Skip to main content
SpringerLink
Log in

Alternatives to the ‘water oxidation pathway’ of biological ozone formation

  • Opinion Paper
  • Published:
Journal of Chemical Biology

Abstract

Recent studies have shown that ozone (O3) is endogenously generated in living tissues, where it makes both positive and negative physiological contributions. A pathway for the formation of both O3 and hydrogen peroxide (H2O2) was previously proposed, beginning with the antibody or amino acid-catalyzed oxidation of water by singlet oxygen (1O2) to form hydrogen trioxide (H2O3) as a key intermediate. A key pillar of this hypothesis is that some of the H2O2 molecules incorporate water-derived oxygen atoms. However, H2O3 decomposes extremely readily in water to form 1O2 and water, rather than O3 and H2O2. This article highlights key literature indicating that the oxidation of organic molecules such as the amino acids methionine, tryptophan, histidine, and cysteine by 1O2 is involved in ozone formation. Based on this, an alternative hypothesis for ozone formation is developed involving a further reaction of singlet oxygen with various oxidized organic intermediates. H2O2 having water-derived oxygen atoms is subsequently formed during ozone decomposition in water by known reactions.

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

Similar content being viewed by others

References

  1. Balla J, Tyihak E (2010) Direct measurement of emission of endogenous ozone from plants by GC-MS-SIM. Chromatographia Supp 71:S87–S91

    Article  CAS  Google Scholar 

  2. Tyihak E, Moricz AM, Ott PG (2012) BioArena studies: unique function of endogenous formaldehyde and ozone in the antibiotic effect—a review. Med Chem 8:75–84

    Article  CAS  Google Scholar 

  3. Beltran FJ (2004) Ozone reaction kinetics for water and wastewater systems. CRC Press, pp 13–14

  4. Wentworth P Jr, McDunn JE, Wentworth AD, Takeuchi C, Nieva J, Jones T, Bautista C, Ruedi JM, Gutierrez A, Janda KD, Babior BM, Eschenmoser A, Lerner RA (2002) Evidence for antibody-catalyzed ozone formation in bacterial killing and inflammation. Science 298:2195–2199

    Article  CAS  Google Scholar 

  5. Pereira PMR (2015) Antibodies armed with photosensitizers: from chemical synthesis to photobiological applications. Org Biomol Chem. doi:10.1039/C4OB02334

    Google Scholar 

  6. Wentworth P Jr, Nieva J, Takeuchi C, Galve R, Wentworth AD, Dilley RB, DeLaria GA, Saven A, Babior BM, Janda KD, Eschenmoser A, Lerner RA (2003) Evidence for ozone formation in human atherosclerotic arteries. Science 302:1053–1056

    Article  CAS  Google Scholar 

  7. Wentworth AD, Song B-D, Nieva J, Shafton A, Sangeetha T, Wentworth P Jr (2009) The ratio of cholesterol 5,6 secosterols formed from ozone and singlet oxygen offers insight into the oxidation of cholesterol in vivo. Chem Comm (Camb) 3098-3100

  8. Kettle AJ, Clark BM, Winterbourn CC (2004) Superoxide converts indigo carmine to isatin sulfonic acid: implications for the hypothesis that neutrophils produce ozone. J Biol Chem 279:18521–18525

    Article  CAS  Google Scholar 

  9. Brinkhorst J, Nara SJ, Pratt DA (2008) Hock cleavage of cholesterol-5α-hydroperoxide: an ozone-free pathway to the cholesterol ozonolysis products identified in arterial plague and brain tissue. J Am Chem Soc 130:12224–12225

    Article  CAS  Google Scholar 

  10. Tomono S, Miyoshi N, Shiokawa H, Iwabuchi T, Aratani Y, Higashi T, Nukaya H, Ohshima H (2011) Formation of cholesterol ozonolysis products in vitro and in vivo through a myeloperoxidase-dependent pathway. J Lipid Res 52:87–97

