1932

Abstract

Chirality in life has been preserved throughout evolution. It has been assumed that the main function of chirality is its contribution to structural properties. In the past two decades, however, it has been established that chiral molecules possess unique electronic properties. Electrons that pass through chiral molecules, or even charge displacements within a chiral molecule, do so in a manner that depends on the electron's spin and the molecule's enantiomeric form. This effect, referred to as chiral induced spin selectivity (CISS), has several important implications for the properties of biosystems. Among these implications, CISS facilitates long-range electron transfer, enhances bio-affinities and enantioselectivity, and enables efficient and selective multi-electron redox processes. In this article, we review the CISS effect and some of its manifestations in biological systems. We argue that chirality is preserved so persistently in biology not only because of its structural effect, but also because of its important function in spin polarizing electrons.

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2022-05-09
2024-06-19
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Literature Cited

  1. 1.
    Abendroth JM, Nakatsuka N, Ye M, Kim D, Fullerton EE et al. 2017. Analyzing spin selectivity in DNA-mediated charge transfer via fluorescence microscopy. ACS Nano 11:7516–26
    [Google Scholar]
  2. 2.
    Avnir D. 2021. Critical review of chirality indicators of extraterrestrial life. New Astron. Rev. 92:101596
    [Google Scholar]
  3. 3.
    Babcock GT. 1999. How oxygen is activated and reduced in respiration. PNAS 96:12971–73
    [Google Scholar]
  4. 4.
    Banerjee-Ghosh K, Ghosh S, Mazal H, Riven I, Haran G, Naaman R. 2020. Long-range charge reorganization as an allosteric control signal in proteins. J. Am. Chem. Soc. 142:20456–62
    [Google Scholar]
  5. 5.
    Banerjee-Ghosh K, Zhang W, Tassinari F, Mastai Y, Lidor-Shalev O et al. 2019. Controlling chemical selectivity in electrocatalysis with chiral CuO-coated electrodes. J. Phys. Chem. C 123:3024–31
    [Google Scholar]
  6. 6.
    Beratan DN, Liu CR, Migliore A, Polizzi NF, Skourtis SS et al. 2015. Charge transfer in dynamical biosystems, or the treachery of (static) images. Acc. Chem. Res. 48:2474–81
    [Google Scholar]
  7. 7.
    Beratan DN, Naaman R, Waldeck DH. 2017. Charge and spin transport through nucleic acids. Curr. Opin. Electrochem. 4:175–81
    [Google Scholar]
  8. 8.
    Blankenship RE. 2014. Molecular Mechanisms of Photosynthesis. Hoboken, NJ: Wiley
    [Google Scholar]
  9. 9.
    Bloom BP, Graff BM, Ghosh S, Beratan DN, Waldeck DH. 2017. Chirality control of electron transfer in quantum dot assemblies. J. Am. Chem. Soc. 139:9038–43
    [Google Scholar]
  10. 10.
    Cahn RS, Ingold C, Prelog V. 1996. Specification of molecular chirality. Angew. Chem. Int. Ed. 5:385–415
    [Google Scholar]
  11. 11.
    Cohen-Tannoudji C, Dupont J, Grynberg RG. 1998. Atom-Photon Interactions: Basic Processes and Applications Hoboken, NJ: Wiley
    [Google Scholar]
  12. 12.
    Garcés-Pineda FA, Blasco-Ahicart M, Nieto-Castro D, López N, Galán-Mascarós JR. 2019. Direct magnetic enhancement of electrocatalytic water oxidation in alkaline media. Nat. Energy 4:519–25
    [Google Scholar]
  13. 13.
    Gazzotti M, Stefani A, Bonechi M, Giurlani W, Innocenti M, Fontanesi C. 2020. Influence of chiral compounds on the oxygen evolution reaction (OER) in the water splitting process. Molecules 25:3988
    [Google Scholar]
  14. 14.
    Ghosh S, Bloom BP, Lu Y, Lamont D, Waldeck DH 2020. Increasing the efficiency of water splitting through spin polarization using cobalt oxide thin film catalysts. J. Phys. Chem. C 124:22610–18
    [Google Scholar]
  15. 15.
