Skip to main content

Advertisement

SpringerLink
Log in

Evaluation of mtr cluster expression in Shewanella RCRI7 during uranium removal

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

In recent years, bioremediation is considered as an efficient method to remove the pollutants from the industrial wastewater. In this study, quantitative gene expressions (Real-time RT-PCR) of mtr gene cluster (mtrA, mtrB, mtrC, mtrD, mtrE, mtrF and omcA) in five different uranium concentrations (0.1, 0.25, 0.5, 1 and 2 mM) were performed with ICP and microscopic live cell counting analysis under anaerobic condition, by Shewanella RCRI7 as a native bacterium. The results indicated that the amount of uranium removal and live-cell counting were decreased in the higher uranium concentrations (1 and 2 mM), due to the uranium toxicity, suggesting 0.5 mM as the optimum uranium concentration for Shewanella RCRI7 resistance. The expression of mtrCED and omcA genes presented increasing trend in the lower uranium concentrations (0.1, 0.25 and 0.5 mM) and a decreasing trend in 1 and 2 mM, while mtrABF, presented an inverse pattern, proving the alternative role of mtrF for mtrC and omcA, as the substantial multiheme cytochromes in Extracellular Electron Transfer (EET) pathway. These data are a proof of these gene vital roles in the EET pathway, proposing them for genetic engineering toward EET optimization, as the certain pathway in heavy metal bioremediation process.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Babij T, Madgwick JC (1993) High yield bacterial leaching of copper concentrate. In Proc Aust Inst Min Met, PP 61–64

  • Barchinger SE et al (2016) Regulation of gene expression during electron acceptor limitation and bacterial nanowire formation in Shewanella oneidensis MR-1. Appl Environ Microbiol AEM 1:01615–01616

    Google Scholar 

  • Beliaev AS, Saffarini DA (1998) Shewanella putrefaciens mtrB encodes an outer membrane protein required for Fe (III) and Mn (IV) reduction. J Bacteriol 180:6292–6297

    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

    CAS  PubMed  Google Scholar 

  • Bretschger O et al (2007) Current production and metal oxide reduction by Shewanella oneidensis MR-1 wild type and mutants. Appl Environ Microbiol 73:7003–7012

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brown SD et al (2006) Cellular response of Shewanella oneidensis to strontium stress. Appl Environ Microbiol 72:890–900

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bücking C, Popp F, Kerzenmacher S, Gescher J (2010) Involvement and specificity of Shewanella oneidensis outer membrane cytochromes in the reduction of soluble and solid-phase terminal electron acceptors. FEMS Microbiol Lett 306:144–151

    PubMed  Google Scholar 

  • Burgos WD et al (2008) Characterization of uraninite nanoparticles produced by Shewanella oneidensis MR-1. Geochim Cosmochim Acta 72:4901–4915

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Czerwinski KR, Polz MF (2008) Uranium enrichment using microorganisms. Google Patents, India

    Google Scholar 

  • Espinosa-Soto C, Wagner A (2010) Specialization can drive the evolution of modularity. PLoS Comput Biol 6:e1000719

    PubMed  PubMed Central  Google Scholar 

  • Gorby YA et al (2006) Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. Proc Natl Acad Sci 103:11358–11363

    CAS  PubMed  Google Scholar 

  • Haas JR, Northup A (2004) Effects of aqueous complexation on reductive precipitation of uranium by Shewanella putrefaciens. Geochem Trans 5:41

    CAS  PubMed Central  Google Scholar 

  • Harris HW, El-Naggar MY, Nealson KH (2012) Shewanella oneidensis MR-1 chemotaxis proteins and electron-transport chain components essential for congregation near insoluble electron acceptors. Portland Press Limited, Portland

    Google Scholar 

  • Haveman SA, Greene EA, Stilwell CP, Voordouw JK, Voordouw G (2004) Physiological and gene expression analysis of inhibition of Desulfovibrio vulgaris Hildenborough by nitrite. J Bacteriol 186:7944–7950

    CAS  PubMed  PubMed Central  Google Scholar 

  • He Q et al (2006) Energetic consequences of nitrite stress in Desulfovibrio vulgaris Hildenborough, inferred from global transcriptional analysis. Appl Environ Microbiol 72:4370–4381

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hungate R (1969) A roll tube method for cultivation of strict anaerobes. Methods in microbiology, Elsevier

