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The Nature and Function of Carotenoids in the Moderately Halophilic Bacterium Halobacillus halophilus

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Halophiles and Hypersaline Environments

Abstract

Carotenoids are widely distributed in extremophiles. Among these organisms especially C30 and C50 carotenoids are found. Here, we describe the structure and function of carotenoids in halophiles with focus on the moderately halophilic bacterium Halobacillus halophilus. H. halophilus produces an unusual C30 carotenoid. The structure was solved by HR-MS and NMR analyses as methyl glucosyl-3,4-dehydro-apo-8 -lycopenoate. Six genes could be identified that are involved in the biosynthesis of carotenoids. Together with the structural analyses of intermediates of methyl glucosyl-3,4-dehydro-apo-8 -lycopenoate produced by a pigment mutant a putative and unique biosynthesis pathway could be postulated. The isolated carotenoid and its intermediates showed a high antioxidative activity and also the protective function of these pigments could be demonstrated for H. halophilus.

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References

  • Aasen AJ, Francis GW, Liaaen-Jensen S (1969) Bacterial Carotenoids. XXIX. The carotenoids of two yellow halophilic cocci – including a new glycosidic methyl apo-lycopene. Acta Chem Scand 23:4–13

    Google Scholar 

  • Anwar M, Khan TH, Prebble J, Zagalsky PF (1977) Membrane-bound carotenoid in Micrococcus luteus protects naphthoquinone from photodynamic action. Nature 270:538–540

    Article  PubMed  CAS  Google Scholar 

  • Balashov SP (2000) Protonation reactions and their coupling in bacteriorhodopsin. Biochim Biophys Acta 1460:75–94

    Article  PubMed  CAS  Google Scholar 

  • Balashov SP, Imasheva ES, Boichenko VA, Anton J, Wang JM, Lanyi JK (2005) Xanthorhodopsin: a proton pump with a light-harvesting carotenoid antenna. Science 309:2061–2064

    Article  PubMed  CAS  Google Scholar 

  • Balashov SP, Imasheva ES, Wang JM, Lanyi JK (2008) Excitation energy-transfer and the relative orientation of retinal and carotenoid in xanthorhodopsin. Biophys J 95:2402–2414

    Article  PubMed  CAS  Google Scholar 

  • Becker HGO, Böttcher H, Dietz F, Rehorek D, Roewer G, Schiller K, Timpe H-J (1991) Einführung in die Photochemie. Deutscher Verlag der Wissenschaften, Berlin

    Google Scholar 

  • Ben-Amotz A, Avron M (1990) The biotechnology of cultivating the halotolerant alga Dunaliella. Trends Biotechnol 8:121–126

    Article  CAS  Google Scholar 

  • Britton G, Liaaen-Jensen S, Pfander H (2004) Handbook of carotenoids. Birkhäuser Verlag, Basel

    Google Scholar 

  • Burchard RP, Dworkin M (1966) Light-induced lysis and carotenogenesis in Myxococcus xanthus. J Bacteriol 91:535–545

    PubMed  CAS  Google Scholar 

  • Chattopadhyay MK, Jagannadham MV, Vairamani M, Shivaji S (1997) Carotenoid pigments of an antarctic psychrotrophic bacterium Micrococcus roseus: temperature dependent biosynthesis, structure, and interaction with synthetic membranes. Biochem Biophys Res Commun 239:85–90

    Article  PubMed  CAS  Google Scholar 

  • Claus D, Fahmy F, Rolf HJ, Tosunoglu N (1983) Sporosarcina halophila sp. nov., an obligate, slightly halophilic bacterium from salt marsh soils. Syst Appl Microbiol 4:496–506

    Google Scholar 

  • D’Souza SE, Altekar W, D’Souza SF (1997) Adaptive response of Haloferax mediterranei to low concentrations of NaCl (<20%) in the growth medium. Arch Microbiol 168:68–71

    Article  PubMed  Google Scholar 

  • Demmig-Adams B, Adams WW 3rd (2002) Antioxidants in photosynthesis and human nutrition. Science 298:2149–2153

    Article  PubMed  CAS  Google Scholar 

  • Duc LH, Fraser PD, Tam NK, Cutting SM (2006) Carotenoids present in halotolerant Bacillus spore formers. FEMS Microbiol Lett 255:215–224

