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RESEARCH ARTICLE

Oxidation products of α- and β-amyrins: potential tracers of abiotic degradation of vascular-plant organic matter in aquatic environments

M.-A. Galeron A , F. Vaultier A and J.-F. Rontani A B
+ Author Affiliations
- Author Affiliations

A Aix Marseille Université, Centre National de la Recherche Scientifique–Institut National des Sciences de l’Univers, Université de Toulon, Institut de la Recherche et du Développement, Mediterranean Institute of Oceanography (MIO) UM 110, F-13288 Marseille, France.

B Corresponding author. Email: jean-francois.rontani@mio.osupytheas.fr

Environmental Chemistry 13(4) 732-744 https://doi.org/10.1071/EN15237
Submitted: 9 September 2015  Accepted: 5 January 2016   Published: 29 February 2016

Environmental context. How can we know what happens to organic matter in aquatic environments? Although several compounds exist that can be used to trace the origin and state of organic matter, not many are sufficiently stable and specific to trace degradation processes, but α- and β-amyrins can fulfil that role. Such knowledge will help us better understand and better quantify carbon fluxes in riverine and marine environments.

Abstract. In order to fulfil the current need for stable and specific tracers to monitor vascular-plant organic matter degradation in aquatic environments, α-amyrin (urs-12-en-3β-ol) and β-amyrin (olean-12-en-3β-ol) were oxidised in vitro and their abiotic degradation products quantified in environmental samples from the Rhône River in France. Although they appear inert to photooxidation, they are clearly affected by autoxidation and the tracer potential of the resulting products was confirmed. Autoxidation of α- and β-amyrins produces urs or olean-12-en-3-one, 3β-hydroxy-urs or olean-12-en-11-one, urs or olean-12-en-3β,11α-diol and urs or olean-12-en-3,11-dione. 3β-Hydroxy-urs-12-en-11-one and 3β-hydroxy-olean-12-en-11-one, the main oxidation products detected, were selected as autoxidation tracers. These compounds, specific to autoxidation, were detected in dry leaves of Smilax aspera and in suspended particulate matter samples collected in the Rhône River and evidenced the importance of autoxidation in the degradation of organic matter of terrestrial origin.

Additional keywords: angiosperms, autoxidation, lipids, photo-oxidation, specific markers.


References

[1]  R. D. Pancost, C. S. Boot, The palaeoclimatic utility of terrestrial biomarkers in marine sediments. Mar. Chem. 2004, 92, 239.
The palaeoclimatic utility of terrestrial biomarkers in marine sediments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVChsL3J&md5=edc39237a4fe26df77bff00819779e65CAS |

[2]  A. Otto, C. Shunthirasingham, M. J. Simpson, A comparison of plant and microbial biomarkers in grassland soils from the Prairie Ecozone of Canada. Org. Geochem. 2005, 36, 425.
A comparison of plant and microbial biomarkers in grassland soils from the Prairie Ecozone of Canada.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFejurs%3D&md5=b4b79e5b8b6cbfb9e4f151222812359bCAS |

[3]  L. H. Vázquez, J. Palazon, A. Navarro-Ocaña, The pentacyclic triterpenes α-, β-amyrins: a review of sources and biological activities, in Phytochemicals – A Global Perspective of Their Role in Nutrition and Health (Ed. V. Rao) 2012, vol. 23, pp. 487–502 (InTech: Rijeka, Croatia).

[4]  B. R. T. Simoneit, Cyclic terpenoids of the geosphere, in Biological Markers in the Sedimentary Record (Ed. R. B. John), 1986, pp. 43–99 (Elsevier: Amsterdam).