    Google Scholar 

  • Hyun B (2003) Flow Cytometry Instrumentation. Curr Prot Cytomet 26:10

    Google Scholar 

  • Jiang X et al (2019) Kinetics of trifurcated electron flow in the decaheme bacterial proteins MtrC and MtrF. Proc Natl Acad Sci 116:3425–3430

    CAS  PubMed  Google Scholar 

  • Jin M et al (2013) Unique organizational and functional features of the cytochrome c maturation system in Shewanella oneidensis. PLoS ONE 8:e75610

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kasai T, Kouzuma A, Nojiri H, Watanabe K (2015) Transcriptional mechanisms for differential expression of outer membrane cytochrome genes omcA and mtrC in Shewanella oneidensis MR-1. BMC Microbiol 15:1

    CAS  Google Scholar 

  • Kouzuma A, Kasai T, Hirose A, Watanabe K (2015) Catabolic and regulatory systems in Shewanella oneidensis MR-1 involved in electricity generation in microbial fuel cells. Front Microbiol 6:609

    PubMed  PubMed Central  Google Scholar 

  • Li D-B et al (2014) Selenite reduction by Shewanella oneidensis MR-1 is mediated by fumarate reductase in periplasm. Sci Rep 4:7

    CAS  Google Scholar 

  • Lovley DR, Phillips EJ, Gorby YA, Landa ER (1991) Microbial reduction of uranium. Nature 350:413

    CAS  Google Scholar 

  • Mahadevan R, Palsson B, Lovley DR (2011) In situ to in silico and back: elucidating the physiology and ecology of Geobacter spp using genome-scale modelling. Nat Rev Microbiol 9:39

    CAS  PubMed  Google Scholar 

  • Marshall MJ et al (2006) c-Type cytochrome-dependent formation of U (IV) nanoparticles by Shewanella oneidensis. PLoS Biol 4:e268

    PubMed  PubMed Central  Google Scholar 

  • McLean JS et al (2008) Oxygen-dependent autoaggregation in Shewanella oneidensis MR-1. Environ Microbiol 10:1861–1876

    CAS  PubMed  Google Scholar 

  • Mullen LM (2007) Bacterial influence on uranium oxidation reduction reactions: implications for environmental remediation and isotopic composition. Massachusetts Institute of Technology, Massachusetts

    Google Scholar 

  • Myers C, Carstens B, Antholine W, Myers J (2000) Chromium (VI) reductase activity is associated with the cytoplasmic membrane of anaerobically grown Shewanella putrefaciens MR-1. J Appl Microbiol 88:98–106

    CAS  PubMed  Google Scholar 

  • O'neil RA et al (2008) Gene transcript analysis of assimilatory iron limitation in Geobacteraceae during groundwater bioremediation. Environ Microbiol 10:1218–1230

    CAS  PubMed  Google Scholar 

  • Orellana R et al (2013) U (VI) reduction by a diversity of outer surface c-type cytochromes of Geobacter sulfurreducens. AEM Appl Environ Microbiol 1:2551–2573

    Google Scholar 

  • Paquete CM et al (2014) Exploring the molecular mechanisms of electron shuttling across the microbe/metal space. Front Microbiol 5:318

    PubMed  PubMed Central  Google Scholar 

  • Pirbadian S et al (2014) Shewanella oneidensis MR-1 nanowires are outer membrane and periplasmic extensions of the extracellular electron transport components. Proc Natl Acad Sci 111:12883–12888

    CAS  PubMed  Google Scholar 

  • Rossi G (1990) Biohydrometallurgy. McGraw-Hill, New york

    Google Scholar 

  • Saffarini D, Brockman K, Beliaev A, Bouhenni R, Shirodkar S (2015) Shewanella oneidensis and extracellular electron transfer to metal oxides. Springer, London.

