Biosynthesis of bismuth nanoparticles and its synergistic effect with antibiotics against Escherichia coli and Klebsiella pneumoniae

Document Type : Original Research

Authors
A. Sadeghi Dousari 1
A. Talebi Bazmin Abadi 1
H. Forootanfar 2
M. Shakibaie 2
1 Department of Bacteriology, Faculty of Medical Sciences, Tarbiat Modares University, Tehran, Iran
2 Department of Pharmaceutical Biotechnology, Faculty of Pharmacy, Kerman University of Medical Sciences, Kerman, Iran
Abstract
Introduction: Today, the biosynthesis of nanoparticles (NPs) assisted by microorganisms (particularly bacteria) received increasing attention. In this study, Bacillus subtilis strain SFTS, a bismuth-reducing bacterium, was isolated from the soil of a copper mine in the South of Iran and used for biosynthesis of bismuth NPs (Bi NPs).

Materials and methods: Bacillus subtilis strain SFTS was identified by conventional identification tests and the 16S rDNA fragment amplification method. Characterizations of the bio-fabricated Bi NPs were examined using FTIR, EDS, XRD, TEM, and SEM analysis after purification of Bi NPs. In addition, the synergistic effect of biogenic Bi NPs in combination with different antibiotics was also investigated.

Results: The attained results revealed that the biosynthesized Bi NPs average size was 22.36 nm and spherical in shape. The XRD pattern showed that the biosynthesized nanoparticles consisted only of Bi4 and monoclinic crystals. Furthermore, the results of antibacterial effect of Bi NPs in combination with various antibiotics showed that the nanoparticles represented the highest synergistic effect together with imipenem and the lowest effect in combination with tetracycline against clinical strains of E. coli and K. pneumoniae. Significant difference between synergistic effect of Bi NPs with antibiotics compared to antibiotics disc alone against E. coli and K. pneumoniae strains was observed (P<0.001).

Conclusion: This study showed that Bi NPs biologically synthesized by Bacillus subtilis strain SFTS had a small size and different structure. However, finding about their antibacterial effect and related mechanism merit further investigations.

