Advertisement

Extremophiles

, Volume 22, Issue 3, pp 359–366 | Cite as

Effects of nicotine on the biosynthesis of carotenoids in halophilic Archaea (class Halobacteria): an HPLC and Raman spectroscopy study

  • Aharon Oren
  • Joseph Hirschberg
  • Varda Mann
  • Jan Jehlička
Original Paper

Abstract

Nicotine has a profound influence on the carotenoid metabolism in halophilic Archaea of the class Halobacteria. In a study of Halobacterium salinarum, Haloarcula marismortui and Halorubrum sodomense, using different analytical techniques to monitor the production of different carotenoids as a function of the presence of nicotine, we showed that the formation of α-bacterioruberin was inhibited in all. In Hbt. salinarum, addition of nicotine led to a significant change in the color of the culture due to the accumulation of lycopene, in addition to the formation of bisanhydrobacterioruberin which does not differ in color from α-bacterioruberin. Very little or no lycopene was formed in Har. marismortui and in Hrr. sodomense; instead bisanhydrobacterioruberin was the only major carotenoid found in nicotine-amended cultures. The findings are discussed in the framework of the recently elucidated biochemical pathway for the formation of the different carotenoid pigments encountered in the Halobacteria.

Keywords

Haloarchaea Carotenoids Bacterioruberin Nicotine 

Notes

Acknowledgements

We thank Lily Mana for technical assistance. AO was supported by Grant no. 2221/15 from the Israel Science Foundation. This study was further supported by the Erasmus+ inter-institutional agreement between the Charles University, Prague, and the Hebrew University of Jerusalem. JJ was funded by the Czech Science Foundation Project 17-04270S. Work in the laboratory of JH is funded by Israel Science Foundation Grant ISF 850/13.

