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Vol. 36 No. 3 (2024): Vol 36 Issue 3, 2024

Copyright (c) 2024 Jamunasri N., Aswetha Iyer, Murugan Sevanan, Lakshmi Prabha M., Reya Issac

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This work is licensed under a Creative Commons Attribution 4.0 International License.

Metalloproteomics: Unraveling the Metal Binding Proteins of Diverse Metal-Resistant Bacteria

https://doi.org/10.14233/ajchem.2024.31102
N. Jamunasri
Division of Biotechnology, Karunya Institute of Technology and Sciences, Coimbatore-641114, India
https://orcid.org/0009-0008-3320-6044
Aswetha Iyer
Division of Biotechnology, Karunya Institute of Technology and Sciences, Coimbatore-641114, India
https://orcid.org/0009-0004-5557-5378
M. Lakshmi Prabha
Division of Biotechnology, Karunya Institute of Technology and Sciences, Coimbatore-641114, India
https://orcid.org/0000-0002-6253-5444
Reya Issac
Division of Biotechnology, Karunya Institute of Technology and Sciences, Coimbatore-641114, India
https://orcid.org/0000-0001-9996-0957
S. Murugan
Division of Biotechnology, Karunya Institute of Technology and Sciences, Coimbatore-641114, India
https://orcid.org/0000-0002-2432-1883

Corresponding Author(s) : Reya Issac

reya@karunya.edu

Asian Journal of Chemistry, Vol. 36 No. 3 (2024): Vol 36 Issue 3, 2024

Abstract

The release of metals into the environment raises serious concerns about their harmful effects on both the wildlife and human health. The biosphere is experiencing with the pervasive presence of heavy metal pollutants such as arsenic (As), cadmium (Cd), mercury (Hg), lead (Pb), chromium (Cr), copper (Cu) and nickel (Ni), which pose significant environmental challenges. While certain metals are essential for regulating fundamental metabolic processes and upholding the overall physiology of microorganisms, excessive exposure to heavy metals can be detrimental to their survival and function. As a result of their remarkable adaptability, microorganisms, particularly bacteria such as Pseudomonas fluorescens, Escherichia coli, Serratia marcescens, Bacillus cereus and Alcaligenes sp., have evolved sophisticated defence mechanisms to combat the stress caused by heavy metals. One such process is the creation of metal-binding proteins (MBPs), which may bind and sequester metals, thus significantly lowering their toxicity in bacteria. Metalloproteomics, a subfield of metallomics, focuses on the discovery and characterization of such metal-binding proteins (MBPs) in metal-resistant bacteria, resulting in the opening of the doors for innovative bioremediation techniques and therapeutic treatments against bacterial diseases. This review explores the intriguing world of MBPs in metal-resistant bacteria and emphasizes their significant role in metal resistance, detoxification and homeostasis. Furthermore, metallochaperones in bacteria have been extensively studied using the metalloproteomic methodologies and techniques utilized in metal-binding proteins. This study also provides useful information on the interactions between these metallochaperones and different MBPs, which advances our understanding of how bacteria respond to exposure to such heavy metals.

Keywords

Bacteria Bioremediation Metalloproteomics Metal-binding proteins Detoxification
Jamunasri, N., Iyer, A., Prabha, M. L., Issac, R., & Murugan, S. (2024). Metalloproteomics: Unraveling the Metal Binding Proteins of Diverse Metal-Resistant Bacteria. Asian Journal of Chemistry, 36(3), 531–542. https://doi.org/10.14233/ajchem.2024.31102
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References
  1. M. Csuros and C. Csuros, Environmental Sampling and Analysis for Metals, Lewis Publishers, Boca Raton, FL, USA (2002).
