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Carotenoids from the extreme halophilic archaeon Haloterrigena turkmenica: identification and antioxidant activity

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Abstract

Haloterrigena turkmenica was able to synthesize carotenoids when grown in halobacteria medium. These molecules have antioxidant properties and find application in food, cosmetic, and pharmaceutical fields. The carotenoids were extracted with methanol, separated by RP-HPLC, and identified by mass spectrometry and UV/Vis spectra analyses. The C50 carotenoids were the main pigments, and C30, C40, and C51 carotenoids were also detected. Seven geometric isomers were distinguished for bacterioruberin, monoanhydrobacterioruberin, and bisanhydrobacterioruberin. The assignment to a specific isomer was tentatively attempted through the analysis of the corresponding UV/Vis spectrum, the intensity of the cis peak, and its spectral fine structure. Lycopene, phytoene, and lycopersene were among the minor carotenoids further identified. The extract displayed antioxidant power higher than alpha-tocopherol, butylhydroxytoluene, and ascorbic acid used as reference compounds. Our studies identified for the first time seven geometric isomers of bacterioruberin derivatives and 30 carotenoids in a haloarchaeon.

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Abbreviations

APCI-ITMSn :

Atmospheric Pressure Chemical Ionization multistage Ion Trap Mass Spectrometry

BABR:

Bisanhydrobacterioruberin

BR:

Bacterioruberin

MABR:

Monoanhydrobacterioruberin

References

  • 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. doi:10.1186/1472-6882-13-255

  • Albrecht M, Takaichi S, Steiger S, Wang Z, Sandmann G (2000) Novel hydroxycarotenoids with improved antioxidative properties produced by gene combination in Escherichia coli. Nat Biotechnol 18:843–846. doi:10.1038/78443

    Article  CAS  PubMed  Google Scholar 

  • Anunciato TP, da Rocha Filho PA (2012) Carotenoids and polyphenols in nutricosmetics, nutraceuticals, and cosmeceuticals. J Cosmet Dermatol 11:51–54

    Article  PubMed  Google Scholar 

  • Asker D, Ohta Y (1999) Production of canthaxanthin by extremely halophilic bacteria. J Biosci Bioeng 88:617–621

    Article  CAS  PubMed  Google Scholar 

  • Asker D, Awad T, Ohta Y (2002) Lipids of Haloferax alexandrinus strain TMT: an extremely halophilic canthaxanthin-producing archaeon. J Biosci Bioeng 93:37–43. doi:10.1016/S1389-1723(02)80051-2

    Article  CAS  PubMed  Google Scholar 

  • Benzie IF, Strain JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem 239:70–76. doi:10.1006/abio.1996.0292

    Article  CAS  PubMed  Google Scholar 

  • Bramley P (2003) The genetic enhancement of phytochemicals: the case of carotenoids. In: Johnson I, Williamson G (eds) Phytochemical functional foods. Woodhead Publishing Limited, CRC Press, Cambridge, pp 253–274

    Chapter  Google Scholar 

  • Cazzonelli CI (2011) Carotenoids in nature: insights from plants and beyond. Funct Plant Biol 38:833–847. doi:10.1071/FP11192

    Article  CAS  Google Scholar 

  • de la Vega M, Sayago A, Ariza J, Barneto AG, Leon R (2016) Characterization of a bacterioruberin-producing haloarchaea isolated from the marshlands of the Odiel River in the southwest of Spain. Biotechnol Prog 32:592–600. doi:10.1002/btpr.2248

    Article  PubMed  Google Scholar 

  • de Lourdes Moreno M, Sánchez-Porro C, García MT, Mellado E (2012) Carotenoids’ production from halophilic bacteria. Methods Mol Biol 892:207–217. doi:10.1007/978-1-61779-879-5_12

    Article  PubMed  Google Scholar 

  • 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. doi:10.1016/j.biortech.2010.03.044

    Article  CAS  PubMed  Google Scholar 

  • Fong NJC, Burgess ML, Barrow KD, Glenn DR (2001) Carotenoid accumulation in the psychrotrophic bacterium Arthrobacter agilis in response to thermal and salt stress. Appl Microbiol Biotechnol 56:750–756. doi:10.1007/s002530100739

    Article  CAS  PubMed  Google Scholar 

  • Furubayashi M, Umeno D (2012) Directed evolution of carotenoid synthases for the production of unnatural carotenoids. Methods Mol Biol 892:245–253. doi:10.1007/978-1-61779-879-5_14