[5]  H. L. ten Haven, J. Rullkötter, The diagenetic fate of taraxer-14-ene and oleanene isomers. Geochim. Cosmochim. Acta 1988, 52, 2543.
The diagenetic fate of taraxer-14-ene and oleanene isomers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXpvVaqtA%3D%3D&md5=a89f3869ab6bdf6cb1f1decfaa559e4cCAS |

[6]  J. W. De Leeuw, C. Largeau, A review of macromolecular organic compounds that comprise living organisms and their role in kerogen, coal, and petroleum formation, in Organic Geochemistry (Eds M. H. Engel, S. A. Macko) 1993, pp. 23–72 (Springer: New York).

[7]  S. G. Wakeham, E. A. Canuel, Degradation and preservation of organic matter in marine sediments, in Marine Organic Matter: Biomarkers, Isotopes and DNA (Ed J. K. Volkman) 2006, pp. 295–321 (Springer: Berlin).

[8]  J. E. Vonk, L. Sanchez-Garcia, I. P. Semiletov, O. V. Dudarev, T. I. Eglinton, A. Andersson, O. Gustafsson, Molecular and radiocarbon constraints on sources and degradation of terrestrial organic carbon along the Kolyma paleoriver transect, East Siberian Sea. Biogeosciences 2010, 7, 3153.
Molecular and radiocarbon constraints on sources and degradation of terrestrial organic carbon along the Kolyma paleoriver transect, East Siberian Sea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsF2ru7fJ&md5=dbd3030b0714e7dd42745f24b2ab031cCAS |

[9]  B. E. van Dongen, Z. Zencak, O. Gustafsson, Differential transport and degradation of bulk organic carbon and specific terrestrial biomarkers in the surface waters of a sub-Arctic brackish bay mixing zone. Mar. Chem. 2008, 112, 203.
Differential transport and degradation of bulk organic carbon and specific terrestrial biomarkers in the surface waters of a sub-Arctic brackish bay mixing zone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVentLbF&md5=15f5ad879e827e206ddeaeffaf85e4c9CAS |

[10]  S. Bourgeois, A. M. Pruski, M.-Y. Sun, R. Buscail, F. Lantoine, P. Kerhervé, G. Vétion, B. Rivière, F. Charles, Distribution and lability of land-derived organic matter in the surface sediments of the Rhône prodelta and the adjacent shelf (Mediterranean Sea, France): a multi proxy study. Biogeosciences 2011, 8, 3107.
Distribution and lability of land-derived organic matter in the surface sediments of the Rhône prodelta and the adjacent shelf (Mediterranean Sea, France): a multi proxy study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjsVGjsbo%3D&md5=12689dba4b57a8db6460ea52f61d34f3CAS |

[11]  J.-F. Rontani, B. Charrière, R. Sempéré, D. Doxaran, F. Vaultier, J. E. Vonk, J. K. Volkman, Degradation of sterols and terrigenous organic matter in waters of the Mackenzie Shelf, Canadian Arctic. Org. Geochem. 2014, 75, 61.
Degradation of sterols and terrigenous organic matter in waters of the Mackenzie Shelf, Canadian Arctic.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXht1Cgu7rK&md5=952e2887623267b4752d260109ad604bCAS |

[12]  M.-A. Galeron, R. Amiraux, B. Charriere, O. Radakovitch, P. Raimbault, N. Garcia, V. Lagadec, F. Vaultier, J.-F. Rontani, Seasonal survey of the composition and degradation state of particulate organic matter in the Rhône River using lipid tracers. Biogeosciences 2015, 12, 1431.
Seasonal survey of the composition and degradation state of particulate organic matter in the Rhône River using lipid tracers.Crossref | GoogleScholarGoogle Scholar |

[13]  J. L. Gellerman, W. H. Anderson, H. Schlenk, Synthesis and analysis of phytyl and phytenoyl wax esters. Lipids 1975, 10, 656.
Synthesis and analysis of phytyl and phytenoyl wax esters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XmtFKmuw%3D%3D&md5=1ddf8e802b062fcf1f6ac84ab695b166CAS | 1196015PubMed |