  2. Kiran, R. Bharti and R. Sharma, Mater. Today Proc., 51, 880 (2022); https://doi.org/10.1016/j.matpr.2021.06.278
  3. C.M. Laureano-Anzaldo, M.E. González-López, A.A. Pérez-Fonseca, L.E. Cruz-Barba and J.R. Robledo-Ortíz, Carbohydr. Polym., 252, 117195 (2021); https://doi.org/10.1016/j.carbpol.2020.117195
  4. M. Balali-Mood, K. Naseri, Z. Tahergorabi, M.R. Khazdair and M. Sadeghi, Front. Pharmacol., 12, 643972 (2021); https://doi.org/10.3389/fphar.2021.643972
  5. X. Li, M. Sun, L. Zhang, R.D. Finlay, R. Liu and B. Lian, Ecotoxicol. Environ. Saf., 246, 114193 (2022); https://doi.org/10.1016/j.ecoenv.2022.114193
  6. T.D. Thai, W. Lim and D. Na, Front. Bioeng. Biotechnol., 11, 1178680 (2023); https://doi.org/10.3389/fbioe.2023.1178680
  7. S. González-Henao and T. Ghneim-Herrera, Front. Environ. Sci., 9, 604216 (2021); https://doi.org/10.3389/fenvs.2021.604216
  8. A. Adeyinka, P. Sunday Mike and S.S. Terseer, Int. J. Curr. Microbiol. Appl. Sci., 12, 138 (2023); https://doi.org/10.20546/ijcmas.2023.1203.018
  9. D.A. Bukhari and A. Rehman, Curr. Opin. Green Sustain. Chem., 40, 100785 (2023); https://doi.org/10.1016/j.cogsc.2023.100785
  10. R.K. Kushwaha, S.M. Joshi, R. Bajaj, A. Mastan, V. Kumar, H. Patel, S. Jayashree and S.P. Chaudhary, Funct. Plant Biol., 50, 482 (2023); https://doi.org/10.1071/FP22263
  11. H. Kinoshita, Methods Mol. Biol., 1887, 145 (2019); https://doi.org/10.1007/978-1-4939-8907-2_13
  12. P. Sharma, A.K. Pandey, A. Udayan and S. Kumar, Bioresour. Technol., 326, 124750 (2021); https://doi.org/10.1016/j.biortech.2021.124750
  13. S. Sun, M. Wang, J. Xiang, Y. Shao, L. Li, R.C.A.A. Sedjoah, G. Wu, J. Zhou and Z. Xin, Int. J. Biol. Macromol., 238, 124062 (2023); https://doi.org/10.1016/j.ijbiomac.2023.124062
  14. H. Yoshida, T. Shimada and A. Ishihama, Int. J. Mol. Sci., 24, 4717 (2023); https://doi.org/10.3390/ijms24054717
  15. A. Mikhaylina, A.Z. Ksibe, D.J. Scanlan and C.A. Blindauer, Biochem. Soc. Trans., 46, 983 (2018); https://doi.org/10.1042/BST20170228
  16. A.J. Guerra and D.P. Giedroc, 35 (2013); https://doi.org/10.1016/B978-0-08-097774-4.00305-3
  17. D. Osman and J.S. Cavet, Nat. Prod. Rep., 27, 668 (2010); https://doi.org/10.1039/B906682A
  18. K. Furukawa, A. Ramesh, Z. Zhou, Z. Weinberg, T. Vallery, W.C. Winkler and R.R. Breaker, Mol. Cell, 57, 1088 (2015); https://doi.org/10.1016/j.molcel.2015.02.009
  19. D. Gupta, S. Satpati, A. Dixit and R. Ranjan, Appl. Microbiol. Biotechnol., 103, 5411 (2019); https://doi.org/10.1007/s00253-019-09852-6
  20. P.L. Hagedoorn, Proteomes, 3, 424 (2015); https://doi.org/10.3390/proteomes3040424
  21. X. Sun, C. Xiao, R. Ge, X. Yin, H. Li, N. Li, X. Yang, Y. Zhu, X. He and Q.-Y. He, Proteomics, 11, 3288 (2011); https://doi.org/10.1002/pmic.201000396
  22. E. Goethe, A. Gieseke, K. Laarmann, J. Luhrs and R. Goethe, J. Bacteriol., 203, e00049-21 (2021); https://doi.org/10.1128/JB.00049-21
  23. J. Briffa, E. Sinagra and R. Blundell, Heliyon, 6, e04691 (2020); https://doi.org/10.1016/j.heliyon.2020.e04691