    Article  CAS  PubMed  Google Scholar 

  • Grant WD, Kamekura M, McGenity TJ, Ventosa A (2001) Class III. Halobacteria class Nov. In: Boone DR, Castenholz RW, Garrity GM (eds) Bergey’s manual of systematic bacteriology, 2nd edn. Springer, New York, pp 294–299

    Google Scholar 

  • Gupta RS, Naushad S, Fabros R, Adeolu M (2016) A phylogenomic reappraisal of family-level divisions within the class Halobacteria: proposal to divide the order Halobacteriales into the families Halobacteriaceae, Haloarculaceae fam. nov., and Halococcaceae fam. nov., and the order Haloferacales into the families, Haloferacaceae and Halorubraceae fam nov. Antonie Van Leeuwenhoek 109:565–587

    Article  PubMed  Google Scholar 

  • Jaswir I, Noviendri D, Hasrini RF, Octavianti F (2011) Carotenoids: sources, medicinal properties and their application in food and nutraceutical industry. J Med Plant Res 5:7119–7131

    CAS  Google Scholar 

  • Jiménez-Escrig A, Jiménez-Jiménez I, Sánchez-Moreno C, Saura-Calixto F (2000) Evaluation of free radical scavenging of dietary carotenoids by the stable radical 2,2-diphenyl-1-picrylhydrazyl. J Sci Food Agric 80:1686–1690. doi:10.1002/1097-0010(20000901)80

    Article  Google Scholar 

  • Ke B, Imsgard F, Kjøsen H, Liaaen-Jensen S (1970) Electronic spectra of carotenoids at 77° K. Biochim Biophys Acta Lipids Lipid Metab 210:139–152

    Article  CAS  Google Scholar 

  • Kiokias S, Gordon MH (2004) Antioxidant properties of carotenoids in vitro and in vivo. Food Rev Int 20:99–121. doi:10.1081/FRI-120037155

    Article  CAS  Google Scholar 

  • Kirti K, Amita S, Priti S, Kumar AM, Jyoti S (2014) Colorful world of microbes: carotenoids and their applications. Adv Biol. doi:10.1155/2014/837891

    Google Scholar 

  • Kuchina N (2014a) Topical halobacteria extract composition for treating radiation skin tissue damage. Patent WO2014045280 A1. 27 Mar 2014

  • Kuchina N (2014b) Halobacteria extracts composition for tumor reduction. Patent WO/2014/045279. 27 Mar 2014

  • Kushwaha SC, Kates M, Porter JW (1976) Enzymatic synthesis of C40 carotenes by cell-free preparation from Halobacterium cutirubrum. Can J Biochem 54:816–823

    Article  CAS  PubMed  Google Scholar 

  • Lobasso S, Lopalco P, Mascolo G, Corcelli A (2008) Lipids of the ultra-thin square halophilic archaeon Haloquadratum walsbyi. Archaea 2:177–183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lorantfy B, Renkecz T, Koch C, Horvai G, Lendl B, Herwig C (2014) Identification of lipophilic bioproduct portfolio from bioreactor samples of extreme halophilic archaea with HPLC–MS/MS. Anal Bioanal Chem 406:2421–2432. doi:10.1007/s00216-014-7626-x

    Article  CAS  PubMed  Google Scholar 

  • Lu S, Li L (2008) Carotenoid metabolism: biosynthesis, regulation, and beyond. J Integr Plant Biol 50:778–785. doi:10.1111/j.1744-7909.2008.00708.x

    Article  CAS  PubMed  Google Scholar 

  • 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. doi:10.1007/s11274-011-0993-y

    Article  CAS  PubMed  Google Scholar 

  • Mariutti LR, Pereira DM, Mercadante AZ, Valentão P, Teixeira N, Andrade PB (2012) Further insights on the carotenoid profile of the echinoderm Marthasterias glacialis L. Mar Drugs 10:1498–1510. doi:10.3390/md10071498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martinez-Espinosa RM, Bonete-Perez MJ, Martinez-Martinez P (2009) COMPUESTO A BASE DE MEMBRANAS CELULARES LIOFILIZADAS. Patent ES2324077 A1. 29 July 2009

  • Miller NJ, Sampson J, Candeias LP, Bramley PM, Rice-Evans CA (1996) Antioxidant activities of carotenoids and xanthophylls. FEBS Lett 384:240–242. doi:10.1016/0014-5793(96)00323-7

    Article  CAS  PubMed  Google Scholar 

  • Naziri D, Hamidi M, Hassanzadeh S, Tarhriz V, Maleki Zanjani B, Nazemyieh H, Hejazi MA, Hejazi MS (2014) Analysis of carotenoid production by Halorubrum sp. TBZ126; an extremely halophilic Archeon from Urmia Lake. Adv Pharm Bull 4:61–67. doi:10.5681/apb.2014.010