[14]  H. Seki, K. Ohyama, S. Sawai, M. Mizutani, T. Ohnishi, H. Sudo, T. Akashi, T. Aoki, K. Saito, T. Muranaka, Licorice β-amyrin 11-oxidase, a cytochrome P450 with a key role in the biosynthesis of the triterpene sweetener glycyrrhizin. Proc. Natl. Acad. Sci. USA 2008, 105, 14204.
Licorice β-amyrin 11-oxidase, a cytochrome P450 with a key role in the biosynthesis of the triterpene sweetener glycyrrhizin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFKjsbfL&md5=3384ee3eb88fd79c698e41bf14e17900CAS | 18779566PubMed |

[15]  C. Mathe, G. Culioli, P. Archier, C. Viellescazes, Characterization of archaeological frankincense by gas chromatography–mass spectrometry. J. Chromatogr. A 2004, 1023, 277.
Characterization of archaeological frankincense by gas chromatography–mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpsVSrs7g%3D&md5=ebcbdda317b6973df05bd2522f164ff2CAS | 14753694PubMed |

[16]  A. A. Matloub, M. A. Hamed, S. S. M. Al Souda, Chemo-protective effect on hepato-renal toxicity and cytotoxic activity of lipoidal matter of Atripex lindleyi MOQ. Int. J. Pharmacy Pharm. Sci. 2014, 6, 187.

[17]  N. A. Porter, S. E. Caldwell, K. A. Mills, Mechanisms of free-radical oxidation of unsaturated lipids. Lipids 1995, 30, 277.
Mechanisms of free-radical oxidation of unsaturated lipids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXltFCqtLc%3D&md5=39ecb1b586784f339f4ad937780d258aCAS | 7609594PubMed |

[18]  C. S. Foote, Photosensitized oxidation and singlet oxygen: consequences in biological systems, in Free Radicals in Biology (Ed. W.A. Pryor) 1976, vol. 2, pp. 85–133 (Academic Press: New York).

[19]  J. P. Knox, A. D. Dodge, Singlet oxygen and plants. Phytochemistry 1985, 24, 889.
Singlet oxygen and plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXktlCrsbo%3D&md5=9a492f4f6f7fbc760a037bb10cd2e620CAS |

[20]  J.-F. Rontani, P. Cuny, V. Grossi, Photodegradation of chlorophyll phytyl chain in senescent leaves of higher plants. Phytochemistry 1996, 42, 347.
Photodegradation of chlorophyll phytyl chain in senescent leaves of higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjtlWrtLk%3D&md5=5d987ee8196dc3aca8d4b6ee55ae7a9dCAS |

[21]  D. Marchand, J.-F. Rontani, Visible light-induced oxidation of lipid components of purple sulfur bacteria: a significant process in microbial mats. Org. Geochem. 2003, 34, 61.
Visible light-induced oxidation of lipid components of purple sulfur bacteria: a significant process in microbial mats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xpsl2qsLg%3D&md5=de236ab37724220663bea76c2ee34b23CAS |

[22]  J.-F. Rontani, Photo- and free-radical-mediated oxidation of lipid components during the senescence of phototrophic organisms, in Senescence 2012, pp. 3–31 (Intech Open Access Publishers, Rijeka, Croatia).

[23]  K. Suwa, T. Kimura, A. P. Schaap, Reactivity of singlet molecular oxygen with cholesterol in a phospholipid membrane matrix. A model for oxidative damage of membranes. Biochem. Biophys. Res. Commun. 1977, 75, 785.
Reactivity of singlet molecular oxygen with cholesterol in a phospholipid membrane matrix. A model for oxidative damage of membranes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2sXhs1Kku7w%3D&md5=0d4937ff9db4758957743f5eaf688760CAS | 577147PubMed |

[24]  E. N. Frankel, Methods to determine extent of oxidation, in Lipid Oxidation (Ed. E. N. Frankel) 1998, pp. 129–160 (The Oily Press: Glasgow, UK).

