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The astaxanthin dideoxyglycoside biosynthesis pathway in Sphingomonas sp. PB304

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Abstract

A major carotenoid in Sphingomonas sp. PB304, originally isolated from a river in Daejon City, South Korea, was identified as astaxanthin dideoxyglycoside. Gene clusters encoding the astaxanthin dideoxyglycoside biosynthetic enzymes were identified by screening Sphingomonas sp. PB304 fosmid libraries using degenerate probes that harbor highly conserved sequences from the Sphigomonas elodea-derived crtI and Nostoc sp. PCC 7120-dervied crtW genes. Selected positive gene clusters were fully sequenced and annotated, revealing genes encoding six putative carotenogenic enzymes: phytoene synthase (CrtB), phytoene desaturase (CrtI), lycopene cyclase (CrtY), carotene hydroxylase (CrtZ), carotene ketolase (CrtW), and glycosyltransferase (CrtX). All of the carotenogenic enzymes, except for CrtX, were functional in the recombinant host Escherichia coli expressing synthetic carotenogenic modules from Pantoea agglomerans. CrtX did not take up UDP-glucose or GDP-fucose as sugar substrates during the in vitro reaction. Although no direct experimental evidence was obtained for the function of Sphingomonas sp. PB304 CrtX, it can be categorized as a putative deoxyglycosyltransferase based on the presence of astaxanthin dideoxyglycoside in Sphingomonas sp. PB304, a putative corresponding gene in the carotenoid biosynthetic gene cluster, and high amino acid sequence homology to the existing glycosyltransferases. Therefore, we propose that astaxanthin dideoxyglycoside can be synthesized in Sphingomonas sp. PB304 via sequential reactions of six pathway enzymes, including CrtX on the phytoene intermediate.

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References

  • An G, Schuman DB, Johnson EA (1989) Isolation of Phaffia rhodozyma mutants with increased astaxanthin content. Appl Environ Microbiol 55:116–124

    CAS  PubMed Central  PubMed  Google Scholar 

  • Asker D, Beppu T, Ueda K (2007a) Sphingomonas astaxanthinifaciens sp. nov., a novel astaxanthin-producing bacterium of the family Sphingomonadaceae isolated from Misasa, Tottori, Japan. FEMS Microbiol Lett 273:140–148

    Article  CAS  PubMed  Google Scholar 

  • Asker D, Beppu T, Ueda K (2007b) Unique diversity of carotenoid-producing bacteria isolated from Misasa, a radioactive site in Japan. Appl Microbiol Biotechnol 77:383–392

    Article  CAS  PubMed  Google Scholar 

  • Asker D, Amano SI, Morita K, Tamura K, Sakuda S, Kikuchi N, Furihata K, Matsufuji H, Beppu T, Ueda K (2009) Astaxanthin dirhamnoside, a new astaxanthin derivative produced by a radio-tolerant bacterium, Sphingomonas astaxanthinifaciens. J Antibiot 62:397–399

    Article  CAS  PubMed  Google Scholar 

  • Britton G (1995) Structure and properties of carotenoids in relation to function. FASEB J 9:1551–1558

    CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Dembitsky VM (2005) Astonishing diversity of natural surfactants: 3. Carotenoid glycosides and isoprenoid glycolipids. Lipids 40:535–557

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Graham JE, Bryant DA (2009) The biosynthetic pathway for myxol-2′ fucoside (myxoxanthophyll) in the cyanobacterium Synechococcus sp. strain PCC 7002. J Bacteriol 191:3292–3300

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Heider SAE, Peters-Wendisch P, Netzer R, Stafnes M, Brautaset T, Wendisch VF (2014) Production and glucosylation of C50 and C40 carotenoids by metabolically engineered Corynebacterium glutamicum. Appl Microbiol Biotechnol 98:1223–1235

    Article  CAS  PubMed  Google Scholar 

  • Hundle BS, O’Brien DA, Alberti M, Beyer P, Hearst JE (1992) Functional expression of zeaxanthin glucosyltransferase from Erwinia herbicola and a proposed uridine diphosphate binding site. Proc Natl Acad Sci U S A 89:9321–9325

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. Academic, New York, pp 21–132

