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In Vitro Antioxidant, Antihemolytic, and Anticancer Activity of the Carotenoids from Halophilic Archaea

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Abstract

Halophilic archaea represent a promising natural source of carotenoids. However, little information is available about the biological effects of carotenoids from halophilic archaea. In this study, the carotenoids produced by seven halophilic archaeal strains Halogeometricum rufum, Halogeometricum limi, Haladaptatus litoreus, Haloplanus vescus, Halopelagius inordinatus, Halogranum rubrum, and Haloferax volcanii were identified by ultraviolet/visible spectroscopy, thin-layer chromatography, and high-performance liquid chromatography-tandem mass spectrometry. The C50 carotenoids bacterioruberin and its derivatives monoanhydrobacterioruberin and bisanhydrobacterioruberin were found to be the predominant carotenoids. The antioxidant capacities of the carotenoids from these strains were significantly higher than β-carotene as determined by 1,1-diphenyl-2-picrylhydrazyl radical scavenging assay. The antihemolytic activities of these carotenoid extracts against H2O2-induced hemolysis in mouse erythrocytes were 3.9–6.3 times higher than β-carotene. A dose-dependent in vitro antiproliferative activity against HepG2 cells was observed for the extract from Hgm. limi, while that from Hpn. vescus exhibited a relatively high activity in a dose-independent manner. These results suggested that halophilic archaea could be considered as an alternative source of natural carotenoids with high antioxidant, antihemolytic, and anticancer activity.

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References

  1. Abbes M, Baati H, Guermazi S, Messina C, Santulli A, Gharsallah N, Ammar E (2013) Biological properties of carotenoids extracted from Halobacterium halobium isolated from a Tunisian solar saltern. BMC Complement Altern Med 13:255–262

    Article  PubMed  PubMed Central  Google Scholar 

  2. Ajila CM, Prasada Rao UJ (2008) Protection against hydrogen peroxide induced oxidative damage in rat erythrocytes by Mangifera indica L. peel extract. Food Chem Toxicol 46:303–309

    Article  CAS  PubMed  Google Scholar 

  3. Albrecht M, Takaichi S, Steiger S, Wang ZY, Sandmann G (2000) Novel hydroxycarotenoids with improved antioxidative properties produced by gene combination in Escherichia coli. Nat Biotechnol 18:843–846

    Article  CAS  PubMed  Google Scholar 

  4. Barua RK, Barua AB (1966) Oxidation of zeaxanthin. Isolation and properties of 3-hydroxyretinene. Biochem J 101:250–255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Britton G (1995) UV/Visible spectroscopy. In: Britton G, Liaaen-Jensen S, Pfander H (eds) Carotenoids: spectroscopy, vol 1B. Birkhäuser Verlag, Basel, pp 13–62

    Google Scholar 

  6. Britton G, Liaaen-Jensen S, Pfander H, Mercadante AZ, Egeland ES (2004) Carotenoids-handbook. Birkhäuser Verlag, Basel

    Book  Google Scholar 

  7. Burgess LC, Rice E, Fischer T, Seekins JR, Burgess TP, Sticka SJ, Klatt K (2008) Lycopene has limited effect on cell proliferation in only two of seven human cell lines (both cancerous and noncancerous) in an in vitro system with doses across the physiological range. Toxicol In Vitro 22:1297–1300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Calegari-Santos R, Diogo RA, Fontana JD, Bonfim TM (2016) Carotenoid production by halophilic archaea under different culture conditions. Curr Microbiol 72:641–651

    Article  CAS  PubMed  Google Scholar 

  9. Chen CW, Hsu SH, Lin MT, Hsu YH (2015) Mass production of C50 carotenoids by Haloferax mediterranei in using extruded rice bran and starch under optimal conductivity of brined medium. Bioprocess Biosyst Eng 38:2361–2367

    Article  PubMed  Google Scholar 

  10. Cui HL, Gao X, Li XY, Xu XW, Zhou YG, Liu HC, Zhou PJ (2010) Halosarcina limi sp. nov., a halophilic archaeon from a marine solar saltern, and emended description of the genus Halosarcina. Int J Syst Evol Microbiol 60:2462–2466

