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Abstract

Biomineralization is a ubiquitous process in organisms to produce biominerals, and a wide range of metallic nanoscale minerals can be produced as a consequence of the interactions of micro-organisms with metals and minerals. Copper-bearing nanoparticles produced by biomineralization mechanisms have a variety of applications due to their remarkable catalytic efficiency, antibacterial properties and low production cost. In this study, we demonstrate the biotechnological potential of copper carbonate nanoparticles (CuNPs) synthesized using a carbonate-enriched biomass-free ureolytic fungal spent culture supernatant. The efficiency of the CuNPs in pollutant remediation was investigated using a dye (methyl red) and a toxic metal oxyanion, chromate Cr(VI). The biogenic CuNPs exhibited excellent catalytic properties in a Fenton-like reaction to degrade methyl red, and efficiently removed Cr(VI) from solution due to both adsorption and reduction of Cr(VI). X-ray photoelectron spectroscopy (XPS) identified the oxidation of reducing Cu species of the CuNPs during the reaction with Cr(VI). This work shows that urease-positive fungi can play an important role not only in the biorecovery of metals through the production of insoluble nanoscale carbonates, but also provides novel and simple strategies for the preparation of sustainable nanomineral products with catalytic properties applicable to the bioremediation of organic and metallic pollutants, solely and in mixtures.

Funding
This study was supported by the:
  • Natural Environment Research Council (Award NE/M010910/1)
    • Principle Award Recipient: GeoffreyMichael Gadd
  • Natural Environment Research Council (Award NE/M011275/1)
    • Principle Award Recipient: GeoffreyMichael Gadd
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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/content/journal/micro/10.1099/mic.0.001116
2021-12-09
2022-01-28
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References

  1. Schätz A, Reiser O, Stark WJ. Nanoparticles as semi-heterogeneous catalyst supports. Chemistry 2010; 16:8950–8967 [View Article] [PubMed]
    [Google Scholar]
  2. Zhang W, Elliott DW. Applications of iron nanoparticles for groundwater remediation. Remediation 2006; 16:7–21 [View Article]
    [Google Scholar]
  3. Reidy B, Haase A, Luch A, Dawson KA, Lynch I. Mechanisms of silver nanoparticle release, transformation and toxicity: a critical review of current knowledge and recommendations for future studies and applications. Materials (Basel) 2013; 6:2295–2350 [View Article] [PubMed]
    [Google Scholar]
  4. Tolaymat TM, El Badawy AM, Genaidy A, Scheckel KG, Luxton TP et al. An evidence-based environmental perspective of manufactured silver nanoparticle in syntheses and applications: a systematic review and critical appraisal of peer-reviewed scientific papers. Sci Total Environ 2010; 408:999–1006 [View Article] [PubMed]
    [Google Scholar]
  5. Salata OV. Applications of nanoparticles in biology and medicine. J Nanobiotechnol 2004; 2:3 [View Article]
    [Google Scholar]
  6. Wang AZ, Langer R, Farokhzad OC. Nanoparticle delivery of cancer drugs. Annu Rev Med 2012; 63:185–198 [View Article] [PubMed]
    [Google Scholar]
  7. Kowshik M, Ashtaputre S, Kharrazi S, Vogel W, Urban J et al. Extracellular synthesis of silver nanoparticles by a silver-tolerant yeast strain MKY3. Nanotechnology 2003; 14:95–100 [View Article]
    [Google Scholar]
  8. Kumar V, Yadav SK. Plant-mediated synthesis of silver and gold nanoparticles and their applications. J Chem Technol Biotechnol 2009; 84:151–157 [View Article]
    [Google Scholar]
  9. Mukherjee P, Ahmad A, Mandal D, Senapati S, Sainkar SR et al. Fungus-mediated synthesis of silver nanoparticles and their immobilization in the mycelial matrix: a novel biological approach to nanoparticle synthesis. Nano Lett 2001; 1:515–519 [View Article]
    [Google Scholar]
  10. Hulkoti NI, Taranath TC. Biosynthesis of nanoparticles using microbes—a review. Colloids and Surfaces B: Biointerfaces 2014; 121:474–483 [View Article]
    [Google Scholar]
  11. Mukherjee P, Ahmad A, Mandal D, Senapati S, Sainkar SR et al. Bioreduction of AuCl4 ions by the fungus, Verticillium sp. and surface trapping of the gold nanoparticles formed. Angewandte Chemie International Edition 2001; 40:3585–3588
    [Google Scholar]