    Article  CAS  Google Scholar 

  11. Miyoshi N, Iuliano L, Tomono S, Ohshima H (2014) Implications of cholesterol autoxidation products in the pathogenesis of inflammatory diseases. Biochem Biophys Res Comm 446:702–708

    Article  Google Scholar 

  12. Tyihak E, Moricz AM, Ott PG, Katay G, Mincsovics E (2012) Biological characterization of ingredients in OPLC-BioArena-greenhouse-system: unique reactions of endogenous HCHO and O3 in in vitro and in vivo conditions. Chromatographia 75:983–990

    Article  CAS  Google Scholar 

  13. Tyihak E, Moricz AM, Ott PG, Kiraly-Veghely Z, Katay G (2013) BioArena system for knowing and understanding the biological world: a review with new experimental results. J AOAC Int 96:1189–1199

    Article  CAS  Google Scholar 

  14. Wentworth P Jr, Jones LH, Wentworth AD, Zhu X, Larsen NA, Wilson IA, Xu X, Goddard WA III, Janda KD, Eschenmoser A, Lerner RA (2001) Antibody catalysis of the oxidation of water. Science 293:1806–1811

    Article  CAS  Google Scholar 

  15. Xu X, Muller RP, Goddard WA III (2002) The gas phase reaction of singlet dioxygen with water: a water-catalyzed mechanism. Proc Natl Acad Sci U S A 99:3376–3381

    Article  CAS  Google Scholar 

  16. Cerkovnic J, Plesnicar B (2013) Recent advances in the chemistry of hydrogen trioxide (HOOOH). Chem Rev 113:7930–7951

    Article  Google Scholar 

  17. Yamashita K, Miyoshi T, Arai T, Endo N, Itoh H, Makino K, Mizugishi K, Uchiyama T, Masataka S (2008) Ozone production by amino acids contributes to killing of bacteria. Proc Natl Acad Sci U S A 105:16912–16917

    Article  CAS  Google Scholar 

  18. Wei C, Song B, Yuan J, Feng Z, Jia G, Li C (2007) Luminescence and Raman spectroscopic studies on the damage of tryptophan, histidine and carnosine by singlet oxygen. J Photochem Photobiol A Chem 189:39–45

    Article  CAS  Google Scholar 

  19. Pattison DI, Rahmanto AS, Davies MJ (2012) Photo-oxidation of proteins. Photochem Photobiol Sci 11:38–53

    Article  CAS  Google Scholar 

  20. Jensen RL, Arnbjerg J, Ogilby R (2012) Reaction of singlet oxygen with tryptophan in proteins: a pronounced effect of the local environment on the reaction rate. J Am Chem Soc 134:9820–9826

    Article  CAS  Google Scholar 

  21. Lundeen RA, McNeill K (2013) Reactivity differences of combined and free amino acids: quantifying the relationship between three-dimensional protein structure and singlet oxygen reaction rates. Environ Sci Technol 47:14215–14223

    Article  CAS  Google Scholar 

  22. Zhu X, Wentworth P Jr, Wentworth AD, Eschenmoser A, Lerner RA, Wilson IA (2004) Probing the antibody-catalyzed water-oxidation pathway at atomic resolution. Proc Natl Acad Sci U S A 101:2247–2252

    Article  CAS  Google Scholar 

  23. Sreethara A, Lau K, Hosken B, Macchi F, Zhan D, Shen A, Steinmann D, Schoneich C, Lentz Y (2013) Role of surface exposed tryptophan as substrate generators for the antibody catalyzed water oxidation pathway. Mol Pharm 10:278–288

    Article  Google Scholar 

  24. Khor HK, Jacoby ME, Squler TC, Chu GC, Chelius D (2010) Identification of methionine sulfoxide diastereomers in immunoglobin gamma antibodies using methionine sulfoxide reductase enzymes. mAbs 2:299–308

    Article  Google Scholar 

  25. Amano M, Kobayashi N, Yabuta M, Uchiyama S, Fukui K (2014) Detection of histidine oxidation in a monoclonal immunoglobulin gamma (IgG) 1 antibody. Anal Chem 86:7536–7543