    CAS  PubMed  Google Scholar 

  • Nelis HJ, de Leenheer AP (1991) Microbial sources of carotenoid pigments used in foods and feeds. J Appl Bacteriol 70:181–191. doi:10.1111/j.1365-2672.1991.tb02922.x

    Article  CAS  Google Scholar 

  • Rivera SM, Christou P, Canela-Garayoa R (2014) Identification of carotenoids using mass spectrometry. Mass Spectrom Rev 33:353–372. doi:10.1002/mas.21390

    Article  CAS  PubMed  Google Scholar 

  • 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. doi:10.3390/md13095508

    Article  PubMed  PubMed Central  Google Scholar 

  • Rønnekleiv M, Liaaen-Jensen S (1992) Bacterial carotenoids. 52. C50-carotenoids 22. Naturally occurring geometric isomers of bacterioruberin. Acta Chem Scand 46:1092–1095

    Article  Google Scholar 

  • Saito T, Terato H, Yamamoto O (1994) Pigments of Rubrobacter radiotolerans. Arch Microbiol 162:414–421. doi:10.1007/s002030050159

    Article  CAS  Google Scholar 

  • Shi J, Le Maguer M (2000) Lycopene in tomatoes: chemical and physical properties affected by food processing. Crit Rev Biotechnol 20:293–334. doi:10.1080/07388550091144212

    Article  CAS  PubMed  Google Scholar 

  • Snodderly DM (1995) Evidence for protection against age-related macular degeneration by carotenoids and antioxidant vitamins. Am J Clin Nutr 62:1448S–14615S

    CAS  PubMed  Google Scholar 

  • Squillaci G, Finamore R, Diana P, Restaino OF, Schiraldi C, Arbucci S, Ionata E, La Cara F, Morana A (2016) Production and properties of an exopolysaccharide synthesized by the extreme halophilic archaeon Haloterrigena turkmenica. Appl Microbiol Biotechnol 100:613–623. doi:10.1007/s00253-015-6991-5

    Article  CAS  PubMed  Google Scholar 

  • Tornabene TG, Kates M, Gelpi E, Oro J (1969) Occurrence of squalene, di- and tetrahydrosqualenes, and vitamin MK8 in an extremely halophilic bacterium, Halobacterium cutirubrun. J Lipid Res 10:294–303

    CAS  PubMed  Google Scholar 

  • 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. doi:10.3390/md9030319

    Article  PubMed  PubMed Central  Google Scholar 

  • Yachai M (2009) Carotenoid production by halophilic Archaea and its applications. PhD Thesis, Prince of Songkla University

  • Yang Y, Yatsunami R, Ando A, Miyoko N, Fukui T, Takaichi S, Nakamura S (2015) Complete biosynthetic pathway of the C50 carotenoid bacterioruberin from lycopene in the extremely halophilic archaeon Haloarcula japonica. J Bacteriol 197:1614–1623. doi:10.1128/JB.02523-14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yatsunami R, Ando A, Yang Y, Takaichi S, Kohno M, Matsumura Y, Ikeda H, Fukui T, Nakasone K, Fujita N, Sekine M, Takashina T, Nakamura S (2014) Identification of carotenoids from the extremely halophilic archaeon Haloarcula japonica. Front Microbiol 5:100. doi:10.3389/fmicb.2014.00100

    Article  PubMed  PubMed Central  Google Scholar 

  • Zechmeister L (1944) Cis–trans isomerization and stereochemistry of carotenoids and diphenylpolyenes. Chem Rev 34:267–344

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Institute of Agro-environmental and Forest Biology, National Research Council of Italy (CNR), Via Pietro Castellino 111, 80131, Naples, Italy

    Giuseppe Squillaci, Roberta Parrella, Francesco La Cara & Alessandra Morana

  2. Proteomic and Biomolecular Mass Spectrometry Center, Institute of Food Sciences, National Research Council of Italy (CNR), Via Roma 64, 83100, Avellino, Italy

    Virginia Carbone & Paola Minasi

Authors
  1. Giuseppe Squillaci
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  2. Roberta Parrella
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  3. Virginia Carbone
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  4. Paola Minasi
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  5. Francesco La Cara
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  6. Alessandra Morana
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Correspondence to Alessandra Morana.

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Communicated by A. Oren.

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Squillaci, G., Parrella, R., Carbone, V. et al. Carotenoids from the extreme halophilic archaeon Haloterrigena turkmenica: identification and antioxidant activity. Extremophiles 21, 933–945 (2017). https://doi.org/10.1007/s00792-017-0954-y

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