    Article  CAS  Google Scholar 

  • Dundas ID, Larsen H (1963) A study on the killing by light of photosensitized cells of Halobacterium salinarium. Arch Mikrobiol 46:19–28

    Article  PubMed  CAS  Google Scholar 

  • Fong NJ, 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

    Article  PubMed  CAS  Google Scholar 

  • Gai F, Hasson KC, McDonald JC, Anfinrud PA (1998) Chemical dynamics in proteins: the photoisomerization of retinal in bacteriorhodopsin. Science 279:1886–1891

    Article  PubMed  CAS  Google Scholar 

  • Goodwin W (1980) The biochemnistry of carotenoids. Chapman and Hall, London

    Google Scholar 

  • Gruszecki WI (1999) Carotenoids in membranes. In: Frank HA, Young AJ, Britton G, Cogdell R (eds) The Photochemistry of Carotenoids. Kluwer, Dordrecht, Netherlands, pp 363–379

    Google Scholar 

  • Gruszecki WI, Sielewiesiuk J (1990) Orientation of xanthophylls in phosphatidylcholine multibilayers. Biochim Biophys Acta 1023:405–412

    Article  PubMed  CAS  Google Scholar 

  • Gruszecki WI, Sielewiesiuk J (1991) Galactolipid multibilayers modified with xanthophylls: orientational and diffractometric studies. Biochim Biophys Acta 1069:21–26

    Article  PubMed  CAS  Google Scholar 

  • Gruszecki WI, Sujak A, Strzalka K, Radunz A, Schmid GH (1999) Organisation of xanthophyll-lipid membranes studied by means of specific pigment antisera, spectrophotometry and monomolecular layer technique lutein versus zeaxanthin. Z Naturforsch C 54:517–525

    PubMed  CAS  Google Scholar 

  • Herbst J, Heyne K, Diller R (2002) Femtosecond infrared spectroscopy of bacteriorhodopsin chromophore isomerization. Science 297:822–825

    Article  PubMed  CAS  Google Scholar 

  • Jagannadham MV, Chattopadhyay MK, Subbalakshmi C, Vairamani M, Narayanan K, Rao CM, Shivaji S (2000) Carotenoids of an antarctic psychrotolerant bacterium, Sphingobacterium antarcticus, and a mesophilic bacterium, Sphingobacterium multivorum. Arch Microbiol 173:418–424

    Article  PubMed  CAS  Google Scholar 

  • Johanson CE (1981) Commonalities and differences among reinforcers. NIDA Res Monogr 37:235–237

    PubMed  CAS  Google Scholar 

  • Kahan A, Nahmias O, Friedman N, Sheves M, Ruhman S (2007) Following photoinduced dynamics in bacteriorhodopsin with 7-fs impulsive vibrational spectroscopy. J Am Chem Soc 129:537–546

    Article  PubMed  CAS  Google Scholar 

  • Kelly M, Norgård S, Liaaen-Jensen S (1970) Bacterial carotenoids. 31. C50-carotenoids 5. Carotenoids of Halobacterium salinarium, especially bacterioruberin. Acta Chem Scand 24:2169–2182

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi T, Saito T, Ohtani H (2001) Real-time spectroscopy of transition states in bacteriorhodopsin during retinal isomerization. Nature 414:531–534

    Article  PubMed  CAS  Google Scholar 

  • Kochendoerfer GG, Mathies RA (1995) Ultrafast spectroscopy of rhodopsins-photochemistry at its best. Isr J Chem 35:211–226

    CAS  Google Scholar 

  • Kottemann M, Kish A, Iloanusi C, Bjork S, DiRuggiero J (2005) Physiological responses of the halophilic archaeon Halobacterium sp. strain NRC1 to desiccation and gamma irradiation. Extremophiles 9:219–227

    Google Scholar 

  • Köcher S, Breitenbach J, Müller V, Sandmann G (2009) Structure, function and biosynthesis of carotenoids in the moderately halophilic bacterium Halobacillus halophilus. Arch Microbiol 191:95–104