    Article  CAS  Google Scholar 

  26. Liu M, Zhang Z, Cheetham J, Ren D, Zhou ZS (2014) Discovery and characterization of a photo-oxidative histidine-histidine cross-link in IgG1 antibody utilizing 18O-labeling and mass spectrometry. Anal Chem 86:4940–4948

    Article  CAS  Google Scholar 

  27. Liu F, Lu W, Fang Y, Liu J (2014) Evolution of oxidation dynamics of histidine: nonreactivity in the gas phase, peroxides in hydrated clusters, and pH dependence in solution. Phys Chem Chem Phys 16:22179–22191

    Article  CAS  Google Scholar 

  28. Kim J, Rodriquez ME, Guo M, Kenney ME, Oleinic NL, Anderson VE (2008) Oxidative modification of cytochrome c by singlet oxygen. Free Radic Biol Med 44:1700–1711

    Article  CAS  Google Scholar 

  29. Kasson TMD, Rexroth S, Barry BA (2012) Light-induced oxidative stress, N-formylkynurenine, and oxygenic photosynthesis. PLoS ONE 7:e42220

    Article  CAS  Google Scholar 

  30. Rehman AU, Cser K, Sass L, Vass I (2013) Characterization of singlet oxygen production and its involvement in photochemical damage of photosystem II in the cyanobacterium Cynechocystis PCC 6803 by histidine-mediated chemical trapping. Biochim Biophys Acta 1827:689–698

    Article  CAS  Google Scholar 

  31. Ronsein GE, de Oliveira MCB, de Medeiros MHG, Mascio PD (2009) Characterization of 1O2-derived oxidation products of tryptophan: a combination of tandem mass spectrometry analyses and isotopic labeling studies. J Am Soc Mass Spectrom 20:188–197

    Article  CAS  Google Scholar 

  32. Ronsein GE, de Oliveira MCB, de Medeiros MHG, Mascio PD (2011) Mechanism of dioxindolylalanine formation by singlet molecular oxygen-mediated oxidation of tryptophan residues. Photochem Photobiol Sci 10:1727–1730

    Article  CAS  Google Scholar 

  33. Kobayakawa H, Imai K (2011) Effects of the interaction between ozone and carbon dioxide on gas exchange, photosystem II and antioxidants in rice leaves. Photosynthetica 49:227–238

    Article  CAS  Google Scholar 

  34. Liu L, Flatoy F, Ordonez C, Braathen GO, Hak C, Junkermann W, Andreani-Aksoyoglu S, Mellqvist J, Galle B, Prevot ASH, Isaksen ISA (2007) Photochemical modelling in the Po basin with focus on formaldehyde and ozone. Atmos Chem Phys 7:121–137

    Article  CAS  Google Scholar 

  35. Hajimohammadi M, Safari N, Mofakham H, Shaabani A (2010) A new and efficient aerobic oxidation of aldehydes to carboxylic acids with singlet oxygen in the presence of porphyrin sensitizers and visible light. Tetrahedron Lett 51:4061–4065

    Article  CAS  Google Scholar 

  36. Fang Y, Liu F, Bennet A, Ara S, Liu J (2011) Experimental and trajectory study on the reaction of protonated methionine with electronically excited singlet molecular oxygen (a1Δg): reaction dynamics and collision energy effects. Phys Chem B 115:2671–2682

    Article  CAS  Google Scholar 

  37. Kanofsky JR, Sima P (1991) Singlet oxygen production from the reactions of ozone with biological molecules. J Biol Chem 266:9039–9042

    CAS  Google Scholar 

  38. Munoz F, Mvula E, Braslavsky SE, von Sonntag C (2001) Singlet dioxygen formation in ozone reactions in aqueous solution. J Chem Soc Perkin Trans 2:1109–1116