References

  1. Asker D, Ohta Y (1999) Production of canthaxanthin by extremely halophilic bacteria. J Biosci Bioengin 88:617–621CrossRefGoogle Scholar
  2. Asker D, Ohta Y (2002) Production of canthaxanthin by Haloferax alexandrinus under non-aseptic conditions and a simple, rapid method for its extraction. Appl Microbiol Biotechnol 58:743–750CrossRefPubMedGoogle Scholar
  3. Calo P, de Miguel T, Sieiro C, Velazquez JB, Villa TG (1995) Ketocarotenoids in halobacteria: 3-hydroxy-echinenone and trans-astaxanthin. J Appl Bacteriol 79:282–285CrossRefGoogle Scholar
  4. Camacho-Córdova DI, Camacho-Ruíz RM, Córdova-López JA, Cervantes-Martínez J (2014) Estimation of bacterioruberin by Raman spectroscopy during the growth of halophilic archaeon Haloarcula marismortui. Appl Opt 53:7470–7475CrossRefPubMedGoogle Scholar
  5. Chen CW, S-h Hsu, Lin M-T, Y-h Hsu (2015) Mass production of C50 carotenoids by Haloferax mediterranei in using extruded rice bran and starch under optimal conductivity of brine medium. Bioprocess Biosyst Env 38:2361–2367CrossRefGoogle Scholar
  6. de la Vega M, Sayago A, Ariza J, Barneto AG, León R (2016) Characterization of a bacterioruberin-producing haloarchaea isolated from the marshlands of the Odiel River in the southwest of Spain. Biotechnol Progr 32:592–600CrossRefGoogle Scholar
  7. de Oliveira VE, Castro HV, Edwards HGM, de Oliveira LFC (2010) Carotenes and carotenoids in natural biological samples: a Raman spectroscopic analysis. J Raman Spectrosc 41:642–650CrossRefGoogle Scholar
  8. Dundas ID, Larsen H (1962) The physiological role of the carotenoid pigments of Halobacterium salinarium. Arch Mikrobiol 44:233–239CrossRefGoogle Scholar
  9. Dundas ID, Larsen H (1963) A study on the killing by light of photosensitized cells of Halobacterium salinarium. Arch Mikrobiol 46:19–28CrossRefPubMedGoogle Scholar
  10. Fang C-J, Ku K-L, Lee M-H, Su N-W (2010) Influence of nutritive factors on C50 carotenoids production by Haloferax mediterranei ATCC 33500 with two-stage cultivation. Biores Technol 101:6487–6493CrossRefGoogle Scholar
  11. Fendrihan S, Musso M, Stan-Lotter H (2009) Raman spectroscopy as a potential method for the detection of extremely halophilic archaea embedded in halite in terrestrial and possibly extraterrestrial samples. J Raman Spectrosc 40:1996–2003CrossRefPubMedPubMedCentralGoogle Scholar
  12. Harris LV, McHugh M, Hutchinson IB, Ingley R, Malherbe C, Parnell J, Marshall AO, Edwards HGM (2015) Avoiding misidentification of bands in planetary Raman spectra. J Raman Spectrosc 46:863–872CrossRefGoogle Scholar
  13. Hou J, Gao X, Lü Z-Z, Li Y, Zhou Y, Cui H-L (2017) In vitro antioxidant, antihemolytic and anticancer activity of the carotenoids from halophilic archaea. Curr Microbiol.  https://doi.org/10.1007/s00284-017-1374-z Google Scholar
  14. Howes CD, Batra PP (1970) Accumulation of lycopene and inhibition of cyclic carotenoids in Mycobacterium in the presence of nicotine. Biochim Biophys Acta 222:174–179CrossRefPubMedGoogle Scholar
  15. Jehlička J, Oren A (2013) Raman spectroscopy in halophile research. Front Microbiol 10:380Google Scholar
  16. Jehlička J, Edwards HGM, Oren A (2013) Bacterioruberin and salinixanthin carotenoids of extremely halophilic Archaea and Bacteria: a Raman spectroscopic study. Spectrosc Acta A 106:99–103CrossRefGoogle Scholar
  17. Jehlička J, Edwards HGM, Oren A (2014a) Raman spectroscopic of microbial pigments. Appl Environ Microbiol 80:3286–3295CrossRefPubMedPubMedCentralGoogle Scholar
  18. Jehlička J, Edwards HGM, Osterrothová K, Novotná J, Nedbalová L, Kopecký J, Němec I, Oren A (2014b) Potential and limits of Raman spectroscopy for carotenoid detection in microorganisms: implications for astrobiology. Philos Trans R Soc A 372:20140199CrossRefGoogle Scholar
  19. Kelly M, Norgård S, Liaaen-Jensen S (1970) XXXI. C50 carotenoids of Halobacterium salinarium, especially bacterioruberin. Acta Chem Scand 24:2169–2182CrossRefPubMedGoogle Scholar
  20. Kushwaha SC, Kates M (1976) Effect of nicotine on biosynthesis of C50 carotenoids in Halobacterium cutirubrum. Can J Biochem 54:824–829CrossRefPubMedGoogle Scholar
  21. Kushwaha SC, Kates M (1979a) Studies on the biosynthesis of C50 carotenoids in Halobacterium cutirubrum. Can J Microbiol 25:1292–1297CrossRefPubMedGoogle Scholar
  22. Kushwaha SC, Kates M (1979b) Effect of nicotine on carotenogenesis in extremely halophilic bacteria. Phytochemistry 18:2061–2062CrossRefGoogle Scholar
  23. Kushwaha SC, Gochnauer MB, Kushner DJ, Kates M (1974) Pigments and isoprenoid compounds in extremely and moderately halophilic bacteria. Can J Microbiol 20:241–245CrossRefPubMedGoogle Scholar