    Ghosh S, Mishra S, Avigad E, Bloom BP, Baczewski LT et al. 2020. Effect of chiral molecules on the electron's spin wavefunction at interfaces. J. Phys. Chem. Lett. 11:1550–57
    [Google Scholar]
  16. 16.
    Goehler B, Hamelbeck V, Markus TZ, Kettner M, Hanne GF et al. 2011. Spin selectivity in electron transmission through self-assembled monolayers of double-stranded DNA. Science 331:894–97
    [Google Scholar]
  17. 17.
    Gracia J. 2017. Spin dependent interactions catalyse the oxygen electrochemistry. Phys. Chem. Chem. Phys. 19:20451–56
    [Google Scholar]
  18. 18.
    Gray HB, Winkler JR. 2003. Electron tunneling through proteins. Q. Rev. Biophys. 36:3341–72
    [Google Scholar]
  19. 19.
    Hohenberg P, Kohn W. 1964. Inhomogeneous electron gas. Phys. Rev. 136:B864–71
    [Google Scholar]
  20. 20.
    Jones ML, Kurnikov IV, Beratan DN. 2002. The nature of tunneling pathway and average packing density models for protein-mediated electron transfer. J. Phys. Chem. A 106:2002–6
    [Google Scholar]
  21. 21.
    Kettner M, Gohler B, Zacharias H, Mishra D, Kiran V et al. 2015. Spin filtering in electron transport through chiral oligopeptides. J. Phys. Chem. C 119:14542–47
    [Google Scholar]
  22. 22.
    Kohn KP, Underwood SM, Cooper MM. 2018. Connecting structure-property and structure-function relationships across the disciplines of chemistry and biology: exploring student perceptions. CBE Life Sci. Educ. 17:ar33
    [Google Scholar]
  23. 23.
    Koshland DE. 1994. The key-lock theory and the induced fit theory. Angew. Chem. Int. Ed. 33:2375–78
    [Google Scholar]
  24. 24.
    Kulkarni C, Mondal AK, Das TK, Grinbom G, Tassinari F et al. 2020. Highly efficient and tunable filtering of electrons’ spin by supramolecular chirality of nanofiber-based materials. Adv. Mat. 32:1904965
    [Google Scholar]
  25. 25.
    Kumar A, Capua E, Kesharwani MK, Martin JML, Sitbon E et al. 2017. Chirality-induced spin polarization places symmetry constraints on biomolecular interactions. PNAS 114:2474–78
    [Google Scholar]
  26. 26.
    Linthorne NP, Thomas JM. 2016. The effect of ball spin rate on distance achieved in a long soccer throw-in. Procedia Eng 147:677–82
    [Google Scholar]
  27. 27.
    London F. 1937. The general theory of molecular forces. Trans. Faraday Soc. 33:8–26
    [Google Scholar]
  28. 28.
    Lu H, Wang J, Xiao C, Pan X, Chen X et al. 2019. Spin-dependent charge transport through 2D chiral hybrid lead-iodide perovskites. Sci. Adv. 5:eaay0571
    [Google Scholar]
  29. 29.
    Mason SF. 1984. Origins of biomolecular handedness. Nature 311:19–23
    [Google Scholar]
  30. 30.
    Massimi M. 2005. Pauli's Exclusion Principle: The Origin and Validation of a Scientific Principle Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  31. 31.
    Medina E, Lopez F, Ratner MA, Mujica V. 2012. Chiral molecular films as electron polarizers and polarization modulators. EPL 99:17006
    [Google Scholar]
  32. 32.
    Meirzada I, Sukenik N, Haim G, Yochelis S, Baczewski LT et al. 2021. Long-timescale magnetization ordering induced by an adsorbed chiral monolayer on ferromagnets. ACS Nano 15:35574–79
    [Google Scholar]
  33. 33.
