (2012) Shuttling happens: soluble flavin mediators of extracellular electron transfer in Shewanella Appl Microbiol Biotechnol 93:41–48

    Article  PubMed  Google Scholar 

  • Chasteen TG, Fuentes DE, Tantaleán JC, Vásquez CC (2009) Tellurite: history, oxidative stress, and molecular mechanisms of resistance. FEMS Microbiol Rev 33:820–832

    Article  CAS  PubMed  Google Scholar 

  • Cheng M, Sun Y, Sui X, Zhang H (2022) Characterization of the differentiated reduction of selenite and tellurite by a halotolerant bacterium: Process and mechanism. J Water Proc Eng 47:102809

    Article  Google Scholar 

  • Coursolle D, Gralnick JA (2010) Modularity of the Mtr respiratory pathway of Shewanella oneidensis strain MR-1. Mol Microbiol 77:995–1008

    Article  CAS  PubMed  Google Scholar 

  • Dikow RB (2011) Genome-level homology and phylogeny of Shewanella (Gammaproteobacteria: lteromonadales: Shewanellaceae). BMC Genomics 12(1):1–14

    Article  Google Scholar 

  • Huang ShengWei, Wang Y, Tang C, Jia HuiLing, Lifang Wu (2020) Speeding up selenite bioremediation using the highly selenite-tolerant strain Providencia rettgeri HF16-A novel mechanism of selenite reduction based on proteomic analysis. J Hazard Mater 406:124690

    Article  PubMed  Google Scholar 

  • Ismail NA, Kasmuri N, Hamzah N, Jaafar J, Mojiri A, Kindaichi T (2023) Influence of pH and concentration on the growth of bacteria - fungus and benzo[a]pyrene degradation. Environ Technol Innov 29:102995

    Article  CAS  Google Scholar 

  • Kadir MFZ, Aspanut Z, Majid SR, Arof AK (2010) FTIR studies of plasticized poly(vinyl alcohol)–chitosan blend doped with NH4NO3 polymer electrolyte membrane. Spectrochim Acta Part A Mol Biomol Spectrosc 78(3):1068–1074

    Article  Google Scholar 

  • Kami M, Filzah NA, Tao W, Hamzah N (2020) Establishing the order of importance factor based on optimization of conditions in pahs biodegradation. Polycyclic Aromat Compd 42(5):2348–2362

    Article  Google Scholar 

  • Khoei NS, Lampis S, Zonaro E, Yrjälä K, Bernardi P, Vallini G (2017) Insights into selenite reduction and biogenesis of elemental selenium nanoparticles by two environmental isolates of Burkholderia fungorum New Biotechnol 34:1–11

    Article  CAS  Google Scholar 

  • Kim R-R, Illarionov B, Joshi M, Cushman M, Lee CY, Eisenreich W, Fischer M, Bacher A (2010) Mechanistic insights on riboflavin synthase inspired by selective binding of the 6,7-dimethyl-8-ribityllumazine exomethylene anion. J Am Chem Soc 132(9):2983–2990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim D-H, Kim M-G, Jiang S, Lee J-H, Hur H-G (2013) Promoted reduction of tellurite and formation of extracellular tellurium nanorods by concerted reaction between iron and Shewanella oneidensis MR-1. Environ Sci Technol 47(15):8709–8715

    CAS  Google Scholar 

  • Klonowska A, Heulin T, Vermeglio A (2005) Selenite and tellurite reduction by Shewanella oneidensis Appl Environ Microbiol 71(9):5607–5609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kreienbaum M, Dörrich AK, Brandt D, Schmid NE, Leonhard T, Hager F, Brenzinger S, Hahn J, Glatter T, Ruwe M, Briegel A, Kalinowski J, Thormann KM (2020) Isolation and characterization of Shewanella phage thanatos infecting and lysing Shewanella oneidensis and promoting nascent biofilm formation. Front Microbiol 11

    Article  PubMed  PubMed Central  Google Scholar 

  • Lampis S, Zonaro E, Bertolini C, Cecconi D, Monti F, Micaroni M, Turner RJ, Butler CS, Vallini G (2016) Selenite biotransformation and detoxification by Stenotrophomonas maltophilia SeITE02: Novel clues on the route to bacterial biogenesis of selenium nanoparticles. J Hazard Mater 324:3–14

