Stability of bacterial carotenoids in the presence of iron in a model of the gastric compartment - Comparison with dietary reference carotenoids

Charlotte Sy; Olivier Dangles; Patrick Borel; Catherine Caris-Veyrat

doi:10.1016/j.abb.2014.12.030

Stability of bacterial carotenoids in the presence of iron in a model of the gastric compartment - Comparison with dietary reference carotenoids

Charlotte Sy
, Olivier Dangles
, Patrick Borel
, Catherine Caris-Veyrat^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

22 Scopus citations

Abstract

Recently isolated spore-forming pigmented marine bacteria, Bacillus indicus HU36 and Bacillus firmus GB1 are sources of carotenoids (∼fifteen distinct yellow and orange pigments and ∼thirteen distinct pink pigments, respectively). They are glycosides of oxygenated lycopene derivatives (apo-lycopenoids) and are assumed to be more heat- and gastric-stable than common carotenoids. In this study, the oxidation by O₂ of the bacterial carotenoids was initiated by free iron (Fe^II and Fe^III) or by heme iron (metmyoglobin) in a mildly acidic aqueous solution mimicking the gastro-intestinal compartment and compared to the oxidation of the common dietary carotenoids β-carotene, lycopene and astaxanthin. Under these conditions, all bacterial carotenoids appear more stable in the presence of heme iron vs. free iron. Carotenoid autoxidation initiated by Fe^II is relatively fast and likely involves reactive oxygen-iron species derived from Fe^II and O₂. By contrast, the corresponding reaction with Fe^III is kinetically blocked by the slow preliminary reduction of Fe^III into Fe^II by the carotenoids. The stability of carotenoids toward autoxidation increases as follows: β-carotene < lycopene < astaxanthin < HU36 and GB1. In particular, bacterial carotenoids react more quickly than reference carotenoids with Fe^III, but much more slowly than the reference carotenoids with Fe^II. This reaction is correlated with the structure of the carotenoids, which can have opposite effects in a micellar system: bacterial carotenoids with electro-attracting terminal groups have a lower reducing capacity than β-carotene and lycopene. However, their polar head favours their location close to the interface of micelles, in closer contact with oxidative species. Kinetic analyses of the iron-induced autoxidation of astaxanthin and HU36 carotenoids has been performed and gives insights in the underlying mechanisms.

Original language	English
Pages (from-to)	89-100
Number of pages	12
Journal	Archives of Biochemistry and Biophysics
Volume	572
DOIs	https://doi.org/10.1016/j.abb.2014.12.030
State	Published - 15 Apr 2015
Externally published	Yes

Bibliographical note

Publisher Copyright:
© 2015 Elsevier Inc.

Funding

This work was supported by a grant from the European Community’s Seventh Framework Program (Colorspore, No. 207948, “New sources of natural, gastric stable, food additives, colorants and novel functional foods”, which was a small collaborative project coordinated by Simon Cutting, Royal Holloway University of London, within the work program topic “(Bio)Technologies for the production of food additives, and flavours (KBBE-2007-2-3-03)”). This publication reflects only the authors’ view. The Colorspore community is not liable for any use that may be made of the results. Special thanks are given to Paul Fraser, Laura Perez-Fons and Reena Khaneja (Royal Holloway University of London, UK) for providing carotenoid-rich bacterial extracts. We thank the company Conesa (Conservas Vegetales de Extremadura, Badajoz, Spain) for its gift of (all- E )-lycopene. We also thank Michel Carail (INRA) for his technical assistance with the UPLC-DAD–MS analysis, Christian Ginies (INRA) for his help with the GC–MS analysis and Rachel Kopec for the critical reading of the manuscript.