  24. Kushwaha SC, Kramer JKG, Kates M (1975) Isolation and characterization of C50-carotenoid pigments and other polar isoprenoids from Halobacterium cutirubrum. Biochim Biophys Acta 398:303–314CrossRefPubMedGoogle Scholar
  25. Kushwaha SC, Kates M, Porter JW (1976) Enzymatic synthesis of C40 carotenes by cell-free preparation from Halobacterium cutirubrum. Can J Biochem 54:816–823CrossRefPubMedGoogle Scholar
  26. Lazrak T, Wolff G, Albrechts A-M, Nakatani Y, Ourisson G, Kates M (1988) Bacterioruberins reinforce reconstituted Halobacterium lipid membranes. Biochim Biophys Acta 939:160–162CrossRefGoogle Scholar
  27. Marshall CP, Leuko S, Coyle CM, Walter MR, Burns BP, Neilan BA (2007) Carotenoid analysis of halophilic archaea by resonance Raman spectroscopy. Astrobiology 7:631–643CrossRefPubMedGoogle Scholar
  28. McDermott JCB, Ben-Aziz A, Singh RK, Britton G, Goodwin TW (1973a) Recent studies of carotenoid biosynthesis in bacteria. Pure Appl Chem 35:29–46CrossRefPubMedGoogle Scholar
  29. McDermott JCB, Britton G, Goodwin TW (1973b) Effect of inhibitors of zeaxanthin synthesis in a Flavobacterium. J Gen Microbiol 77:161–171CrossRefGoogle Scholar
  30. Merlin JC (1985) Resonance Raman spectroscopy of carotenoids and carotenoid-containing systems. Pure Appl Chem 57:785–792CrossRefGoogle Scholar
  31. Neuman H, Galpaz N, Cunningham FX Jr, Zamir D, Hirschberg J (2014) The tomato mutation nxd1 reveals a gene necessary for neoxanthin biosynthesis and demonstrates that violaxanthin is a sufficient precursor for abscisic acid biosynthesis. Plant J 78:80–93CrossRefPubMedGoogle Scholar
  32. Oren A, Rodríguez-Valera F (2001) The contribution of halophilic Bacteria to the red coloration of saltern crystallizer ponds. FEMS Microbiol Ecol 36:123–130PubMedGoogle Scholar
  33. Rodrigo-Baños M, Garbayo I, Vílchez C, Bonete MJ, Martínez-Espinosa RM (2015) Carotenoids from haloarchaea and their potential in biotechnology. Mar Drugs 13:5508–5532CrossRefPubMedPubMedCentralGoogle Scholar
  34. Ronen G, Cohen M, Zamir D, Hirschberg J (1999) Regulation of carotenoid biosynthesis during tomato fruit development: expression of the gene for lycopene epsilon-cyclase is down-regulated during ripening and is elevated in the mutant Delta. Plant J 17:341–351CrossRefPubMedGoogle Scholar
  35. Rønnekleiv M, Liaaen-Jensen S (1995) Bacterial carotenoids 53, C50-carotenoids 23; carotenoids of Haloferax volcanii versus other halophilic bacteria. Biochem Syst Ecol 23:627–634CrossRefGoogle Scholar
  36. Rønnekleiv M, Lenes M, Norgård S, Liaaen-Jensen S (1995) Three dodecaene C50-carotenoids from halophilic bacteria. Phytochemistry 39:631–634CrossRefGoogle Scholar
  37. Shahmohammadi HR, Asgarani E, Terato H, Saito T, Ohyama Y, Gekko K, Yamamoto O, Ide H (1998) Protective roles of bacterioruberin and intracellular KCl in the resistance of Halobacterium salinarium against DNA-damaging agents. J Radiat Res 39:251–262CrossRefPubMedGoogle Scholar
  38. Sikkandar S, Murugan K, Al-Sohaibani S, Rayappan F, Nair A, Tilton F (2013) Halophilic bacteria—a potent source of carotenoids with antioxidant and anticancer potentials. J Pure Appl Microbiol 7:2825–2830Google Scholar
  39. Squillaci G, Parrella R, Carbone V, Minasi P, La Cara F, Morana F (2017) Carotenoids from the extreme halophilic Haloterrigena turkmenica: identification and antioxidant activity. Extremophiles 21:933–945CrossRefPubMedGoogle Scholar
  40. Straub O (1987) In: Pfander H, Gerspacher M, Rychener M, Schwabe R (eds) Key to carotenoids, 2nd edn. Birkhäuser Verlag, Basel, pp 11–218CrossRefGoogle Scholar
  41. Withnall R, Chowdhry BZ, Silver J, Edwards HGM, de Oliveira LFC (2003) Raman spectra of carotenoids in natural products. Spectrochim Acta A 59:2207–2212CrossRefGoogle Scholar
  42. Yang Y, Yatsunami R, 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 197:1614–1623CrossRefPubMedPubMedCentralGoogle Scholar
  43. Yatsunami R, Ando A, Yang Y, Takaichi S, Kohno M, Matsumara Y, Ideka 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 5:100CrossRefPubMedPubMedCentralGoogle Scholar
  44. Yoshimura K, Kouyama T (2008) Structural role of bacterioruberin in the trimeric structure of archaerhodopsin-2. J Mol Biol 375:1267–1281CrossRefPubMedGoogle Scholar

Copyright information

© Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  • Aharon Oren
    • 1
  • Joseph Hirschberg
    • 2
  • Varda Mann
    • 2
  • Jan Jehlička
    • 3
  1. 1.Department of Plant and Environmental Sciences, Alexander Silberman Institute of Life SciencesThe Hebrew University of JerusalemJerusalemIsrael
  2. 2.Department of Genetics, Alexander Silberman Institute of Life SciencesThe Hebrew University of JerusalemJerusalemIsrael
  3. 3.Institute of Geochemistry, Mineralogy and Mineral ResourcesCharles UniversityPragueCzech Republic

Personalised recommendations