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BMC Complementary Medicine and Therapies
Published in: BMC Complementary Medicine and Therapies 1/2013

Open Access 01-12-2013 | Research article

Biological properties of carotenoids extracted from Halobacterium halobium isolated from a Tunisian solar saltern

Authors: Molka Abbes, Houda Baati, Sonda Guermazi, Concetta Messina, Andrea Santulli, Neji Gharsallah, Emna Ammar

Published in: BMC Complementary Medicine and Therapies | Issue 1/2013

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Abstract

Background

Bioactive molecules have received increasing attention due to their nutraceutical attributes and anticancer, antioxidant, antiproliferative and apoptosis-inducing properties. This study aimed to investigate the biological properties of carotenoids extracted from Archaea.

Methods

Halophilic Archaea strains were isolated from the brine of a local crystallizer pond (TS7) of a solar saltern at Sfax, Tunisia. The most carotenoid-producing strain (M8) was investigated on heptoma cell line (HepG2), and its viability was assessed by the MTT-test. The cells were incubated with different sub-lethal extract rates, with carotenoid concentrations ranging from 0.2 to 1.5 μM. Antioxidant activity was evaluated through exposing the cells to sub-lethal extract concentrations for 24 hours and then to oxidative stress induced by 60 μM arachidonic acid and 50 μM H2O2.

Results

Compared to non-treated cells, bacterial carotenoid extracts inhibited HepG2 cell viability (50%). A time and dose effect was observed, with cell viability undergoing a significant (P < 0.05) decrease with extract concentration. After exposure to oxidative stress, control cells underwent a significant (P < 0.05) decrease in viability as compared to the non-treated cells.