    Article  PubMed  Google Scholar 

  • Krubasik P, Takaichi S, Maoka T, Kobayashi M, Masamoto K, Sandmann G (2001) Detailed biosynthetic pathway to decaprenoxanthin diglucoside in Corynebacterium glutamicum and identification of novel intermediates. Arch Microbiol 176:217–223

    Article  PubMed  CAS  Google Scholar 

  • Lanyi JK, Schobert B (2004) Local-global conformational coupling in a heptahelical membrane protein: transport mechanism from crystal structures of the nine states in the bacteriorhodopsin photocycle. Biochemistry 43:3–8

    Article  PubMed  CAS  Google Scholar 

  • Lazrak T, Milon A, Wolff G, Albrecht AM, Miehe M, Ourisson G, Nakatani Y (1987) Comparison of the effects of inserted C40- and C50-terminally dihydroxylated carotenoids on the mechanical properties of various phospholipid vesicles. Biochim Biophys Acta 903:132–141

    Article  PubMed  CAS  Google Scholar 

  • Lutnæs BF, Oren A, Liaaen-Jensen S (2002) New C(40)-carotenoid acyl glycoside as principal carotenoid in Salinibacter ruber, an extremely halophilic eubacterium. J Nat Prod 65:1340–1343

    Article  PubMed  Google Scholar 

  • Marshall JH, Wilmoth GJ (1981) Pigments of Staphylococcus aureus, a series of triterpenoid carotenoids. J Bacteriol 147:900–913

    PubMed  CAS  Google Scholar 

  • Mathies RA, Lin SW, Ames JB, Pollard WT (1991) From femtoseconds to biology: mechanism of bacteriorhodopsin’s light-driven proton pump. Annu Rev Biophys Biophys Chem 20:491–518

    Article  PubMed  CAS  Google Scholar 

  • Müller V, Saum SH (2005) The chloride regulon of Halobacillus halophilus: a novel regulatory network for salt perception and signal transduction in bacteria. In: Gunde-Cimerman N, Oren A, Plemenitaš A (eds) Adaptation to life at high salt concentrations in Archaea, Bacteria, and Eukarya. Springer, Dordrecht, pp 303–310

    Google Scholar 

  • Okulski W, Sujak A, Gruszecki WI (2000) Dipalmitoylphosphatidylcholine membranes modified with zeaxanthin: numeric study of membrane organisation. Biochim Biophys Acta 1509: 216–228

    Google Scholar 

  • Oren A (2002) Diversity of halophilic microorganisms: environments, phylogeny, physiology, and applications. J Ind Microbiol Biotechnol 28:56–63

    PubMed  CAS  Google Scholar 

  • Osawa A, Ishii Y, Sasamura N, Morita M, Köcher S, Müller V, Sandmann G, Shindo K (2010) Hydroxy-3,4-dehydro-apo-8′-lycopene and methyl hydroxy-3,4-dehydro-apo-8′-lycopenoate, novel C(30) carotenoids produced by a mutant of marine bacterium Halobacillus halophilus. J Antibiot (Tokyo) 63:291–295

    CAS  Google Scholar 

  • Rodriguez-Valera F, Nieto JJ, Ruiz-Berraquero F (1983) Light as an energy source in continuous cultures of bacteriorhodopsin-containing halobacteria. Appl Environ Microbiol 45:868–871

    PubMed  CAS  Google Scholar 

  • Roeßler M, Müller V (1998) Quantitative and physiological analyses of chloride dependence of growth of Halobacillus halophilus. Appl Environ Microbiol 64:3813–3817

    PubMed  Google Scholar 

  • Roeßler M, Müller V (2001) Chloride dependence of glycine betaine transport in Halobacillus halophilus. FEBS Lett 489:125–128

    Article  PubMed  Google Scholar 

  • Rottem S, Markowitz O (1979) Carotenoids acts as reinforcers of the Acholeplasma laidlawii lipid bilayer. J Bacteriol 140:944–948

    PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Saito T, Miyabe Y, Ide H, Yamamoto O (1997) Hydroxyl radical scavenging ability of bacterioruberin. Radiat Phys Chem 50:267–269

    Article  CAS  Google Scholar 

  • Sandmann G, Fraser PD (1993) Differential inhibition of phytoene desaturases from diverse origins and analysis of resistant cyanobacterial mutants. Z Naturforsch C 48c:307–311