  12. Li Q, Liu D, Chen C, Shao Z, Wang H et al. Experimental and geochemical simulation of nickel carbonate mineral precipitation by carbonate-laden ureolytic fungal culture supernatants. Environ Sci: Nano 2019; 6:1866–1875 [View Article]
    [Google Scholar]
  13. Narayanan KB, Sakthivel N. Biological synthesis of metal nanoparticles by microbes. Adv Colloid Interface Sci 2010; 156:1–13 [View Article] [PubMed]
    [Google Scholar]
  14. Durán N, Seabra AB. Metallic oxide nanoparticles: state of the art in biogenic syntheses and their mechanisms. Appl Microbiol Biotechnol 2012; 95:275–288 [View Article] [PubMed]
    [Google Scholar]
  15. Castro-Longoria E, Vilchis-Nestor AR, Avalos-Borja M. Biosynthesis of silver, gold and bimetallic nanoparticles using the filamentous fungus Neurospora crassa. Colloids Surf B 2011; 83:42–48 [View Article]
    [Google Scholar]
  16. Rubilar O, Rai M, Tortella G, Diez MC, Seabra AB et al. Biogenic nanoparticles: copper, copper oxides, copper sulphides, complex copper nanostructures and their applications. Biotechnol Lett 2013; 35:1365–1375 [View Article] [PubMed]
    [Google Scholar]
  17. Jia B, Mei Y, Cheng L, Zhou J, Zhang L. Preparation of copper nanoparticles coated cellulose films with antibacterial properties through one-step reduction. ACS Appl Mater Interfaces 2012; 4:2897–2902 [View Article] [PubMed]
    [Google Scholar]
  18. Li Q, Liu F, Li M, Chen C, Gadd GM. Nanoparticle and nanomineral production by fungi. Fungal Biol Rev 2021 [View Article] [PubMed]
    [Google Scholar]
  19. Li Q, Gadd GM. Biosynthesis of copper carbonate nanoparticles by ureolytic fungi. Appl Microbiol Biotechnol 2017; 101:7397–7407
    [Google Scholar]
  20. Li Q, Gadd GM. Fungal nanoscale metal carbonates and production of electrochemical materials. Microb Biotechnol 2017; 10:1131–1136 [View Article] [PubMed]
    [Google Scholar]
  21. Li Q, Liu D, Wang T, Chen C, Gadd GM. Iron coral: novel fungal biomineralization of nanoscale zerovalent iron composites for treatment of chlorinated pollutants. Chem Eng Sci 2020; 402:126263
    [Google Scholar]
  22. Saikia J, Saha B, Das G. Efficient removal of chromate and arsenate from individual and mixed system by malachite nanoparticles. J Hazard Mater 2011; 186:575–582 [View Article] [PubMed]
    [Google Scholar]
  23. Deka P, Borah BJ, Saikia H, Bharali P. Cu-based nanoparticles as emerging environmental catalysts. Chem Rec 2019; 19:462–473 [View Article] [PubMed]
    [Google Scholar]
  24. Wang S. A comparative study of Fenton and Fenton-like reaction kinetics in decolourisation of wastewater. Dyes and Pigments 2008; 76:714–720 [View Article]
    [Google Scholar]
  25. Pereira L, Alves M. Dyes—environmental impact and remediation. Environmental protection strategies for sustainable development. Springer; 2012 pp 111–162
  26. Hassaan MA, El Nemr A. Health and environmental impacts of dyes: mini review. Am J Environ Sci 2017; 1:64–67
    [Google Scholar]
  27. Chequer FD, de Oliveira GAR, Ferraz EA, Cardoso JC, Zanoni MB et al. Textile dyes: dyeing process and environmental impact. Eco-friendly textile dyeing and finishing 2013; 6:151–176
    [Google Scholar]
  28. Cheung KH, Gu J-D. Mechanism of hexavalent chromium detoxification by microorganisms and bioremediation application potential: a review. Int Biodeterior 2007; 59:8–15 [View Article]
    [Google Scholar]
  29. Hao OJ, Kim H, Chiang P-C. Decolorization of wastewater. Crit Rev Environ Sci Technol 2000; 30:449–505 [View Article]
    [Google Scholar]
  30. Li Q, Csetenyi L, Gadd GM. Biomineralization of metal carbonates by Neurospora crassa. Environ Sci Technol 2014; 48:14409–14416 [View Article] [PubMed]
    [Google Scholar]
  31. Liu F, Csetenyi L, Gadd GM. Amino acid secretion influences the size and composition of copper carbonate nanoparticles synthesized by ureolytic fungi. Appl Microbiol Biotechnol 2019; 103:7217–7230 [View Article]
    [Google Scholar]
  32. Liu F, Shah DS, Gadd GM. Role of protein in fungal biomineralization of copper carbonate nanoparticles. Current Biology 2021; 31:358–368 [View Article]
    [Google Scholar]
  33. Coreno-alonso A, Cruz-jimenez G, López-martinez L, Reyna-lópez GE, Acevedo-aguilar FJ. A rapid, eco-friendly, and reliable microplate method for determination of Cr(VI). Turk J Chem 2017; 41:420–425 [View Article]
    [Google Scholar]
  34. Perovic I, Davidyants A, Evans JS. Aragonite-associated mollusk shell protein aggregates to form mesoscale “smart” hydrogels. ACS Omega 2016; 1:886–893 [View Article] [PubMed]
    [Google Scholar]