    Minaev BF. 2002. Spin effects in reductive activation of O2 by oxydase enzymes. RIKEN Review No. 44 (February, 2002): Focused on Magnetic Field and Spin Effects in Chemistry and Related Phenomena147–49 Hyogo, Jpn: RIKEN
    [Google Scholar]
  34. 34.
    Mishra D, Markus TZ, Naaman R, Kettner M, Göhler B et al. 2013. Spin-dependent electron transmission through bacteriorhodopsin embedded in purple membrane. PNAS 110:3714872–76
    [Google Scholar]
  35. 35.
    Mishra S, Mondal AK, Pal S, Das TK, Smolinsky EZB et al. 2020. Length-dependent electron spin polarization in oligopeptides and DNA. J. Phys. Chem. C 124:10776–82
    [Google Scholar]
  36. 36.
    Mishra S, Pirbadian S, Mondal AK, El-Naggar MY, Naaman R. 2019. Spin-dependent electron transport through bacterial cell surface multiheme electron conduits. J. Am. Chem. Soc. 141:19198–202
    [Google Scholar]
  37. 37.
    Mishra S, Poonia VS, Fontanesi C, Naaman R, Fleming AM, Burrows CJ 2019. The effect of oxidative damage on charge and spin transport in DNA. J. Am. Chem. Soc. 141:123–26
    [Google Scholar]
  38. 38.
    Mondal AK, Preuss MD, Ślęczkowski ML, Das TK, Vantomme G et al. 2021. Spin filtering in supramolecular polymers assembled from achiral monomers mediated by chiral solvents. J. Am. Chem. Soc. 143:7189–95
    [Google Scholar]
  39. 39.
    Morgenstern A, Wilson TR, Eberhart ME. 2017. Predicting chemical reactivity from the charge density through gradient bundle analysis: moving beyond Fukui. J. Phys. Chem. A 121:4341–51
    [Google Scholar]
  40. 40.
    Mtangi W, Kiran V, Fontanesi C, Naaman R. 2015. The role of the electron spin polarization in water splitting. J. Phys. Chem. Lett. 6:4916–22
    [Google Scholar]
  41. 41.
    Mtangi W, Tassinari F, Vankayala K, Jentzsch AV, Adelizzi B et al. 2017. Control of electrons’ spin eliminates hydrogen peroxide formation during water splitting. J. Am. Chem. Soc. 139:2794–98
    [Google Scholar]
  42. 42.
    Murai H. 2003. Spin-chemical approach to photochemistry: reaction control by spin quantum operation. J. Photochem. Photobiol. C 3:183–201
    [Google Scholar]
  43. 43.
    Naaman R, Paltiel Y, Waldeck DH. 2019. Chiral molecules and the electron spin. Nat. Rev. Chem. 3:250–60
    [Google Scholar]
  44. 44.
    Naaman R, Paltiel Y, Waldeck DH. 2020. Chiral induced spin selectivity gives a new twist on spin-control in chemistry. Acc. Chem. Res. 53:2659–67
    [Google Scholar]
  45. 45.
    Naaman R, Paltiel Y, Waldeck DH. 2020. Chiral molecules and the spin selectivity effect. J. Phys. Chem. Lett. 11:93660–66
    [Google Scholar]
  46. 46.
    Naaman R, Paltiel Y, Waldeck DH. 2020. A perspective on chiral molecules and the spin selectivity effect. J. Phys. Chem. Lett. 11:3660–66
    [Google Scholar]
  47. 47.
    Naaman R, Waldeck DH. 2012. The chiral induced spin selectivity effect. J. Phys. Chem. Lett. 3:2178–87
    [Google Scholar]
  48. 48.
    Naaman R, Waldeck DH. 2015. Spintronics and chirality: spin selectivity in electron transport through chiral molecules. Annu. Rev. Phys. Chem. 66:263–81
    [Google Scholar]
  49. 49.
    Naaman R, Waldeck DH, Paltiel Y. 2019. Chiral molecules-ferromagnetic interfaces, an approach towards spin controlled interactions featured. Appl. Phys. Lett. 115:133701
    [Google Scholar]
  50. 50.