    Google Scholar 

  • Saffarini DA, Schultz R, Beliaev A (2003) Involvement of cyclic AMP (cAMP) and cAMP receptor protein in anaerobic respiration of Shewanella oneidensis. J Bacteriol 185:3668–3671

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schuetz B, Schicklberger M, Kuermann J, Spormann AM, Gescher J (2009) Periplasmic electron transfer via the c-type cytochromes MtrA and FccA of Shewanella oneidensis MR-1. Appl Environ Microbiol 75:7789–7796

    CAS  PubMed  PubMed Central  Google Scholar 

  • Seyrig G (2010) Uranium bioremediation: current knowledge and trends. Basic Biotechnol 6:19

    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 65:12–20

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tarhriz V et al (2014) Isolation and characterization of naphtalene-degradation bacteria from Qurugol lake located at Azerbaijan. Biosci Biotechnol Res Asia 11:715–722

    Google Scholar 

  • Tapia-Rodríguez A, Luna-Velasco A, Field JA, Sierra-Alvarez R (2012) Toxicity of uranium to microbial communities in anaerobic biofilms. Water Air Soil Pollut 223:3859–3868

    Google Scholar 

  • TerAvest MA (2014) Biological limitations of Shewanella oneidensis MR-1 in bioelectrochemical systems. Cornell University, Cornell

    Google Scholar 

  • Thorgersen MP et al (2017) A highly expressed high-molecular-weight S-layer complex of Pelosinus sp. strain UFO1 binds uranium. Appl Environ Microbiol 83:e03044–e3076

    PubMed  PubMed Central  Google Scholar 

  • Wall JD, Krumholz LR (2006) Uranium reduction. Annu Rev Microbiol 60:149–166

    CAS  PubMed  Google Scholar 

  • Wan X-F et al (2004) Transcriptomic and proteomic characterization of the Fur modulon in the metal-reducing bacterium Shewanella oneidensis. J Bacteriol 186:8385–8400

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yarzabal A, Appia-Ayme C, Ratouchniak J, Bonnefoy V (2004) Regulation of the expression of the Acidithiobacillus ferrooxidans rus operon encoding two cytochromes c, a cytochrome oxidase and rusticyanin. Microbiology 150:2113–2123

    CAS  PubMed  Google Scholar 

  • Yarzábal A, Duquesne K, Bonnefoy V (2003) Rusticyanin gene expression of Acidithiobacillus ferrooxidans ATCC 33020 in sulfur-and in ferrous iron media. Hydrometallurgy 71:107–114

    Google Scholar 

  • Zaheri Abdehvand A, Keshtkar A, Fatemi F, Tarhriz V, Hejazi MS (2017) Removal of U (VI) from aqueous solutions using Shewanella sp. RCRI7, isolated from Qurugöl Lake in Iran. Radiochim Acta 105:109–120

    CAS  Google Scholar 

Download references

Acknowledgements

The isolate was kindly provided by V. Tarhriz and M.S, Hejazi from Tabriz University of Medical Sciences, Tabriz, Iran.

Author information

Authors and Affiliations

  1. Department of Life Science Engineering, Faculty of New Sciences and Technologies, University of Tehran, Tehran, Iran

    Razieh Ghasemi, Mohammad Mir-Derikvand & Mahsa Zarei

  2. Materials and Nuclear Fuel Research School, Nuclear Science and Technology Research Institute, Tehran, Iran

    Faezeh Fatemi

Authors
  1. Razieh Ghasemi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Faezeh Fatemi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mohammad Mir-Derikvand
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mahsa Zarei
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Faezeh Fatemi or Mohammad Mir-Derikvand.

Additional information

Communicated by Erko Stackebrandt.

Publisher's Note

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

Appendix

Appendix

See Figs. 11 , 12 and Table 3 .

Fig. 11
figure 11

Growth curve of Shewanella RCRI7 under anaerobic condition, during 90 h; pH 6.4, temperature 30 °C, cell density 1 × 109 cells mL−1. 21 h were chosen as the appropriate time at the end of the logarithm phase, in anaerobic growth curve

Full size image
Fig. 12
figure 12

A summery of mtrA, mtrB, mtrC, mtrD, mtrE, mtrF and omcA quantitative expressions (Real-time RT-PCR), amount of uranium reduction, and microscopic live cell counting for different treatments in Shewanella RCRI7

Full size image
Table 3 Consequence of mtrABCDEF/omcA mutations on EET pathway in S.oneidensis MR-1
Full size table

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ghasemi, R., Fatemi, F., Mir-Derikvand, M. et al. Evaluation of mtr cluster expression in Shewanella RCRI7 during uranium removal. Arch Microbiol 202, 2711–2726 (2020). https://doi.org/10.1007/s00203-020-01981-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-020-01981-1

Keywords

Search

Navigation