Conclusions

The bacterial extracts under investigation were noted to exhibit the strongest free radical scavenging activity with high carotenoid concentrations. The carotenoid extract also showed significant antiproliferative activity against HepG2 human cancer cell lines.
Appendix
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Literature
1.
Chattopadhyay P, Chatterjee S, Sen SK: Biotechnological potential of natural food grade biocolorants. Review, African J Biotechnol. 2008, 7: 2972-2985.
2.
Fernández-García E, Carvajal-Lérida I, Jarén-Galán M, Garrido-Fernández J, Pérez-Gálvez A, Hornero-Méndez D: Carotenoids bioavailability from foods: From plantpigments to efficient biological activities. Food Res Int. 2012, 46: 438-450. 10.1016/j.foodres.2011.06.007.CrossRef
3.
Boeuf G: Marine biodiversity characteristics. C R Biol. 2011, 334: 435-440. 10.1016/j.crvi.2011.02.009.CrossRefPubMed
4.
Benlloch S, Acinas SG, Anto’n J, Lopez L, Rodriguez-Valera F: Archaeal biodiversityin crystallizer ponds from a solar saltern: culture versus PCR. Microb Ecol. 2001, 41: 12-19.PubMed
5.
Ovreas L, Daae FL, Torsvik V, Rodriguez-Valera F: Characterization of microbial diversity in hypersaline environments by melting profiles and reassociation kinetics in combination with terminal restriction fragment length polymorphism (T-RFLP). Microb Ecol. 2003, 46: 291-301. 10.1007/s00248-003-3006-3.CrossRefPubMed
6.
7.
Baati H, Guermazi S, Amdouni R, Gharsallah N, Sghir A, Ammar E: Prokaryotic diversity of a Tunisian multipond solar saltern. Extremophiles. 2008, 12: 505-518. 10.1007/s00792-008-0154-x.CrossRefPubMed
8.
Baati H, Amdouni R, Gharsallah N, Sghir A, Ammar E: Isolation and characterization of moderately halophilic bacteria from Tunisian Solar saltern. Curr Microbiol. 2010, 60: 157-161. 10.1007/s00284-009-9516-6.CrossRefPubMed
9.
Oren A, Trüper HG: Anaerobic growth of halophilic archaeobacteria by reduction of dimethylsulfoxide and trimethylamine N-oxide. FEMS Microbiol Lett. 1990, 70: 33-36. 10.1111/j.1574-6968.1990.tb03772.x.CrossRef
10.
Bergey's Manual of Systematic Bacteriology. Edited by: Garrity GM, Boone DR, Castenholz RW. 2001, Baltimore: Williams & Wilkins, 261-264. 2
11.
Lu Y, Etoh H, Watanabe N, Ina K, Ukai N, Oshima S, Ojima F, Sakamoto H, Ishiguro Y: A new carotenoid, hydrogen peroxide oxidation products from lycopene. Biosci Biotech Bioch. 1995, 59: 2153-2155. 10.1271/bbb.59.2153.CrossRef
12.
Elliot R: Mechanisms of genomic and non-genomic action of carotenoids. Biochem Bioph Acta. 2005, 1740: 147-154. 10.1016/j.bbadis.2004.12.009.
13.
Rodriguez-Amaya DB: A Guide to Carotenoid Analysis in Foods. 2001, Washington: ILSI (International Life Sciences Institute) Press, 14-22.
14.
Saito T, Miyabe Y, Ide H, Yamamoto O: Hydroxyl radical scavenging ability of bacterioruberin. Radiat Phys Chem. 1997, 50: 267-269. 10.1016/S0969-806X(97)00036-4.CrossRef
15.
Mandelli F, Miranda VS, Rodrigues E, Mercadante AZ: Identification of carotenoids with high antioxidant capacity produced by extremophile microorganisms. World J Microbiol Biotechnol. 2012, 28: 1781-1790. 10.1007/s11274-011-0993-y.CrossRefPubMed
16.
Shahmohammadi HR, Asgarani E, Terato H, Saito T, Ohyama Y, Gekko K, Yamamoto O, Ide H: Protective roles of bacterioruberin and intracellular KCl in the resistance of Halobacterium salinarium against DNA-damaging agents. J Radiat Res. 1998, 39: 251-262. 10.1269/jrr.39.251.CrossRefPubMed
17.
Strand A, Shivaji S, LiaaenJensen S: Bacterial carotenoids, C-50-carotenoids, revised structures of carotenoids associated with membranes in psychrotrophic Micrococcus roseus. Biochem Syst Ecol. 1997, 25: 547-552. 10.1016/S0305-1978(97)00039-2.CrossRef
18.
Fong NJC, Burgess ML, Barrow KD, Glenn DR: Carotenoid accumulation in the psychrotrophic bacterium Arthrobacter agilis in response to thermal and salt stress. Appl Microbio Biot. 2001, 56: 750-756. 10.1007/s002530100739.CrossRef
19.