    Article  PubMed  Google Scholar 

  • Lee J-H, Han J, Choi H, Hur H-G (2007) Effects of temperature and dissolved oxygen on Se(IV) removal and Se(0) precipitation by Shewanella sp. HN-41. Chemosphere 68:1898–1905

    Article  CAS  PubMed  Google Scholar 

  • Lemly AD (2014) 'Teratogenic effects and monetary cost of selenium poisoning of fish in Lake Sutton. North Carolina', Ecotoxicol Environ Safety 104:160–167

    Article  CAS  PubMed  Google Scholar 

  • Lies DP, Hernandez ME, Kappler A, Mielke RE, Gralnick JA, Newman DK (2005) Shewanella oneidensis MR-1 uses overlapping pathways for iron reduction at a distance and by direct contact under conditions relevant for Biofilms. Appl Environ Microbiol 71(8):4414–4426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lizárraga WC, Mormontoy CG, Calla H, Castañeda M, Taira M, Garcia R, Marín C, Abanto M, Ramirez P (2022) Complete genome sequence of Shewanella algae strain 2NE11, a decolorizing bacterium isolated from industrial effluent in Peru. Biotechnol Rep 33:e00704

    Article  PubMed  PubMed Central  Google Scholar 

  • Long Q, Cui L-K, He S-B, Sun J, Chen Q-Z, Bao H-D, Liang T-Y, Liang B-Y, Cui L-y (2023) Preparation, characteristics and cytotoxicity of green synthesized selenium nanoparticles using Paenibacillus motobuensis LY5201 isolated from the local specialty food of longevity area. Sci Rep 13:53

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Mal J, Nancharaiah YV, Maheshwari N, van Hullebusch ED, Lens PNL (2017) Continuous removal and recovery of tellurium in an upflow anaerobic granular sludge bed reactor. J Hazard Mater 327:79–88

    Article  CAS  PubMed  Google Scholar 

  • Maltman C, Yurkov V (2018) Bioremediation potential of bacteria able to reduce high levels of selenium and tellurium oxyanions. Arch Microbiol 200:1411–1417

    Article  CAS  PubMed  Google Scholar 

  • Marsili E, Baron DB, Shikhare ID, Coursolle D, Gralnick JA, Bond DR (2008) Shewanella secretes flavins that mediate extracellular electron transfer. Proc Natl Acad Sci USA 105(10):3968–3973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moharram MA, Mahmoud OM (2007) FTIR spectroscopic study of the effect of microwave heating on the transformation of cellulose I into cellulose II during mercerization. J Appl Polym Sci 107(1):30–36

    Article  Google Scholar 

  • Nancharaiah YV, Lens PNL (2015) Selenium biomineralization for biotechnological applications. Trends Biotechnol 42(5):2348–2362

    Google Scholar 

  • Negi BB, Sinharoy A, Pakshirajan K (2019) Selenite removal from wastewater using fungal pelleted airlift bioreactor. Environ Sci Pollut Res 27:992–1003

    Article  Google Scholar 

  • Qin H-b, Zhu J-M, Liang L, Wang M-S, Hui Su (2013) 'The bioavailability of selenium and risk assessment for human selenium poisoning in high-Se areas. China', Environ Int 52:66–74

    Article  CAS  PubMed  Google Scholar 

  • Reddy G. Kiran, Kumar Pathak Snigdha, Nancharaiah YV (2023) Aerobic reduction of selenite and tellurite to elemental selenium and tellurium nanostructures by Alteromonas sp under saline conditions. Int Biodeter Biodeg 179:105571

    Article  Google Scholar 

  • Schwarz K, Foltzs CM (2009) Selenium as an integral part of factor 3 against dietary necrotic liver degeneration. Nutr Rev 79(12):3292–3293

    Google Scholar 

  • Sheng G-P, Han-Qing Yu, Wang C-M (2006) FTIR-spectral analysis of two photosynthetic hydrogen-producing [corrected] strains and their extracellular polymeric substances. Appl Microbiol Biotechnol 73(1):241

    Article  CAS  Google Scholar 

  • Shi L, Squier TC, Zachara JM, Fredrickson JK (2007) Respiration of metal (hydr)oxides by Shewanella and Geobacter: a key role for multihaem c-type cytochromes. Mol Microbiol 65(1):12–20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sinharoy A, Lens PNL (2020) Biological removal of selenate and selenite from wastewater: options for selenium recovery as nanoparticles. Curr Pollut Rep 6:230–249