[25]  J.-F. Rontani, A. Rabourdin, D. Marchand, C. Aubert, Photochemical oxidation and autoxidation of chlorophyll phytyl side chain in senescent phytoplanktonic cells: potential sources of several acyclic isoprenoid compounds in the marine environment. Lipids 2003, 38, 241.
Photochemical oxidation and autoxidation of chlorophyll phytyl side chain in senescent phytoplanktonic cells: potential sources of several acyclic isoprenoid compounds in the marine environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjvFOrtb0%3D&md5=2f327da2e3d28bd16c51d5ee108b6cbfCAS | 12784864PubMed |

[26]  J. Pokorny, Major factors affecting the autoxidation of lipids, in Autoxidation of Unsaturated Lipids (Ed. H. W. S. Chan) 1987, pp. 141–206 (Academic Press: London).

[27]  K. M. Schaich, Metals and lipid oxidation: contemporary issues. Lipids 1992, 27, 209.
Metals and lipid oxidation: contemporary issues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xhs1ynsbo%3D&md5=da46066bbb2412e0272545aafc94bdaeCAS | 1522766PubMed |

[28]  J. Fossey, D. Lefort, J. Sorba, Free Radicals in Organic Chemistry 1995 (Wiley: Chichester, UK).

[29]  J.-F. Rontani, C. Aubert, S. T. Belt, EIMS fragmentation pathways and MRM quantification of 7α/β-hydroxy-dehydroabietic acid TMS derivatives. J. Am. Soc. Mass Spectrom. 2015, 26, 1606.
EIMS fragmentation pathways and MRM quantification of 7α/β-hydroxy-dehydroabietic acid TMS derivatives.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtFChtbjI&md5=e7b87881addb04f9b29d5f64e8d949fbCAS | 26138887PubMed |

[30]  K. M. Schaich, Lipid oxidation: theoretical aspects, in Bailey’s Industrial Oil and Fat Products 2005, pp. 269–355 (Wiley: New York).

[31]  A. W. Girotti, Lipid hydroperoxide generation, turnover, and effect or action in biological systems. J. Lipid Res. 1998, 39, 1529.
| 1:CAS:528:DyaK1cXlsVansb8%3D&md5=ec337d023e4162c573edd42258c6186eCAS | 9717713PubMed |

[32]  A. W. Girotti, Photosensitized oxidation of membrane lipids: reaction pathways, cytotoxic effects, and cytoprotective mechanisms. J. Photochem. Photobiol. B 2001, 63, 103.
Photosensitized oxidation of membrane lipids: reaction pathways, cytotoxic effects, and cytoprotective mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnvFGrtLg%3D&md5=6feb77b70bda89ea41d1589861366ba0CAS | 11684457PubMed |

[33]  A. A. Frimer, The reaction of singlet oxygen with olefins: the question of mechanism. Chem. Rev. 1979, 79, 359.
The reaction of singlet oxygen with olefins: the question of mechanism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXmtFSns78%3D&md5=6bdbda2b850eb18f88938f5252e3d1ceCAS |

[34]  A. A. Frimer, Singlet oxygen in peroxide chemistry, in Peroxides (Ed. S. Patai) 1983, pp. 201–234 (Wiley: New York).

[35]  J.-F. Rontani, S. T. Belt, F. Vaultier, T. A. Brown, G. Massé, Autoxidative and photooxidative reactivity of highly branched isoprenoid (HBI) alkenes. Lipids 2014, 49, 481.
Autoxidative and photooxidative reactivity of highly branched isoprenoid (HBI) alkenes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjs1Kqt7w%3D&md5=d905a16b00578a7c94d84444c7d359bfCAS | 24604601PubMed |