Keywords

Subjects

References
1. Bankier, C., Matharu, R., Cheong, Y., Ren, G., Cloutman-Green, E., Ciric, L. (2019). Synergistic antibacterial effects of metallic nanoparticle combinations. Scientific reports, 9, 1-8. https://doi.org/10.1038/s41598-019-52473-2
2. Lee, N.-Y., Ko, W.-C., Hsueh, P.-R. (2019). Nanoparticles in the treatment of infections caused by multidrug-resistant organisms. Frontiers in pharmacology, 1153. https://doi.org/10.3389/fphar.2019.01153
3. Qais, F. A., Shafiq, A., Khan, H. M., Husain, F. M., Khan, R. A., Alenazi, B., Alsalme, A., Ahmad, I. (2019). Antibacterial effect of silver nanoparticles synthesized using Murraya koenigii (L.) against multidrug-resistant pathogens. Bioinorganic chemistry and applications, 2019, https://doi.org/10.1155/2019/4649506
4. Thuesombat, P., Hannongbua, S., Akasit, S., Chadchawan, S. (2014). Effect of silver nanoparticles on rice (Oryza sativa L. cv. KDML 105) seed germination and seedling growth. Ecotoxicology and environmental safety, 104, 302-9. https://doi.org/10.1016/j.ecoenv.2014.03.022
5. Li, X., Xu, H., Chen, Z.-S., Chen, G. (2011). Biosynthesis of nanoparticles by microorganisms and their applications. Journal of Nanomaterials, 2011, https://doi.org/10.1155/2011/270974
6. Lahiri, D., Nag, M., Sheikh, H. I., Sarkar, T., Edinur, H. A., Pati, S., Ray, R. R. (2021). Microbiologically-synthesized nanoparticles and their role in silencing the biofilm signaling cascade. Frontiers in microbiology, 12, 636588. https://doi.org/10.3389/fmicb.2021.636588
7. Atalah, J., Espina, G., Blamey, L., Muñoz-Ibacache, S. A., Blamey, J. M. (2022). Advantages of Using Extremophilic Bacteria for the Biosynthesis of Metallic Nanoparticles and Its Potential for Rare Earth Element Recovery. Front Microbiol, 13, 855077. 10.3389/fmicb.2022.855077
8. Chokriwal, A., Sharma, M. M., Singh, A. (2014). Biological synthesis of nanoparticles using bacteria and their applications. American Journal of PharmTech Research, 4, 38-61.
9. Vazquez-Munoz, R., Arellano-Jimenez, M. J., Lopez-Ribot, J. L. (2020). Bismuth nanoparticles obtained by a facile synthesis method exhibit antimicrobial activity against Staphylococcus aureus and Candida albicans. BMC biomedical engineering, 2, 1-12. https://doi.org/10.1186/s42490-020-00044-2
10. Ferraz, K. S., Reis, D. C., Da Silva, J. G., Souza-Fagundes, E. M., Baran, E. J., Beraldo, H. (2013). Investigation on the bioactivities of clioquinol and its bismuth (III) and platinum (II, IV) complexes. Polyhedron, 63, 28-35. https://doi.org/10.1016/j.poly.2013.07.008
11. Folsom, J. P., Baker, B., Stewart, P. S. (2011). In vitro efficacy of bismuth thiols against biofilms formed by bacteria isolated from human chronic wounds. Journal of applied microbiology, 111, 989-96. https://doi.org/10.1111/j.1365-2672.2011.05110.x
12. Tarjoman, Z., Ganji, S. M., Mehrabian, S. (2015). Synergistic effects of the bismuth nanoparticles along with antibiotics on PKS positive Klebsiella pneumoniae isolates from colorectal cancer patients; comparison with quinolone antibiotics. M. Res J Med Med Sci, 3, 387-93.
13. Veloira, W. G., Domenico, P., LiPuma, J. J., Davis, J. M., Gurzenda, E., Kazzaz, J. A. (2003). In vitro activity and synergy of bismuth thiols and tobramycin against Burkholderia cepacia complex. Journal of Antimicrobial Chemotherapy, 52, 915-9. https://doi.org/10.1093/jac/dkg471
14. Vos, P., Garrity, G., Jones, D., Krieg, N. R., Ludwig, W., Rainey, F. A., Schleifer, K.-H., Whitman, W. B. (2011). Bergey's manual of systematic bacteriology: Volume 3: The Firmicutes. 3,
15. Faramarzi, M., Fazeli, M., Yazdi, M. T., Adrangi, S., Al-Ahmadi, K. J., Tasharrofi, N., Mohseni, F. A. (2009). Optimization of cultural conditions for production of chitinase by a soil isolate of Massilia timonae. Biotechnology, 8, 93-9. https://doi.org/10.3923/biotech.2009.93.99
16. Chatterjee, S., Bandyopadhyay, A., Sarkar, K. (2011). Effect of iron oxide and gold nanoparticles on bacterial growth leading towards biological application. Journal of Nanobiotechnology, 9, 34. https://doi.org/10.1186/1477-3155-9-34
17. Faisal, M., Ismail, A. A., Harraz, F. A., Bouzid, H., Al-Sayari, S. A., Al-Hajry, A. (2014). Highly selective colorimetric detection and preconcentration of Bi (III) ions by dithizone complexes anchored onto mesoporous TiO 2. Nanoscale research letters, 9, 1-7. https://doi.org/10.1186/1556-276X-9-62