  24. S. Mitra, A.J. Chakraborty, A.M. Tareq, T. Emran, F. Bin, A. Nainu, A. Khusro, M. Idris, M.U. Khandaker, H. Osman, F.A. Alhumaydhi and J. Simal-Gandara, J. King Saud Univ. Sci., 34, 101865 (2022); https://doi.org/10.1016/j.jksus.2022.101865
  25. N. Akhtar, M.I. Syakir Ishak, S.A. Bhawani and K. Umar, Water, 13, 2660 (2021); https://doi.org/10.3390/w13192660
  26. J. Saha, S. Adhikary and A. Pal, Geomicrobiol. J., 39, 891 (2022); https://doi.org/10.1080/01490451.2022.2089781
  27. X. Hao, J. Zhu, C. Rensing, Y. Liu, S. Gao, W. Chen, Q. Huang and Y.-R. Liu, Comput. Struct. Biotechnol. J., 19, 94 (2021); https://doi.org/10.1016/j.csbj.2020.12.006
  28. R. Dixit, D. Wasiullah, D. Malaviya, K. Pandiyan, U. Singh, A. Sahu, R. Shukla, B. Singh, J. Rai, P. Sharma, H. Lade and D. Paul, Sustainability, 7, 2189 (2015); https://doi.org/10.3390/su7022189
  29. N. Thirumoorthy, K. T. M. Kumar, A. S. Sundar, L. Panayappan and M. Chatterjee, World J. Gastroenterol., 13, 993 (2007); https://doi.org/10.3748/wjg.v13.i7.993
  30. K. Mathivanan, J.U. Chandirika, A. Vinothkanna, H. Yin, X. Liu and D. Meng, Ecotoxicol. Environ. Saf., 226, 112863 (2021); https://doi.org/10.1016/j.ecoenv.2021.112863
  31. P. Vats, U.J. Kaur and P. Rishi, J. Appl. Microbiol., 132, 4058 (2022); https://doi.org/10.1111/jam.15492
  32. A.C. Carroll and A. Wong, Can. J. Microbiol., 64, 293 (2018); https://doi.org/10.1139/cjm-2017-0609
  33. A. Escamilla-Rodríguez, S. Carlos-Hernández and L. Díaz-Jiménez, Water, 13, 2766 (2021); https://doi.org/10.3390/w13192766
  34. W. Yin, Y. Wang, L. Liu and J. He, Int. J. Mol. Sci., 20, 3423 (2019); https://doi.org/10.3390/ijms20143423
  35. M. Medfu Tarekegn, F. Zewdu Salilih and A.I. Ishetu, Cogent Food Agric., 6, 1783174 (2020); https://doi.org/10.1080/23311932.2020.1783174
  36. P. Chandrangsu, C. Rensing and J.D. Helmann, Nat. Rev. Microbiol., 15, 338 (2017); https://doi.org/10.1038/nrmicro.2017.15
  37. P. Chandrangsu, C. Rensing and J.D. Helmann, Nat. Rev. Microbiol., 15, 379 (2017); https://doi.org/10.1038/nrmicro.2017.53
  38. C. Parsons, S. Lee and S. Kathariou, Mol. Microbiol., 113, 560 (2020); https://doi.org/10.1111/mmi.14470
  39. B.M. Staehlin, J.G. Gibbons, A. Rokas, T.V. O’Halloran and J.C. Slot, Genome Biol. Evol., 8, 811 (2016); https://doi.org/10.1093/gbe/evw031
  40. L. Banci, I. Bertini, K.S. McGreevy and A. Rosato, Nat. Prod. Rep., 27, 695 (2010); https://doi.org/10.1039/b906678k
  41. U.O. Edet, I.U. Bassey and A.P. Joseph, Heliyon, 9, e13457 (2023); https://doi.org/10.1016/j.heliyon.2023.e13457
  42. V. Kumar, A. Kumari, M. Pandey and M. Sharma, Molecular Mechanism of Radio-Resistance and Heavy Metal Tolerance Adaptation In Microbes, In: Microbial Extremozymes Novel Sources and Industrial Applications, Academic Press, Chap. 21, pp. 275-293 (2022); https://doi.org/10.1016/B978-0-12-822945-3.00003-8
  43. G. Porcheron, A. Garénaux, J. Proulx, M. Sabri and C.M. Dozois, Front. Cell. Infect. Microbiol., 3, 1 (2013); https://doi.org/10.3389/fcimb.2013.00090