Fong NJC, Burgess ML, Barrow KD, Glenn DR:Influence of nutritive factors on C50 carotenoids production byHaloferax mediterraneiATCC 33500 with two-stage cultivation.Bioresource Technol. 2010, 101 (16): 6487-6493. 10.1016/j.biortech.2010.03.044.CrossRef
20.
Wang L, Chen SJ: Environment, genome and cancer. Comptes rendus de l’Académie des Sciences, Paris, Sciences de la vie, Life Sciences. 2001, 324: 1085-1091.
21.
Labi GV, Grespi F, Baumer F, Villunger A: Targeting the Bcl-2-regulated apoptosis pathway by BH3 mimetics: a breakthrough in anticancer therapy?. Cell Death Differ. 2008, 15: 977-987. 10.1038/cdd.2008.37.CrossRefPubMedPubMedCentral
22.
Ganesan P, Noda K, Manabe Y, Ohkubo T, Tanaka Y, Maoka T, Sugawara T, Hirata T: Siphonaxanthin, a marine carotenoid from green algae, effectively induces apoptosis in human leukemia (HL-60) cells. Biochem Bioph Acta. 2011, 1810: 497-503. 10.1016/j.bbagen.2011.02.008.CrossRef
23.
Tamsyn SAT, Pauline H, Declan PN: Anti-collagenase, anti-elastase and antioxidant activities of extracts from 21 plants. BMC Comple Altern M. 2009, 1472: 9-27.
24.
Gunasekara RS, Sewgobind K, Desai S, Dunn L, Black HS, McKeehan WL, Patil B: Lycopene and lutein inhibit proliferation in rat prostate carcinoma cells. Nutr Cancer. 2007, 58: 171-177. 10.1080/01635580701328339.CrossRef
25.
Peters U, Leitzmann MF, Chatterjee N, Wang Y, Albanes D, Gelmann EP, Friesen MD, Riboli E, Hayes RB: Serum lycopene, other carotenoids, and prostate cancer risk: a nested case-control study in the prostate, lung, colorectal, and ovarian cancer screening trial. Cancer Epidem Biomar Prev. 2007, 16: 962-968. 10.1158/1055-9965.EPI-06-0861.CrossRef
26.
Wang CC, Chang SC, Inbaraj BS, Chen BH: Isolation of carotenoids, flavonoids and polysaccharides from Lycium barbarum L and evaluation of antioxidant activity. Food Chem. 2010, 120: 184-192. 10.1016/j.foodchem.2009.10.005.CrossRef
27.
Baati H, Amdouni R, Azri C, Gharsallah N, Ammar E: Brines modelling progress: a management tool for Tunisian multipond solar salterns, based on physical, chemical and microbial parameters. Geophys J Roy Astron Soc. 2011, 29: 139-150.
28.
Birbir M, Calli B, Mertoglu B, Bardavid RE, Oren A, Ogman MN, Ogan A: Extremely halophilic archaea from Tuz lake, turkey, and the adjacent kaldirim and kayacik salterns. World J Microb Biot. 2007, 23: 309-316. 10.1007/s11274-006-9223-4.CrossRef
29.
Asker D, Ohta Y: Haloferax alexandrinus sp. nov., an extremely halophilic canthaxanthin-producing Archaeon from a solar saltern in Alexandria (Egypt). Int J Syst Evol Micr. 2002, 52: 729-738. 10.1099/ijs.0.01999-0.
30.
Enache M, Itoh T, Kamekura M, Popescu G, Dumitru L: Halophilic archaea of Haloferax genus isolated from anthropocentric Telega (Palada) salt lake. Proc Rom Acad, Series B. 2008, 2: 11-16.
31.
32.
Zheng A, Alm EW, Stahl DA, Raskin L: Characterization of universal small subunit rRNA hybridization probes for quantitative molecular microbial ecology studies. Appl Environ Microb. 1996, 62: 4504-4513.
33.
Swift IE, Milborrow BV: Retention of the 4-pro-R hydrogen atom of mevalonate at C-2, 2′ of bacterioruberin in halobacterium halobium. Biochem J. 1980, 187: 261-264.CrossRefPubMedPubMedCentral
34.
Britton G: UV/Visible spectroscopy. Carotenoids: spectroscopy, vol 1B. Edited by: Britton G, Liaaen- Jensen S, Pfander H. 1995, Basel: Birkhauser
35.
Xu Y, Leo MA, Lieber CS: Lycopene attenuates arachidonic acid toxicity in HepG2 cells over expressing CYP2E1. Biochem Biophys Res Commun. 2003, 303: 745-750. 10.1016/S0006-291X(03)00404-2.CrossRefPubMed
36.
Mosmann T: Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods. 1983, 65: 55-63. 10.1016/0022-1759(83)90303-4.CrossRefPubMed
37.
Youqing X, Maria AL, Charle SL: Lycopene attenuates alcoholic apoptosis in HepG2 cells expressing CYP2E1. Biochem Biophys Res Commun. 2003, 308: 614-618. 10.1016/S0006-291X(03)01435-9.CrossRef
38.