    Google Scholar 

  • Saum SH, Müller V (2007) Salinity-dependent switching of osmolyte strategies in a moderately halophilic bacterium: glutamate induces proline biosynthesis in Halobacillus halophilus. J Bacteriol 189:6968–6975

    Article  PubMed  CAS  Google Scholar 

  • Saum SH, Müller V (2008a) Growth phase-dependent switch in osmolyte strategy in a moderate halophile: ectoine is a minor osmolyte but major stationary phase solute in Halobacillus halophilus. Environ Microbiol 10:716–726

    Article  PubMed  CAS  Google Scholar 

  • Saum SH, Müller V (2008b) Regulation of osmoadaptation in the moderate halophile Halobacillus halophilus: chloride, glutamate and switching osmolyte strategies. Saline Systems 4:4

    Article  PubMed  Google Scholar 

  • Saum SH, Sydow JF, Palm P, Pfeiffer F, Oesterhelt D, Müller V (2006) Biochemical and molecular characterization of the biosynthesis of glutamine and glutamate, two major compatible solutes in the moderately halophilic bacterium Halobacillus halophilus. J Bacteriol 188:6808–6815

    Article  PubMed  CAS  Google Scholar 

  • 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 (Tokyo) 39:251–262

    Article  CAS  Google Scholar 

  • Sharkov AV, Matveets Iu A, Chekalin SV, Pakulev AV (1985) Subpicosecond spectroscopy of bacteriorhodopsin. Dokl Akad Nauk SSSR 281:466–470

    PubMed  CAS  Google Scholar 

  • Shimidzu N, Goto M, Miki W (1996) Carotenoids as singlet oxygen quenchers in marine organisms. Fish Sci 62:134–137

    CAS  Google Scholar 

  • Shindo K, Kikuta K, Suzuki A, Katsuta A, Kasai H, Yasumoto-Hirose M, Matsuo Y, Misawa N, Takaichi S (2007) Rare carotenoids, (3R)-saproxanthin and (3R,2′S)-myxol, isolated from novel marine bacteria (Flavobacteriaceae) and their antioxidative activities. Appl Microbiol Biotechnol 74:1350–1357

    Article  PubMed  CAS  Google Scholar 

  • Shindo K, Endo M, Miyake Y, Wakasugi K, Morritt D, Fraser PD, Kasai H, Misawa N (2008) Methyl glucosyl-3,4-dehydro-apo-8′-lycopenoate, a novel antioxidative glyco-C(30)-carotenoic acid produced by a marine bacterium Planococcus maritimus. J Antibiot (Tokyo) 61:729–735

    CAS  Google Scholar 

  • Sies H, Mehlhorn R (1986) Mutagenicity of nitroxide-free radicals. Arch Biochem Biophys 251:393–396

    Article  PubMed  CAS  Google Scholar 

  • Spring S, Ludwig W, Marquez MC, Ventosa A, Schleifer K-H (1996) Halobacillus gen. nov., with descriptions of Halobacillus litoralis sp. nov. and Halobacilus trueperi sp. nov., and transfer of Sporosarcina halophila to Halobacillus halophilus comb. nov. Int J Syst Bacteriol 46:492–496

    Article  Google Scholar 

  • Straub O (1987) Key of carotenoids. Birkhäuser Verlag, Basel

    Google Scholar 

  • Strzalka K, Gruszecki WI (1994) Effect of β-carotene on structural and dynamic properties of model phosphatidylcholine membranes. I. An EPR spin label study. Biochim Biophys Acta 1194:138–142

    Article  PubMed  CAS  Google Scholar 

  • Subczynski WK, Markowska E, Gruszecki WI, Sielewiesiuk J (1992) Effects of polar carotenoids on dimyristoylphosphatidylcholine membranes: a spin-label study. Biochim Biophys Acta 1105:97–108

    Article  PubMed  CAS  Google Scholar 

  • Subczynski WK, Markowska E, Sielewiesiuk J (1993) Spin-label studies on phosphatidylcholine-polar carotenoid membranes: effects of alkyl-chain length and unsaturation. Biochim Biophys Acta 1150:173–181

    Article  PubMed  CAS  Google Scholar 

  • Subramaniam S, Hirai T, Henderson R (2002) From structure to mechanism: electron crystallographic studies of bacteriorhodopsin. Philos Transact A Math Phys Eng Sci 360:859–874