  44. C.J. Murray, K.S. Ikuta, F. Sharara, L. Swetschinski, G. Robles Aguilar, A. Gray, C. Han, C. Bisignano, P. Rao, E. Wool, S.C. Johnson, A.J. Browne, M.G. Chipeta, F. Fell, S. Hackett, G. Haines-Woodhouse, B.H. Kashef Hamadani, E.A.P. Kumaran, B. McManigal, S. Achalapong, R. Agarwal, S. Akech, S. Albertson, J. Amuasi, J. Andrews, A. Aravkin, E. Ashley, F.-X. Babin, F. Bailey, S. Baker, B. Basnyat, A. Bekker, R. Bender, J.A. Berkley, A. Bethou, J. Bielicki, S. Boonkasidecha, J. Bukosia, C. Carvalheiro, C. Castañeda-Orjuela, V. Chansamouth, S. Chaurasia, S. Chiurchiù, F. Chowdhury, R. Clotaire Donatien, A.J. Cook, B. Cooper, T.R. Cressey, E. Criollo-Mora, M. Cunningham, S. Darboe, N.P.J. Day, M. De Luca, K. Dokova, A. Dramowski, S.J. Dunachie, T. Duong Bich, T. Eckmanns, D. Eibach, A. Emami, N. Feasey, N. Fisher-Pearson, K. Forrest, C. Garcia, D. Garrett, P. Gastmeier, A.Z. Giref, R.C. Greer, V. Gupta, S. Haller, A. Haselbeck, S.I. Hay, M. Holm, S. Hopkins, Y. Hsia, K.C. Iregbu, J. Jacobs, D. Jarovsky, F. Javanmardi, A.W.J. Jenney, M. Khorana, S. Khusuwan, N. Kissoon, E. Kobeissi, T. Kostyanev, F. Krapp, R. Krumkamp, A. Kumar, H.H. Kyu, C. Lim, K. Lim, D. Limmathurotsakul, M.J. Loftus, M. Lunn, J. Ma, A. Manoharan, F. Marks, J. May, M. Mayxay, N. Mturi, T. Munera-Huertas, P. Musicha, L.A. Musila, M.M. Mussi-Pinhata, R.N. Naidu, T. Nakamura, R. Nanavati, S. Nangia, P. Newton, C. Ngoun, A. Novotney, D. Nwakanma, C.W. Obiero, T.J. Ochoa, A. Olivas-Martinez, P. Olliaro, E. Ooko, E. Ortiz-Brizuela, P. Ounchanum, G.D. Pak, J.L. Paredes, A.Y. Peleg, C. Perrone, T. Phe, K. Phommasone, N. Plakkal, A. Ponce-de-Leon, M. Raad, T. Ramdin, S. Rattanavong, A. Riddell, T. Roberts, J.V. Robotham, A. Roca, V.D. Rosenthal, K.E. Rudd, N. Russell, H.S. Sader, W. Saengchan, J. Schnall, J.A.G. Scott, S. Seekaew, M. Sharland, M. Shivamallappa, J. Sifuentes-Osornio, A.J. Simpson, N. Steenkeste, A.J. Stewardson, T. Stoeva, N. Tasak, A. Thaiprakong, G. Thwaites, C. Tigoi, C. Turner, P. Turner, H.R. van Doorn, S. Velaphi, A. Vongpradith, M. Vongsouvath, H. Vu, T. Walsh, J.L. Walson, S. Waner, T. Wangrangsimakul, P. Wannapinij, T. Wozniak, T.E.M.W. Young Sharma, K.C. Yu, P. Zheng, B. Sartorius, A.D. Lopez, A. Stergachis, C. Moore, C. Dolecek and M. Naghavi, Lancet, 399, 629 (2022); https://doi.org/10.1016/S0140-6736(21)02724-0
  45. J.L. Hobman and L.C. Crossman, J. Med. Microbiol., 64, 471 (2015); https://doi.org/10.1099/jmm.0.023036-0
  46. M.-R. Meini, L.J. González and A.J. Vila, Future Microbiol., 8, 947 (2013); https://doi.org/10.2217/fmb.13.34
  47. M. Ellerman and J.C. Arthur, Free Rad. Biol. Med., 105, 68 (2017); https://doi.org/10.1016/j.freeradbiomed.2016.10.489
  48. I.J. Schalk, C. Rigouin and J. Godet, Environ. Microbiol., 22, 1447 (2020); https://doi.org/10.1111/1462-2920.14937
  49. M. Remenár, A. Kamlárova, J. Harichova, M. Zámocky and P. Ferianc, Pol. J. Microbiol., 67, 191 (2018); https://doi.org/10.21307/pjm-2018-022
  50. C. Yuan, P. Li, C. Qing, Z. Kou and H. Wang, Front. Microbiol., 13, 817891 (2022); https://doi.org/10.3389/fmicb.2022.817891
  51. J. Daniels and E. Spencer, in eds.: M.E. and M.A. Peterson, Bacterial Infections, In: Small Animal Pediatrics. Elsevier; Saint Louis, MO, USA, edn. 1, pp. 113–118 (2011).