    Article  CAS  PubMed  Google Scholar 

  11. Cui HL, Li XY, Gao X, Xu XW, Zhou YG, Liu HC, Oren A, Zhou PJ (2010) Halopelagius inordinatus gen. nov., sp. nov., a new member of the family Halobacteriaceae isolated from a marine solar saltern. Int J Syst Evol Microbiol 60:2089–2093

    Article  CAS  PubMed  Google Scholar 

  12. Cui HL, Yang X, Gao X, Xu XW (2011) Halobellus clavatus gen. nov., sp. nov. and Halorientalis regularis gen. nov., sp. nov., two new members of the family Halobacteriaceae. Int J Syst Evol Microbiol 61:2682–2689

    Article  CAS  PubMed  Google Scholar 

  13. Fang CJ, Ku KL, Lee MH, Su NW (2010) Influence of nutritive factors on C50 carotenoids production by Haloferax mediterranei ATCC 33500 with two-stage cultivation. Bioresour Technol 101:6487–6493

    Article  CAS  PubMed  Google Scholar 

  14. Huang D, Ou B, Prior RL (2005) The chemistry behind antioxidant capacity assays. J Agric Food Chem 53:1841–1856

    Article  CAS  PubMed  Google Scholar 

  15. Kelly M, Jensen SL (1967) Bacterial carotenoids. XXVI. C50-carotenoids. 2. Bacterioruberin. Acta Chem Scand 21:2578–2580

    Article  CAS  PubMed  Google Scholar 

  16. Kotake-Nara E, Kushiro M, Zhang H, Sugawara T, Miyashita K, Nagao A (2001) Carotenoids affect proliferation of human prostate cancer cells. J Nutr 131:3303–3306

    Article  CAS  PubMed  Google Scholar 

  17. Leone A, Zefferino R, Longo C, Leo L, Zacheo G (2010) Supercritical CO2-extracted tomato oleoresins enhance gap junction intercellular communications and recover from mercury chloride inhibition in keratinocytes. J Agric Food Chem 58:4769–4778

    Article  CAS  PubMed  Google Scholar 

  18. Mandelli F, Miranda VS, Rodrigues E, Mercadante AZ (2012) Identification of carotenoids with high antioxidant capacity produced by extremophile microorganisms. World J Microbiol Biotechnol 28:1781–1790

    Article  CAS  PubMed  Google Scholar 

  19. Margesin R, Schinner F (2001) Potential of halotolerant and halophilic microorganisms for biotechnology. Extremophiles 5:73–83

    Article  CAS  PubMed  Google Scholar 

  20. Rodrigo-Baños M, Garbayo I, Vílchez C, Bonete MJ, Martínez-Espinosa RM (2015) Carotenoids from haloarchaea and their potential in biotechnology. Mar Drugs 13:5508–5532

    Article  PubMed  PubMed Central  Google Scholar 

  21. Ronnekleiv M (1995) Bacterial carotenoids 53* C50-carotenoids 23; carotenoids of Haloferax volcanii versus other halophilic bacteria. Biochem Syst Ecol 23:627–634

    Article  CAS  Google Scholar 

  22. Sachindra NM, Sato E, Maeda H, Hosokawa M, Niwano Y, Kohno M, Miyashita K (2007) Radical scavenging and singlet oxygen quenching activity of marine carotenoid fucoxanthin and its metabolites. J Agric Food Chem 55:8516–8522

    Article  CAS  PubMed  Google Scholar 

  23. Vílchez C, Forján E, Cuaresma M, Bédmar F, Garbayo I, Vega JM (2011) Marine carotenoids: biological functions and commercial applications. Mar Drugs 9:319–333

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was financially supported by grants from National Natural Science Foundation of China (Nos. 31600002 and 31370054), China Postdoctoral Science Foundation funded project (No. 2015M581728), Jiangsu Planned Projects for Postdoctoral Research Funds (No. 1501069C), and the Advanced Talent Foundation of Jiangsu University (No. 15JDG062). The authors thank Prof. Aharon Oren (The Hebrew University of Jerusalem) for many helpful suggestions.

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Correspondence to Heng-Lin Cui.

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Hou, J., Cui, HL. In Vitro Antioxidant, Antihemolytic, and Anticancer Activity of the Carotenoids from Halophilic Archaea. Curr Microbiol 75, 266–271 (2018). https://doi.org/10.1007/s00284-017-1374-z

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