    Article  Google Scholar 

  39. Vahedpour M, Baghary R, Khalili F (2013) Prediction of mechanism and thermochemical properties of O3 + H2S atmospheric reaction. J. Chem. Article ID 65968 http://dx.doi.org/10.1155/2013/659682

  40. Ghesquere B, Jonckheere V, Colaert N, van Durme J, Timmerman E, Goethals M, Schymkowitz J, Rousseau F, Vanderkerckhove J, Gevaert K (2011) Redox proteomics of protein-bound methionine oxidation. Mol Cell Proteomics 10:M110.006866, http://mcponline.org/content/10/5.toc

    Article  Google Scholar 

  41. Lim JC, You Z, Kim G, Levine RL (2011) Methionine sulfoxide reductase A is a stereospecific methionine oxidase. Proc Natl Acad Sci U S A 108:10472–10477

    Article  CAS  Google Scholar 

  42. Glaze WH, Kang J-W, Chapin DH (1987) The chemistry of water treatment processes involving ozone, hydrogen peroxide and ultraviolet radiation. Ozone Sci Eng 9:335–352

    Article  CAS  Google Scholar 

  43. Sharma VK, Graham NJD (2010) Oxidation of amino acids, peptides and proteins by ozone: a review. Ozone Sci Eng 32:81–90

    Article  CAS  Google Scholar 

  44. Merenyi G, Lind J, Sonntag C (2010) Reaction of ozone with hydrogen peroxide (peroxone process): a revision of current mechanistic concepts based on thermokinetic and quantum-chemical considerations. Environ Sci Technol 44:3505–3507

    Article  CAS  Google Scholar 

  45. Codorniu-Hernandez E, Kusalik PG (2012) Mobility mechanism of hydroxyl radicals in aqueous solution via hydrogen transfer. J Am Chem Soc 134:532–538

    Article  CAS  Google Scholar 

  46. Codorniu-Hernandez E, Hall KW, Ziemianowicz D, Carpendale S, Kusalik PG (2014) Aqueous production of oxygen atoms from hydroxyl radicals. Phys Chem Chem Phys 16:26094–26102

    Article  CAS  Google Scholar 

  47. Staehelin J, Buhler RE, Hoigne J (1984) Ozone decomposition in water studied by pulse radiolysis. 2. HO and HO4 as chain intermediates. J Phys Chem 88:5999–6004

    Article  CAS  Google Scholar 

  48. Tomono S, Miyoshi N, Sato K, Ohba Y, Ohshima H (2009) Formation of cholesterol ozonolysis products through an ozone-free mechanism mediated by myeloperoxidase-H2O-chloride system. Biochem Biophys Res Comm 383:222–227

    Article  CAS  Google Scholar 

  49. Otsu K, Sato K, Sato M, Ono H, Ohba Y, Katagata Y (2008) Impaired activation of caspase cascade during cell death induced by newly synthesized singlet oxygen generator, 1-buthylnaphthalene-4-propionate-endoperoxide. Cell Biol Int 32:1380–1387

    Article  CAS  Google Scholar 

  50. Lell B, Viebahn R, Kremsner PG (2001) The activity of ozone against Plasmodium falciparum. Ozone Sci Eng 23:89–93

    Article  CAS  Google Scholar 

  51. Verma P, Biswas S, Mohan T, Ali S, Rao DN (2013) Detection of histidine-rich protein and lactate dehydrogenase of Plasmodium falciparum in malaria patients by sandwich ELISA using in-house reagents. Indian J Med Res 138:977–987

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Food Science and Technology, Jomo Kenyatta University of Agriculture and Technology, P. O. Box 62000, 00200, Nairobi, Kenya

    Arnold N. Onyango

Authors
  1. Arnold N. Onyango
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Arnold N. Onyango.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Onyango, A.N. Alternatives to the ‘water oxidation pathway’ of biological ozone formation. J Chem Biol 9, 1–8 (2016). https://doi.org/10.1007/s12154-015-0140-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12154-015-0140-6

Keywords

Search

Navigation