  35. Pignatello JJ, Oliveros E, MacKay A. Advanced oxidation processes for organic contaminant destruction based on the Fenton reaction and related chemistry. Crit Rev Environ Sci Technol 2006; 36:1–84 [View Article]
    [Google Scholar]
  36. Lucas MS, Peres JA. Decolorization of the azo dye Reactive Black 5 by Fenton and photo-Fenton oxidation. Dyes and Pigments 2006; 71:236–244 [View Article]
    [Google Scholar]
  37. Benitez FJ, Beltran-Heredia J, Acero JL, Rubio FJ. Contribution of free radicals to chlorophenols decomposition by several advanced oxidation processes. Chemosphere 2000; 41:1271–1277 [View Article] [PubMed]
    [Google Scholar]
  38. Karatas M, Argun YA, Argun ME. Decolorization of antraquinonic dye, Reactive Blue 114 from synthetic wastewater by Fenton process: kinetics and thermodynamics. Journal of Industrial and Engineering Chemistry 2012; 18:1058–1062 [View Article]
    [Google Scholar]
  39. Sun Y, Tian P, Ding D, Yang Z, Wang W et al. Revealing the active species of Cu-based catalysts for heterogeneous Fenton reaction. Applied Catalysis B: Environmental 2019; 258:117985 [View Article]
    [Google Scholar]
  40. Cheng L, Wei M, Huang L, Pan F, Xia D et al. Efficient H2O2 oxidation of organic dyes catalyzed by simple copper(ii) ions in bicarbonate aqueous solution. Ind Eng Chem Res 2014; 53:3478–3485 [View Article]
    [Google Scholar]
  41. Jian-Hua Z, Qiong L, Yu-Miao C, Zhao-Qing L, Chang-Wei X et al. Determination of acid dissociation constant of methyl red by multi-peaks Gaussian fitting method based on UV-visible absorption spectrum. Acta Physico-Chimica Sinica 2012; 28:1030–1036 [View Article]
    [Google Scholar]
  42. Kwan WP, Voelker BM. Rates of hydroxyl radical generation and organic compound oxidation in mineral-catalyzed Fenton-like systems. Environ Sci Technol 2003; 37:1150–1158 [View Article] [PubMed]
    [Google Scholar]
  43. Sun B, Li H, Li X, Liu X, Zhang C et al. Degradation of organic dyes over fenton-like Cu2O–Cu/C catalysts. Ind Eng Chem Res 2018; 57:14011–14021 [View Article]
    [Google Scholar]
  44. Martorell MM, Fernández PM, Fariña JI, Figueroa LIC. Cr(VI) reduction by cell-free extracts of Pichia jadinii and Pichia anomala isolated from textile-dye factory effluents. Int Biodeterior 2012; 71:80–85 [View Article]
    [Google Scholar]
  45. Ramírez-Ramírez R, Calvo-Méndez C, Avila-Rodríguez M, Lappe P, Ulloa M et al. Cr(VI) reduction in a chromate-resistant strain of Candida maltosa isolated from the leather industry. Antonie van Leeuwenhoek 2004; 85:63–68 [View Article] [PubMed]
    [Google Scholar]
  46. Ge J, Lei J, Zare RN. Protein-inorganic hybrid nanoflowers. Nat nanotechnol 2012; 7:428–432 [View Article] [PubMed]
    [Google Scholar]
  47. Maiti BK, Maia LB, Moro AJ, Lima JC, Cordas CM et al. Unusual reduction mechanism of copper in cysteine-rich environment. Inorg Chem 2018; 57:8078–8088 [View Article] [PubMed]
    [Google Scholar]
  48. Saikia H, Borah BJ, Yamada Y, Bharali P. Enhanced catalytic activity of CuPd alloy nanoparticles towards reduction of nitroaromatics and hexavalent chromium. J Colloid Interface Sci 2017; 486:46–57 [View Article] [PubMed]
    [Google Scholar]
  49. Zhu F, Ma S, Liu T, Deng X. Green synthesis of nano zero-valent iron/Cu by green tea to remove hexavalent chromium from groundwater. J Clean Prod 2018; 174:184–190 [View Article]
    [Google Scholar]
  50. Sun J, Huang J. C. Co-removal of hexavalent chromium during copper precipitation. Water Sci Technol 2002; 46:413–419 [PubMed]
    [Google Scholar]
  51. Sun J. M, Zhao X. H, Huang J. C. Characterization of adsorbent composition in co-removal of hexavalent chromium with copper precipitation. Chemosphere 2005; 58:1003–1010 [View Article] [PubMed]
    [Google Scholar]
  52. Guo Y, Zhang J, Yang L, Wang H, Wang F et al. Syntheses of amorphous and crystalline cupric sulfide nanoparticles and study on the specific activities on different cells. Chem Commun 2010; 46:3493 [View Article]
    [Google Scholar]
  53. Laha D, Bhattacharya D, Pramanik A, Santra CR, Pramanik P et al. Evaluation of copper iodide and copper phosphate nanoparticles for their potential cytotoxic effect. Toxicol Res 2012; 1:131 [View Article]
    [Google Scholar]
  54. Siddiqui MA, Alhadlaq HA, Ahmad J, Al-Khedhairy AA, Musarrat J et al. Copper oxide nanoparticles induced mitochondria mediated apoptosis in human hepatocarcinoma cells. PLoS ONE 2013; 8:e69534 [View Article] [PubMed]
    [Google Scholar]
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