    Nabei Y, Hirobe D, Shimamoto Y, Shiota K, Inui A et al. 2020. Current-induced bulk magnetization of a chiral crystal CrNb3S6. Appl. Phys. Lett. 117:052408
    [Google Scholar]
  51. 51.
    Okada T, Wakayama NI, Wang L, Shingu H, Okano J-I, Ozawa T. 2003. The effect of magnetic field on the oxygen reduction reaction and its application in polymer electrolyte fuel cells. Electrochim. Acta 48:531–39
    [Google Scholar]
  52. 52.
    Ray K, Ananthavel SP, Waldeck DH, Naaman R. 1999. Aymmetric scattering of polarized electrons by organized organic films made of chiral molecules. Science 283:814–16
    [Google Scholar]
  53. 53.
    Sang Y, Mishra S, Tassinari F, Kumar KS, Carmieli R et al. 2021. Temperature dependence of charge and spin transfer in azurin. J. Phys. Chem. C 125:9875–83
    [Google Scholar]
  54. 54.
    Shi L, Dong HL, Reguera G, Beyenal H, Lu AH et al. 2016. Extracellular electron transfer mechanisms between microorganisms and minerals. Nat. Rev. Microbiol. 14:10651–62
    [Google Scholar]
  55. 55.
    Sontz PA, Mui TP, Fuss JO, Tainer JA, Barton JK. 2012. DNA charge transport as a first step in coordinating the detection of lesions by repair proteins. PNAS 109:61856–61
    [Google Scholar]
  56. 56.
    Stepanović S, Angelone D, Gruden M, Swart M 2017. The role of spin states in the catalytic mechanism of the intra- and extradiol cleavage of catechols by O2. Org. Biomol. Chem. 15:7860–68
    [Google Scholar]
  57. 57.
    Tassinari F, Steidel J, Paltiel S, Fontanesi C, Lahav M et al. 2019. Enantioseparation by crystallization using magnetic substrates. Chem. Sci. 10:5246–50
    [Google Scholar]
  58. 58.
    Valdiviezo J, Clever C, Beall E, Pearse A, Bae Y, Zhang P et al. 2021. Delocalization-assisted transport through nucleic acids in molecular junctions. Biochemistry 60:1368–78
    [Google Scholar]
  59. 59.
    Weibel ER, Taylor CR, Hoppeler H. 1991. The concept of symmorphosis: a testable hypothesis of structure-function relationship. PNAS 88:10357–61
    [Google Scholar]
  60. 60.
    Wilchek M, Bayer EA, Livnah O. 2006. Essentials of biorecognition: the (strept)avidinbiotin system as a model for protein-protein and protein-ligand interaction. Immunol. Lett. 103:127–32
    [Google Scholar]
  61. 61.
    Williams DH, Stephens E, O'Brien DP, Zhou M. 2004. Understanding noncovalent interactions: ligand binding energy and catalytic efficiency from ligand-induced reductions in motion within receptors and enzymes. Angew. Chem. Int. Ed. 43:6596–616
    [Google Scholar]
  62. 62.
    Xie Z, Markus TZ, Cohen SR, Vager Z, Gutierrez R, Naaman R. 2011. Spin specific electron conduction through DNA oligomers. Nano Lett 11:4652–55
    [Google Scholar]
  63. 63.
    Zeng Z, Zhang T, Liu Y, Zhang W, Yin Z et al. 2018. Magnetic field-enhanced 4-electron pathway for well-aligned Co3O4/electrospun carbon nanofibers in the oxygen reduction reaction. ChemSusChem 11:580–88
    [Google Scholar]
  64. 64.
    Ziv A, Saha A, Alpern H, Sukenik N, Baczewski LT et al. 2019. AFM-based spin exchange microscopy using chiral molecules. Adv. Mat. 31:1904206
    [Google Scholar]
  65. 65.
    Zwang TJ, Hürlimann S, Hill MG, Barton JK. 2016. Helix-dependent spin filtering through the DNA duplex. J. Am. Chem. Soc. 138:4815551–54
    [Google Scholar]
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