  52. S.Z. Abbas, M. Rafatullah, K. Hossain, N. Ismail, H.A. Tajarudin and H.P.S. Abdul Khalil, Int. J. Environ. Sci. Technol., 2017, 243 (2017); https://doi.org/10.1007/s13762-017-1400-5
  53. P.K. Singh, M. Tang, S. Kumar and A.K. Shrivastava, Arch. Microbiol., 200, 463 (2018); https://doi.org/10.1007/s00203-017-1462-2
  54. G. Din, A. Farooqi, W. Sajjad, M. Irfan, S. Gul and A. Ali Shah, J. Basic Microbiol., 61, 230 (2021); https://doi.org/10.1002/jobm.202000538
  55. Y. Sheng, X. Yang, Y. Lian, B. Zhang, X. He, W. Xu and K. Huang, Environ. Toxicol. Pharmacol., 46, 286 (2016); https://doi.org/10.1016/j.etap.2016.08.008
  56. S.M. Damo, T.E. Kehl-Fie, N. Sugitani, M.E. Holt, S. Rathi, W.J. Murphy, Y. Zhang, C. Betz, L. Hench, G. Fritz, E.P. Skaar and W.J. Chazin, Proc. Natl. Acad. Sci. USA, 110, 3841 (2013); https://doi.org/10.1073/pnas.1220341110.
  57. T.G. Nakashige, E.M. Zygiel, C.L. Drennan and E.M. Nolan, J. Am. Chem. Soc., 139, 8828 (2017); https://doi.org/10.1021/jacs.7b01212
  58. C.A. Navarro, D. Von Bernath, C. Martínez-Bussenius, R.A. Castillo and C.A. Jerez, Appl. Environ. Microbiol., 82, 1015 (2016); https://doi.org/10.1128/AEM.02810-15
  59. K. Peters, M. Pazos, Z. Edoo, J. Hugonnet, A.M. Martorana, A. Polissi, M.S. VanNieuwenhze, M. Arthur and W. Vollmer, Proc. Natl. Acad. Sci. USA, 115, 10786 (2018); https://doi.org/10.1073/pnas.1809285115
  60. V. Cappello, L. Marchetti, P. Parlanti, S. Landi, I. Tonazzini, M. Cecchini, V. Piazza and M. Gemmi, Sci. Rep., 6, 1 (2016); https://doi.org/10.1038/s41598-016-0001-8
  61. Z. Guo, J. Han, X.Y. Yang, K. Cao, K. He, G. Du, G. Zeng, L. Zhang, G. Yu, Z. Sun, Q.-Y. He and X. Sun, Metallomics, 7, 448 (2015); https://doi.org/10.1039/C4MT00276H
  62. K.Y. Djoko, Z. Xiao, D.L. Huffman and A.G. Wedd, Inorg. Chem., 46, 4560 (2007); https://doi.org/10.1021/ic070107o
  63. J.M. Parks and J.C. Smith, Methods Enzymol., 578, 103 (2016); https://doi.org/10.1016/bs.mie.2016.05.041
  64. M. Priyadarshanee, S. Chatterjee, S. Rath, H.R. Dash and S. Das, J. Hazard. Mater., 423, 126985 (2022); https://doi.org/10.1016/j.jhazmat.2021.126985
  65. V. Keshav, I. Achilonu, H.W. Dirr and K. Kondiah, Protein Expr. Purif., 158, 27 (2019); https://doi.org/10.1016/j.pep.2019.02.008
  66. H. Chen, J. Xu, W. Tan and L. Fang, Environ. Pollut., 250, 118 (2019); https://doi.org/10.1016/j.envpol.2019.03.123
  67. Q. Nong, K. Yuan, Z. Li, P. Chen, Y. Huang, L. Hu, J. Jiang, T. Luan and B. Chen, J. Environ. Sci. (China), 85, 46 (2019); https://doi.org/10.1016/j.jes.2019.04.022
  68. S. Liu, Y. Zheng, Y. Ma, A. Sarwar, X. Zhao, T. Luo and Z. Yang, Int. J. Mol. Sci., 20, 5540 (2019); https://doi.org/10.3390/ijms20225540
  69. T. Rosen, R.C. Hadley, A.T. Bozzi, D. Ocampo, J. Shearer and E.M. Nolan, Metallomics, 14, mfac001 (2022); https://doi.org/10.1093/mtomcs/mfac001
  70. H.G. Colaço, P.E. Santo, P.M. Matias, T.M. Bandeiras and J.B. Vicente, Metallomics, 8, 327 (2016); https://doi.org/10.1039/C5MT00291E