[36]  W. Korytowski, G. J. Bachowski, A. W. Girotti, Photoperoxidation of cholesterol in homogeneous solution, isolated membranes, and cells: comparison of the 5α- and 6β-hydroperoxides as indicators of singlet oxygen intermediacy. Photochem. Photobiol. 1992, 56, 1.
Photoperoxidation of cholesterol in homogeneous solution, isolated membranes, and cells: comparison of the 5α- and 6β-hydroperoxides as indicators of singlet oxygen intermediacy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38Xlt1Ontrk%3D&md5=be81b09f25a05331ffc92ab27d9bba73CAS | 1508976PubMed |

[37]  J.-F. Rontani, P. Cuny, C. Aubert, Rates and mechanism of light-dependent degradation of sterols in senescent cells of phytoplankton. J. Photochem. Photobiol. Chem. 1997, 111, 139.
Rates and mechanism of light-dependent degradation of sterols in senescent cells of phytoplankton.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXnvFSmsrw%3D&md5=f594edd2809e485738755c2842dafbd6CAS |

[38]  H. Yin, L. Xu, N. A. Porter, Free-radical lipid peroxidation: mechanisms and analysis. Chem. Rev. 2011, 111, 5944.
Free-radical lipid peroxidation: mechanisms and analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVOnsrvM&md5=4af656c7a3eb02879e87ae461a5d0932CAS | 21861450PubMed |

[39]  M. Stratakis, M. Orfanopoulos, Regioselectivity in the ene reaction of singlet oxygen with alkenes. Tetrahedron 2000, 56, 1595.
Regioselectivity in the ene reaction of singlet oxygen with alkenes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXit1emtLs%3D&md5=7cf31166255592f211a5b2854be38a3dCAS |

[40]  L. L. Smith, Other oxidations, in Cholesterol Autoxidation 1981, pp. 243–295 (Springer: New York).

[41]  B. P. Koch, J. Harder, R. J. Lara, G. Kattner, The effect of selective microbial degradation on the composition of mangrove-derived pentacyclic triterpenols in surface sediments. Org. Geochem. 2005, 36, 273.
The effect of selective microbial degradation on the composition of mangrove-derived pentacyclic triterpenols in surface sediments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXisFOlsA%3D%3D&md5=576b89508b1f788ac477b0336569e2bfCAS |

[42]  I. Wahlberg, K. Karlsson, C. R. Enzell, Non-volatile constituents of deertongue leaf. Acta Chem. Scand. 1972, 26, 1383.
Non-volatile constituents of deertongue leaf.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE38XkvVyks7w%3D&md5=dfc8d11e1afe332c3e37302d6edd5c0bCAS |

[43]  M.-A. Galeron, J. K. Volkman, J.-F. Rontani, Oxidation products of betulin: new tracers of biotic and abiotic degradation of higher-plant material in the environment. Org. Geochem. 2016, 91, 31.
Oxidation products of betulin: new tracers of biotic and abiotic degradation of higher-plant material in the environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhslyksLfO&md5=585b5fb0ee04c9211243cf0c88ea99b9CAS |

[44]  J. K. Volkman, A review of sterol markers for marine and terrigenous organic matter. Org. Geochem. 1986, 9, 83.
A review of sterol markers for marine and terrigenous organic matter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XitFalu7c%3D&md5=2744784f15cc88254fe3d7ace7f5d042CAS |

[45]  J. K. Volkman, Sterols in microorganisms. Appl. Microbiol. Biotechnol. 2003, 60, 495.
Sterols in microorganisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjvFGnsA%3D%3D&md5=6411d2a8341d47203cbd98025e6b7ce2CAS | 12536248PubMed |

[46]  W. Chaiyasit, R. J. Elias, D. J. McClements, E. A. Decker, Role of physical structures in bulk oils on lipid oxidation. Crit. Rev. Food Sci. Nutr. 2007, 47, 299.
Role of physical structures in bulk oils on lipid oxidation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkvFegt70%3D&md5=9cb3d4e68400066a988d169b21c2b290CAS | 17453926PubMed |

[47]  C. S. Foote, J. Valentine, A. Greenberg, J. F. Liebman, Active Oxygen in Chemistry 1995 (Chapman & Hall: New York).