Garcia-Alonso FJ, Guidarelli A, Periago MJ: Phenolic-rich juice prevents DNA single-strand breakage and cytotoxicity caused by tert-butylhydroperoxide in U937 cells: the role of iron chelation. J Nutr Biochem. 2007, 18: 457-466. 10.1016/j.jnutbio.2006.08.003.CrossRefPubMed
39.
Krieg NR, Holt JG: Bergey’s Manuel of Systematic Bacteriology”, Volume 1. 1984, Baltimore: Williams & Wilkins, 261-262. 1984
40.
Donadio C, Bialecki A, Valla A, Dufosse L: Carotenoid-derived aroma compounds detected and identified in brines and speciality sea salts (fleur de sel) produced in solar salterns from Saint-Armel (France). J Food Comp Anal. 2011, 24: 801-810. 10.1016/j.jfca.2011.03.005.CrossRef
41.
Oren A, Rodriguez-Valera F: The contribution of halophilic Bacteria1 to the red coloration of saltern crystallizer ponds. FEMS Microbiol Ecol. 2001, 1242: 1-8.
42.
Kelly M, Norgard S, Liaaen-Jensen S: Bacterial carotenoids. C50-Carotenoids. Carotenoids of Halobacterium salinarium, especially bacterioruberin. Acta Chem Scand. 1970, 24: 2169-2182.CrossRefPubMed
43.
Asker D, Ohta Y: Production of canthaxanthin by extremely halophilic bacteria. J Biosci Bioeng. 1999, 88: 617-621. 10.1016/S1389-1723(00)87089-9.CrossRefPubMed
44.
Ho YC: Study on the hepatoprotection of Antrodia cinnamomea and anti hepatoma activities of ethanolic extracts from hops and Haloferax mediterranei. Dissertation. 2007, 1: 179-
45.
Teodoro AJ, Oliveira FL, Martins NB, Maia GA, Martucci RB, Borojevic R: Effect of lycopene on cell viability and cell cycle progression in human cancer cell lines. Cancer Cell Inter. 2012, 12: 1475-2867.CrossRef
46.
Burgess LC, Rice E, Fischer T, Seekins JR, Burgess TL, Sticka SJ, Klatt K: Lycopene has limited effect on cell proliferation in only two of seven human cell lines (both cancerous and non cancerous) in an in vitro system with doses across the physiological range. Toxicol in Vitro. 2008, 22: 1297-1300. 10.1016/j.tiv.2008.03.001.CrossRefPubMedPubMedCentral
47.
Park YO, Hwang ES, Moon TW: The effect of lycopene on cell growth and oxidative DNA damage of Hep3B human hepatoma. Cells Biofactors. 2005, 23: 129-139. 10.1002/biof.5520230302.CrossRefPubMed
48.
Kotake-Nara E, Kushiro M, Zhang H, Sugawara T, Miyashita K, Nagao A: Carotenoids affect proliferation of human prostate cancer cells. J Nutr. 2001, 131: 3303-3306.PubMed
49.
Palozza P, Serini S, Di Nicuolo F, Piccioni E, Calviello G: Prooxidant effects of β- carotene in cultured cells molecular. Aspects Med. 2003, 24: 353-362. 10.1016/S0098-2997(03)00031-1.CrossRef
50.
Zhang LX, Cooney KW, Bertram JS: Carotenoids upregulate connexin 43 gene expression independent of their provitamin A activity or antioxidant properties. Cancer Res. 1992, 52: 5707-5712.PubMed
51.
Fornelli F, Leone A, Verdesca I, Minervini F, Zacheo G: The influence of lycopene on the proliferation of human breast cell line (MCF-7). Toxicol in vitro. 2007, 21: 217-223. 10.1016/j.tiv.2006.09.024.CrossRefPubMed
52.
Leone A, Zefferino R, Longo C, Leo L, Zacheo G: Supercritical CO2-extracted tomato oleoresins enhance gap junction intercellularcommunications and recover from mercury chloride inhibition in keratinocytes. J Agric Food Chem. 2010, 58: 4769-4778. 10.1021/jf1001765.CrossRefPubMed
53.
Stahl W, Sies H: Bioactivity and protective effects of natural carotenoids - Review. Biochim Biophys Acta. 2005, 1740: 101-107. 10.1016/j.bbadis.2004.12.006.CrossRefPubMed
54.
Trekli MC, Riss G, Goralczyk R, Tyrrell RM: Beta-carotene suppresses UVA12 induced HO-1 gene expression in cultured FEK4. Free Rad Biol Med. 2003, 34: 456-464. 10.1016/S0891-5849(02)01303-5.CrossRefPubMed
Metadata
Title
Biological properties of carotenoids extracted from Halobacterium halobium isolated from a Tunisian solar saltern
Authors
Molka Abbes
Houda Baati
Sonda Guermazi
Concetta Messina
Andrea Santulli
Neji Gharsallah
Emna Ammar
Publication date
01-12-2013
Publisher
BioMed Central
Published in
BMC Complementary Medicine and Therapies / Issue 1/2013
Electronic ISSN: 2662-7671
DOI
https://doi.org/10.1186/1472-6882-13-255

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