  71. R. Shirakawa, K. Ishikawa, K. Furuta and C. Kaito, PLoS One, 18, e0277162 (2023); https://doi.org/10.1371/journal.pone.0277162
  72. Y. Li, M.R. Sharma, R.K. Koripella, Y. Yang, P.S. Kaushal, Q. Lin, J.T. Wade, T.A. Gray, K.M. Derbyshire, R.K. Agrawal and A.K. Ojha, Proc. Natl. Acad. Sci. USA, 115, 8191 (2018); https://doi.org/10.1073/pnas.1804555115
  73. D.P. Neupane, D. Avalos, S. Fullam, H. Roychowdhury and E.T. Yukl, J. Biol. Chem., 292, 17496 (2017); https://doi.org/10.1074/jbc.M117.804799
  74. E. Parameswari, T. Ilakiya, V. Davamani, P. Kalaiselvi and S.P. Sebastian, in eds.: M.K. Nazal and H. Zhao, Metallothioneins: Diverse Protein Family to Bind Metallic Ions, In: Heavy Metals - Their Environmental Impacts and Mitigation, IntechOpen (2021); https://doi.org/10.5772/intechopen.97658
  75. S. Chatterjee, S. Kumari, S. Rath, M. Priyadarshanee and S. Das, Metallomics, 12, 1637 (2020); https://doi.org/10.1039/d0mt00140f
  76. F. Lehembre, D. Doillon, E. David, S. Perrotto, J. Baude, J. Foulon, L. Harfouche, L. Vallon, J. Poulain, C. Da Silva, P. Wincker, C. Oger-Desfeux, P. Richaud, J.V. Colpaert, M. Chalot, L. Fraissinet-Tachet, D. Blaudez and R. Marmeisse, Environ. Microbiol., 15, 2829 (2013); https://doi.org/10.1111/1462-2920.12143
  77. S. Murthy, G. Bali and S.K. Sarangi, Afr. J. Biotechnol., 10, 15966 (2011); https://doi.org/10.5897/AJB11.1645
  78. S.A. Loutet, A.C.K. Chan, M.J. Kobylarz, M.M. Verstraete, S. Pfaffen, B. Ye, A.L. Arrieta and M.E.P. Murphy, in eds.: J.O. Nriagu and E.P. Skaar, The Fate of Intracellular Metal Ions in Microbes, In: Trace Metals and Infectious Diseases, MIT Press, pp. 39–56 (2015).
  79. F.A. Vaccaro and C.L. Drennan, Metallomics, 14, mfac030 (2022); https://doi.org/10.1093/mtomcs/mfac030
  80. D.A. Capdevila, K.A. Edmonds and D.P. Giedroc, Essays Biochem., 61, 177 (2017); https://doi.org/10.1042/EBC20160076
  81. S. Ammendola, P. Pasquali, C. Pistoia, P. Petrucci, P. Petrarca, G. Rotilio and A. Battistoni, Infect. Immun., 75, 5867 (2007); https://doi.org/10.1128/IAI.00559-07
  82. E.V. Anyaogu, C.N. Umeaku, A.M. Isirue, O. S. Esiobu and N.U. Onuoha, GSC Biol. Pharm. Sci., 21, 88 (2022); https://doi.org/10.30574/gscbps.2022.21.2.0415
  83. H. Johnson, H. Cho, M. Choudhary, H. Johnson, H. Cho and M. Choudhary, Comput. Mol. Biosci., 9, 1 (2019); https://doi.org/10.4236/cmb.2019.91001
  84. Z. Guo, J. Han, X.Y. Yang, K. Cao, K. He, G. Du, G. Zeng, L. Zhang, G. Yu, Z. Sun, Q.Y. He and X. Sun, Metallomics, 7, 1613 (2015); https://doi.org/10.1039/C5MT90043C
  85. S. Nath, I. Sharma, B. Deb and V. Singh, Int. J. Bio-resource Stress Manag., 4, 266 (2013).
  86. M.A. Da Silva, A. Sussulini and M.A. Arruda, Expert Rev. Proteomics, 7, 387 (2010); https://doi.org/10.1586/epr.10.16
  87. P.L. Hagedoorn, in eds.: J.O. Nriagu and E.P. Skaar, Emerging Strategies in Metalloproteomics, In: Trace Metals and Infectious Diseases, Cambridge, MA, Chap. 18, pp. 311-322 (2015).