    Article  PubMed  CAS  Google Scholar 

  • Sujak A, Okulski W, Gruszecki WI (2000) Organization of xanthophyll pigments lutein and zeaxanthin in lipid membranes formed with dipalmitoylphosphatidylcholine. Biochim Biophys Acta 1509:255–263

    Google Scholar 

  • Takaichi S, Inoue K, Akaike M, Kobayashi M, Oh-oka H, Madigan MT (1997) The major carotenoid in all known species of Heliobacteria is the C30 carotenoid 4,4′-diaponeurosporene, not neurosporene. Arch Microbiol 168:277–281

    Article  PubMed  CAS  Google Scholar 

  • Takaichi S, Maoka T, Akimoto N, Carmona ML, Yamaoka Y (2008) Carotenoids in a Corynebacterineae, Gordonia terrae AIST-1: carotenoid glucosyl mycoloyl esters. Biosci Biotechnol Biochem 72:2615–2622

    Article  PubMed  CAS  Google Scholar 

  • Takano H, Obitsu S, Beppu T, Ueda K (2005) Light-induced carotenogenesis in Streptomyces coelicolor A3(2): identification of an extracytoplasmic function sigma factor that directs photodependent transcription of the carotenoid biosynthesis gene cluster. J Bacteriol 187:1825–1832

    Article  PubMed  CAS  Google Scholar 

  • Tao L, Schenzle A, Odom JM, Cheng Q (2005) Novel carotenoid oxidase involved in biosynthesis of 4,4′-diapolycopene dialdehyde. Appl Environ Microbiol 71:3294–3301

    Article  PubMed  CAS  Google Scholar 

  • Turner M, Jervis DI (1963) The distribution of pigmented Bacillus species in saltmarsh and other saline and non-saline soils. Nova Hedwig 16:293–298

    Google Scholar 

  • Yokoyama A, Sandmann G, Hoshino T, Adachi K, Sakai M, Shizuri Y (1995) Thermozeaxanthin, new carotenoid-glycoside-esters from thermophilic eubacterium Thermus thermophilus. Tetrahedron Lett 36:4901–4904

    CAS  Google Scholar 

  • Yokoyama A, Shizuri Y, Hoshino T, Sandmann G (1996a) Thermocryptoxanthins: novel intermediates in the carotenoid biosynthetic pathway of Thermus thermophilus. Arch Microbiol 165:342–345

    Article  PubMed  CAS  Google Scholar 

  • Yokoyama A, Miki W, Izumida H, Shizuri Y (1996b) New trihydroxy-keto-carotenoids isolated from an astaxanthin-producing marine bacterium. Biosci Biotechnol Biochem 60:200–203

    Article  CAS  Google Scholar 

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Acknowledgment

Work from the authors’ laboratory was supported by a fellowship from the Marianne and Dr. Fritz Walter Fisher-Stiftung to Saskia Köcher and by a grant from the Deutsche Forschungsgemeinschaft.

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Authors and Affiliations

  1. Molecular Microbiology & Bioenergetics, Institute of Molecular Biosciences, Johann Wolfgang Goethe University Frankfurt, Max-von-Laue-Strasse 9, 60438, Frankfurt am Main, Germany

    Saskia Köcher & Volker Müller

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  1. Saskia Köcher
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  2. Volker Müller
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Correspondence to Volker Müller .

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Editors and Affiliations

  1. Faculty of Pharmacy, Department of Microbiology, University of Sevilla, Profesor García González 2, Sevilla, 41012, Spain

    Antonio Ventosa

  2. The Institute of Life Sciences, Department of Plant and Environmental Sc, The Hebrew University of Jerusalem, Jerusalem, 91904, Israel

    Aharon Oren

  3. , Insitute of Microbiology, Chinese Academy of Sciences, Beichen West Road 1, Beijing, China, People's Republic

    Yanhe Ma

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Köcher, S., Müller, V. (2011). The Nature and Function of Carotenoids in the Moderately Halophilic Bacterium Halobacillus halophilus . In: Ventosa, A., Oren, A., Ma, Y. (eds) Halophiles and Hypersaline Environments. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-20198-1_16

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