Funders	Funder number
European Community’s Seventh Framework Program	207948, KBBE-2007-2-3-03

Keywords

Astaxanthin
Carotenoids from bacteria
Degradation
Gastric model
Lycopene
Metmyoglobin
Oxidation
Transition metal
β-Carotene

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title = "Stability of bacterial carotenoids in the presence of iron in a model of the gastric compartment - Comparison with dietary reference carotenoids",

abstract = "Recently isolated spore-forming pigmented marine bacteria, Bacillus indicus HU36 and Bacillus firmus GB1 are sources of carotenoids (∼fifteen distinct yellow and orange pigments and ∼thirteen distinct pink pigments, respectively). They are glycosides of oxygenated lycopene derivatives (apo-lycopenoids) and are assumed to be more heat- and gastric-stable than common carotenoids. In this study, the oxidation by O2 of the bacterial carotenoids was initiated by free iron (FeII and FeIII) or by heme iron (metmyoglobin) in a mildly acidic aqueous solution mimicking the gastro-intestinal compartment and compared to the oxidation of the common dietary carotenoids β-carotene, lycopene and astaxanthin. Under these conditions, all bacterial carotenoids appear more stable in the presence of heme iron vs. free iron. Carotenoid autoxidation initiated by FeII is relatively fast and likely involves reactive oxygen-iron species derived from FeII and O2. By contrast, the corresponding reaction with FeIII is kinetically blocked by the slow preliminary reduction of FeIII into FeII by the carotenoids. The stability of carotenoids toward autoxidation increases as follows: β-carotene < lycopene < astaxanthin < HU36 and GB1. In particular, bacterial carotenoids react more quickly than reference carotenoids with FeIII, but much more slowly than the reference carotenoids with FeII. This reaction is correlated with the structure of the carotenoids, which can have opposite effects in a micellar system: bacterial carotenoids with electro-attracting terminal groups have a lower reducing capacity than β-carotene and lycopene. However, their polar head favours their location close to the interface of micelles, in closer contact with oxidative species. Kinetic analyses of the iron-induced autoxidation of astaxanthin and HU36 carotenoids has been performed and gives insights in the underlying mechanisms.",

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author = "Charlotte Sy and Olivier Dangles and Patrick Borel and Catherine Caris-Veyrat",

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T1 - Stability of bacterial carotenoids in the presence of iron in a model of the gastric compartment - Comparison with dietary reference carotenoids

AU - Sy, Charlotte

AU - Dangles, Olivier

AU - Borel, Patrick

AU - Caris-Veyrat, Catherine

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AB - Recently isolated spore-forming pigmented marine bacteria, Bacillus indicus HU36 and Bacillus firmus GB1 are sources of carotenoids (∼fifteen distinct yellow and orange pigments and ∼thirteen distinct pink pigments, respectively). They are glycosides of oxygenated lycopene derivatives (apo-lycopenoids) and are assumed to be more heat- and gastric-stable than common carotenoids. In this study, the oxidation by O2 of the bacterial carotenoids was initiated by free iron (FeII and FeIII) or by heme iron (metmyoglobin) in a mildly acidic aqueous solution mimicking the gastro-intestinal compartment and compared to the oxidation of the common dietary carotenoids β-carotene, lycopene and astaxanthin. Under these conditions, all bacterial carotenoids appear more stable in the presence of heme iron vs. free iron. Carotenoid autoxidation initiated by FeII is relatively fast and likely involves reactive oxygen-iron species derived from FeII and O2. By contrast, the corresponding reaction with FeIII is kinetically blocked by the slow preliminary reduction of FeIII into FeII by the carotenoids. The stability of carotenoids toward autoxidation increases as follows: β-carotene < lycopene < astaxanthin < HU36 and GB1. In particular, bacterial carotenoids react more quickly than reference carotenoids with FeIII, but much more slowly than the reference carotenoids with FeII. This reaction is correlated with the structure of the carotenoids, which can have opposite effects in a micellar system: bacterial carotenoids with electro-attracting terminal groups have a lower reducing capacity than β-carotene and lycopene. However, their polar head favours their location close to the interface of micelles, in closer contact with oxidative species. Kinetic analyses of the iron-induced autoxidation of astaxanthin and HU36 carotenoids has been performed and gives insights in the underlying mechanisms.

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KW - Degradation

KW - Gastric model

KW - Lycopene

KW - Metmyoglobin

KW - Oxidation

KW - Transition metal

KW - β-Carotene

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AN - SCOPUS:84932098484

SN - 0003-9861

VL - 572

SP - 89

EP - 100

JO - Archives of Biochemistry and Biophysics

JF - Archives of Biochemistry and Biophysics

ER -

Stability of bacterial carotenoids in the presence of iron in a model of the gastric compartment - Comparison with dietary reference carotenoids

Abstract

Bibliographical note

Funding

Keywords

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