  88. X. Xu, H. Wang, H. Li and H. Sun, Chem. Lett., 49, 697 (2020); https://doi.org/10.1246/cl.200155
  89. M.-L. Chen and M. Wang, At., 43, 255 (2022); https://doi.org/10.46770/AS.2022.108
  90. M. Ouyang, J. Wu, Y. Yan and C.F. Ding, Anal. Lett., 56, 1016 (2023); https://doi.org/10.1080/00032719.2022.2116644
  91. R. Irankunda, J.A. Camaño Echavarría, C. Paris, L. Stefan, S. Desobry, K. Selmeczi, L. Muhr and L. Canabady-Rochelle, Separations, 9, 11 (2022); https://doi.org/10.3390/separations9110370
  92. P.L. Jiang, C. Wang, A. Diehl, R. Viner, C. Etienne, P. Nandhikonda, L. Foster, R.D. Bomgarden and F. Liu, Angew. Chem. Int. Ed., 61, e202113937 (2022); https://doi.org/10.1002/anie.202113937
  93. B. Steigenberger, R.J. Pieters, A.J.R. Heck and R.A. Scheltema, ACS Cent. Sci., 5, 1514 (2019); https://doi.org/10.1021/acscentsci.9b00416
  94. M. Montes-Bayón and J. Bettmer, Adv. Exp. Med. Biol., 1055, 111 (2018); https://doi.org/10.1007/978-3-319-90143-5_6
  95. P. Iadarola, Molecules, 24, 1133 (2019); https://doi.org/10.3390/molecules24061133
  96. I. Tolbatov, N. Re, C. Coletti and A. Marrone, Inorg. Chem., 59, 790 (2020); https://doi.org/10.1021/acs.inorgchem.9b03059
  97. M.A. Hough and R.L. Owen, Curr. Opin. Struct. Biol., 71, 232 (2021); https://doi.org/10.1016/j.sbi.2021.07.007
  98. A. Volbeda, Methods Mol. Biol., 1122, 189 (2014); https://doi.org/10.1007/978-1-62703-794-5_13
  99. T. Huxford, X-Ray Crystallography, In: Brenner’s Encyclopedia of Genetics, Elsevier Reference Collection in Life Sciences, pp. 366-368 (2013); https://doi.org/10.1016/B978-0-12-374984-0.01657-0
  100. H. Li and H. Sun, Top. Curr. Chem., 326, 69 (2011); https://doi.org/10.1007/128_2011_214
  101. M. Piccioli, Magnetochemistry, 6, 46 (2020); https://doi.org/10.3390/magnetochemistry6040046
  102. M.T. Stiebritz and Y. Hu, Methods Mol. Biol., 1876, 245 (2019); https://doi.org/10.1007/978-1-4939-8864-8_16
  103. J. Li, X. He, S. Gao, Y. Liang, Z. Qi, Q. Xi, Y. Zuo and Y. Xing, J. Mol. Biol., 435, 168117 (2023); https://doi.org/10.1016/j.jmb.2023.168117
  104. L.A. Kelley, S. Mezulis, C.M. Yates, M.N. Wass and M.J. Sternberg, Nat. Protoc., 10, 845 (2015); https://doi.org/10.1038/nprot.2015.053
  105. C.H. Lu, Y.F. Lin, J.J. Lin and C.S. Yu, PLoS One, 7, e39252 (2012); https://doi.org/10.1371/journal.pone.0039252
  106. M. Kapahi and S. Sachdeva, J. Health Pollut., 9, 1 (2019); https://doi.org/10.5696/2156-9614-9.24.191203
  107. B. Mariáh da Silva e Silva and C. Rodrigues e Silva, Rev. Virtual Quim., 12, 1097 (2020); https://doi.org/10.21577/1984-6835.20200090
  108. R.A. Hauser-Davis, R.M. Lopes, F.B. Mota and J.C. Moreira, Ecotoxicol. Environ. Saf., 140, 279 (2017); https://doi.org/10.1016/j.ecoenv.2017.02.024
  109. P.R. Sreedevi, K. Suresh and G. Jiang, J. Water Process Eng., 48, 102884 (2022); https://doi.org/10.1016/j.jwpe.2022.102884
  110. Y. Ma, Y. Wang, X.J. Shi, X.P. Chen and Z.L. Li, Environ. Sci., 43, 4911 (2022); https://doi.org/10.13227/J.HJKX.202112007