18. Shakibaie, M., Hajighasemi, E., Adeli-Sardou, M., Doostmohammadi, M., Forootanfar, H. (2019). Antimicrobial and anti-biofilm activities of Bi subnitrate and BiNPs produced by Delftia sp. SFG against clinical isolates of Staphylococcus aureus, Pseudomonas aeruginosa, and Proteus mirabilis. IET nanobiotechnology, 13, 377-81. https://doi.org/10.1049/iet-nbt.2018.5102
19. Dalvand, L. F., Hosseini, F., Dehaghi, S. M., Torbati, E. S. (2018). Inhibitory effect of bismuth oxide nanoparticles produced by bacillus licheniformis on methicillin-resistant Staphylococcus aureus strains (MRSA). Iranian Journal of Biotechnology, 16, https://doi.org/10.21859/ijb.2102
20. Nazari, P., Faramarzi, M., Sepehrizadeh, Z., Mofid, M., Bazaz, R., Shahverdi, A. (2012). Biosynthesis of bismuth nanoparticles using Serratia marcescens isolated from the Caspian Sea and their characterisation. IET nanobiotechnology, 6, 58-62. https://doi.org/10.1049/iet-nbt.2010.0043
21. Prabhusaran, N. (2016). Exploration of herbal bismuth nanoparticles using Eclipta alba and in vitro antimicrobial activity against pathogenic bacterial strains. Int J Pharm Pharm Res,(Human), 6, 126-39.
22. Das, P. E., Majdalawieh, A. F., Abu-Yousef, I. A., Narasimhan, S., Poltronieri, P. (2020). Use of A hydroalcoholic extract of Moringa oleifera leaves for the green synthesis of bismuth nanoparticles and evaluation of their anti-microbial and antioxidant activities. Materials, 13, 876. https://doi.org/10.3390/ma13040876
23. Shakibaie, M., Amiri-Moghadam, P., Ghazanfari, M., Adeli-Sardou, M., Jafari, M., Forootanfar, H. (2018). Cytotoxic and antioxidant activity of the biogenic bismuth nanoparticles produced by Delftia sp. SFG. Materials Research Bulletin, 104, 155-63. https://doi.org/10.1016/j.materresbull.2018.04.001
24. Rather, G. A., Hassan, S., Pal, S., Khan, M. H., Rahman, H. S., Khan, J. (2021). Antimicrobial Efficacy of Biogenic Silver and Zinc Nanocrystals/Nanoparticles to Combat the Drug Resistance in Human Pathogens. Materials at the Nanoscale, 157.
25. Capeness, M. J., Echavarri-Bravo, V., Horsfall, L. E. (2019). Production of biogenic nanoparticles for the reduction of 4-Nitrophenol and oxidative laccase-like reactions. Frontiers in Microbiology, 10, 997. https://doi.org/10.3389/fmicb.2019.00997
26. Koul, B., Poonia, A. K., Yadav, D., Jin, J.-O. (2021). Microbe-mediated biosynthesis of nanoparticles: Applications and future prospects. Biomolecules, 11, 886. https://doi.org/10.3390/biom11060886
27. Adeli-Sardou, M., Torkzadeh-Mahani, M., Yaghoobi, M. M., Dodel, M. (2018). Antibacterial and anti-biofilm investigation of electrospun PCL/gelatin/lawsone nano fiber scaffolds against biofilm producing bacteria. Biomacromolecular Journal, 4, 46-57.
28. Kuroda, M., Suda, S., Sato, M., Ayano, H., Ohishi, Y., Nishikawa, H., Soda, S., Ike, M. (2019). Biosynthesis of bismuth selenide nanoparticles using chalcogen-metabolizing bacteria. Applied Microbiology and Biotechnology, 103, 8853-61. https://doi.org/10.1007/s00253-019-10160-2
29. Iftikhar, S., Iqtedar, M., Saeed, H., Aftab, M., Abdullah, R., Kaleem, A., Aslam, F. (2021). Comparative and combinatorial study of Biogenic Bismuth nanoparticles with Silver Nanoparticles and Doxycycline against Multidrug Resistant Staphylococcus aureus BTCB02 and Salmonella typhi BTCB06. Revista Mexicana de Ingeniería Química, 20, 271-80. https://doi.org/10.24275/rmiq/Bio1887
30. Motakef-Kazemi, N., Yaqoubi, M. (2020). Green synthesis and characterization of bismuth oxide nanoparticle using mentha pulegium extract. Iranian Journal of Pharmaceutical Research: IJPR, 19, 70.
31. Kamaraj, S. K., Venkatachalam, G., Arumugam, P., Berchmans, S. (2014). Bio-assisted synthesis and characterization of nanostructured bismuth (III) sulphide using Clostridium acetobutylicum. Materials Chemistry and Physics, 143, 1325-30. https://doi.org/10.1016/j.matchemphys.2013.11.042
32. Yue, L., Wu, Y., Liu, X., Xin, B., Chen, S. (2014). Controllable extracellular biosynthesis of bismuth sulfide nanostructure by sulfate‐reducing bacteria in water–oil two‐phase system. Biotechnology Progress, 30, 960-6. https://doi.org/10.1002/btpr.1894
33. Zhou, H., Che, L., Guo, Z., Wu, M., Li, W., Xu, W., Liu, L. (2018). Bacteria-mediated ultrathin Bi2Se3 nanosheets fabrication and their application in photothermal cancer therapy. ACS Sustainable Chemistry & Engineering, 6, 4863-70. https://doi.org/10.1021/acssuschemeng.7b04321
Pathobiology Reserach
Volume 25, Issue 1
January 2022
Pages 23-32