    Article  CAS  Google Scholar 

  • Soda S, Kashiwa M, Kagami T, Kuroda M, Yamashita M, Ike M (2011) Laboratory-scale bioreactors for soluble selenium removal from selenium refinery wastewater using anaerobic sludge. Desalination 279(1–3):433–438

    Article  CAS  Google Scholar 

  • Soda S, Hasegawa A, Kuroda M, Hanada A, Yamashita M, Ike M (2015) Selenium recovery from kiln powder of cement manufacturing by chemical leaching and bioreduction. Water Sci Technol 72(8):1294–1300

    Article  CAS  PubMed  Google Scholar 

  • Soda S, Ma W, Kuroda M, Nishikawa H, Zhang Y, Ike M (2017) Characterization of moderately halotolerant selenate- and tellurite-reducing bacteria isolated from brackish areas in Osaka. Biosci Biotechnol Biochem 82(1):173–181

    Article  PubMed  Google Scholar 

  • Song J-M, Zhu J-H, Shu-Hong Yu (2006) Crystallization and shape evolution of single crystalline selenium nanorods at liquid-liquid interface: from monodisperse amorphous Se nanospheres toward Se nanorods. J Phys Chem B 110(47):23790–23795

    Article  CAS  PubMed  Google Scholar 

  • Staicu LC, Wójtowicz PJ, Molnár Z, Ruiz-Agudo E, José LR, Gallego DB, Pósfai Mihály (2022) Interplay between arsenic and selenium biomineralization in Shewanella sp O23S. Environ Pollut 306:119451

    Article  CAS  PubMed  Google Scholar 

  • Tyson GW, Chapman J, Hugenholtz P, Allen EE, Ram RJ, Richardson PM, Solovyev VV, Rubin EM, Rokhsar DS, Banfield JF (2004) Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428:37–43

    Article  CAS  PubMed  Google Scholar 

  • Valdivia-González MA, Díaz-Vásquez WA, Ruiz-León D, Becerra AA, Aguayo DR, Pérez-Donoso JM, Vásquez CC (2017) A comparative analysis of tellurite detoxification by members of the genus Shewanella Arch Microbiol 200:267–273

    Article  PubMed  Google Scholar 

  • Wang Yi, You L-X, Zhong H-L, Gao-Kai Wu, Li Y-P, Yang X-J, Wang A-J, Nealson KH, Herzberg M, Rensing C (2022) Au(III)-induced extracellular electron transfer by Burkholderia contaminans ZCC for the bio-recovery of gold nanoparticles. Environ Res 210

    Article  CAS  PubMed  Google Scholar 

  • Yu P, Zhou Li, Jia Z, Keyue Wu, Cui J (2020) Morphology and property tuning of Te nanostructures in a hydrothermal growth. J Mater Sci: Mater Electron 31:16332–16337

    CAS  Google Scholar 

  • Yu L, Jian H, Gai Y, Yi Z, Ying Feng Xu, Qiu ZS, Tang Xi (2021) Characterization of two novel psychrophilic and piezotolerant strains, Shewanella psychropiezotolerans sp. nov. and Shewanella eurypsychrophilus sp nov, adapted to an extreme deep-sea environment. Systematic App Microbiol 44:126266

    Article  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 53:1–312

    Article  Google Scholar 

  • Zhang W, Chen Z, Liu H, Zhang L, Gao P, Li D (2011) Biosynthesis and structural characteristics of selenium nanoparticles by Pseudomonas alcaliphila Colloids Surf, B 88(1):196–201

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by the National Key Research and Development Program of China (2020YFD0901003), National Natural Science Foundation of China (42077305), Youth Innovation Promotion Association CAS (2022212), and CSC Scholarship (202104910148).

Author information

Authors and Affiliations

Authors

Contributions

HZ conceived the study. HZ and MC designed the experiments. MC, LL and YS performed the experiments. HZ and MC wrote the manuscript. XH provided funding support. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Haikun Zhang or Xiaoke Hu.

Ethics declarations

Competing Interest

The authors declare no conflict of interest.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 237 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cheng, M., Liang, L., Sun, Y. et al. Reduction of selenite and tellurite by a highly metal-tolerant marine bacterium. Int Microbiol 27, 203–212 (2024). https://doi.org/10.1007/s10123-023-00382-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10123-023-00382-w

Keywords

Navigation