  111. Y. Zhou, H. Li and H. Sun, Annu. Rev. Biochem., 91, 449 (2022); https://doi.org/10.1146/annurev-biochem-040320-104628
  112. G. Wallace, I. Eisenberg, B. Robustelli, N. Dankner, L. Kenworthy, J. Giedd and A. Martin, J. Am. Acad. Child Adolesc. Psychiatry, 54, 464 (2015); https://doi.org/10.1016/j.jaac.2015.03.007
  113. S. Sher, S. Sultan and A. Rehman, Appl. Water Sci., 11, 69 (2021); https://doi.org/10.1007/s13201-021-01407-3
  114. S.Z. Abbas, M. Riaz, N. Ramzan, M.T. Zahid, F.R. Shakoori and M. Rafatullah, 45, 1309 (2014); https://doi.org/10.1590/S1517-83822014000400022
  115. A. Ali, M. Li, J. Su, Y. Li, Z. Wang, Y. Bai, E.F. Ali and S.M. Shaheen, Sci. Total Environ., 813, 152668 (2022); https://doi.org/10.1016/j.scitotenv.2021.152668
  116. H. Kumar, S. Ishtiyaq, P.J.C. Favas, M. Varun and M.S. Paul, J. Plant Growth Regul., 42, 3868 (2023); https://doi.org/10.1007/s00344-022-10853-5
  117. W.M.N.H. Kumari, S. Thiruchittampalam, M.S.S. Weerasinghe, N.V. Chandrasekharan and C.D. Wijayarathna, Appl. Microbiol. Biotechnol., 105, 2573 (2021); https://doi.org/10.1007/s00253-021-11193-2
  118. K. Yamamoto and Y. Tamaru, AMB Express, 6, 1 (2016); https://doi.org/10.1186/s13568-015-0169-5
  119. K. Gopi, H.N. Jinal, P. Prittesh, V.P. Kartik and N. Amaresan, Int. J. Phytoremediation, 22, 662 (2020); https://doi.org/10.1080/15226514.2019.1707161
  120. M. Noman, T. Ahmed, S. Hussain, M.B.K. Niazi, M. Shahid and F. Song, J. Hazard. Mater., 398, 123175 (2020); https://doi.org/10.1016/j.jhazmat.2020.123175
  121. T.M. Palanivel, N. Sivakumar, A. Al-Ansari and R. Victor, J. Environ. Manage., 253, 109706 (2020); https://doi.org/10.1016/j.jenvman.2019.109706
  122. F. Altimira, C. Yáñez, G. Bravo, M. González, L.A. Rojas and M. Seeger, BMC Microbiol., 12, 193 (2012); https://doi.org/10.1186/1471-2180-12-193
  123. H. Yao, H. Wang, J. Ji, A. Tan, Y. Song and Z. Chen, Toxics, 11, 261 (2023); https://doi.org/10.3390/toxics11030261
  124. J.P. Bourdineaud, G. Durn, B. Režun, A. Manceau and J. Hrenoviæ, Chemosphere, 248, 126002 (2020); https://doi.org/10.1016/j.chemosphere.2020.126002
  125. M. Agarwal, R.S. Rathore, C. Jagoe and A. Chauhan, Cells, 8, 309 (2019); https://doi.org/10.3390/cells8040309
  126. S.Z. Abbas, C.J. Yee, K. Hossain, A. Ahmad and M. Rafatullah, Desalination Water Treat., 138, 128 (2019); https://doi.org/10.5004/dwt.2019.23279
  127. T. Mo, D. Jiang, D. Shi, S. Xu, X. Huang and Z. Huang, Ecol. Process., 11, 20 (2022); https://doi.org/10.1186/s13717-021-00347-9
  128. A.S. Ayangbenro and O.O. Babalola, Sci. Rep., 10, 19660 (2020); https://doi.org/10.1038/s41598-020-75170-x
  129. R.K. Mohapatra, P.K. Parhi, S. Pandey, B.K. Bindhani, H. Thatoi and C.R. Panda, J. Environ. Manage., 247, 121 (2019); https://doi.org/10.1016/j.jenvman.2019.06.073
  130. Z. Teng, W. Shao, K. Zhang, Y. Huo and M. Li, J. Environ. Manage., 231, 189 (2019); https://doi.org/10.1016/j.jenvman.2018.10.012
  131. T. von Rozycki and D.H. Nies, Antonie van Leeuwenhoek, 96, 115 (2009); https://doi.org/10.1007/s10482-008-9284-5
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