    Google Scholar 

  • Kakirde KS, Parsley LC, Liles MR (2010) Size does matter: application-driven approaches for soil metagenomics. Soil Biol Biochem 42:1911–1923

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kim SH, Lee PC (2012) Functional expression and extension of staphylococcal staphyloxanthin biosynthetic pathway in Escherichia coli. J Biol Chem 287:21575–21583

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kim SH, Park YH, Schmidt-Dannert C, Lee PC (2010) Redesign, reconstruction, and directed extension of the Brevibacterium linens C40 carotenoid pathway in Escherichia coli. Appl Environ Microbiol 76:5199–5206

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park SC, Jeon YS, Lee JH, Yi H, Won S, Chun J (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721

    Article  CAS  PubMed  Google Scholar 

  • Krubasik P, Sandmann G (2000) A carotenogenic gene cluster from Brevibacterium linens with novel lycopene cyclase genes involved in the synthesis of aromatic carotenoids. Mol Gen Genet 263:423–432

    Article  CAS  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  CAS  PubMed  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Lee PC, Schmidt-Dannert C (2002) Metabolic engineering towards biotechnological production of carotenoids in microorganisms. Appl Microbiol Biotechnol 60:1–11

    Article  CAS  PubMed  Google Scholar 

  • Lee PC, Momen AZR, Mijts BN, Schmidt-Dannert C (2003) Biosynthesis of structurally novel carotenoids in Escherichia coli. Chem Biol 10:453–462

    Article  CAS  PubMed  Google Scholar 

  • Maresca JA, Bryant DA (2006) Two genes encoding new carotenoid-modifying enzymes in the green sulfur bacterium Chlorobium tepidum. J Bacteriol 188:6217–6223

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Misawa N, Nakagawa M, Kobayashi K, Yamano S, Izawa Y, Nakamura K, Harashima K (1990) Elucidation of the Erwinia uredovora carotenoid biosynthetic pathway by functional analysis of gene products expressed in Escherichia coli. J Bacteriol 172:6704–6712

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mohamed HE, van de Meene AML, Roberson RW, Vermaas WFJ (2005) Myxoxanthophyll is required for normal cell wall structure and thylakoid organization in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 187:6883–6892

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Moraga AR, Nohales PF, Pérez JAF, Gómez-Gómez L (2004) Glucosylation of the saffron apocarotenoid crocetin by a glucosyltransferase isolated from Crocus sativus stigmas. Planta 219:955–966

    Article  CAS  PubMed  Google Scholar 

  • Netzer R, Stafsnes MH, Andreassen T, Goksøyr A, Bruheim P, Brautaset T (2010) Biosynthetic pathway for γ-cyclic sarcinaxanthin in micrococcus luteus: heterologous expression and evidence for diverse and multiple catalytic functions of C50 carotenoid cyclases. J Bacteriol 192:5688–5699

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nishino H, Murakoshi M, Tokuda H, Satomi Y (2009) Cancer prevention by carotenoids. Arch Biochem Biophys 483:165–168

    Article  CAS  PubMed  Google Scholar 

  • Oh H-M, Kang I, Vergin KL, Kang D, Rhee K-H, Giovannoni SJ, Cho JC (2011) Complete genome sequence of strain HTCC2503T of Parvularcula bermudensis, the type species of the order “Parvularculales” in the class alphaproteobacteria. J Bacteriol 193:305–306

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pelz A, Wieland KP, Putzbach K, Hentschel P, Albert K, Götz F (2005) Structure and biosynthesis of staphyloxanthin from Staphylococcus aureus. J Biol Chem 280:32493–32498

    Article  CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Schmidt EW, Nelson JT, Rasko DA, Sudek S, Eisen JA, Haygood MG, Ravel J (2005) Patellamide A and C biosynthesis by a microcin-like pathway in Prochloron didemni, the cyanobacterial symbiont of Lissoclinum patella. Proc Natl Acad Sci U S A 102:7315–7320

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Seo YB, Choi SS, Nam SW, Lee JH, Kim YT (2009) Cloning and characterization of the zeaxanthin glucosyltransferase gene (crtX) from the astaxanthin-producing marine bacterium, Paracoccus haeundaensis. J Microbiol Biotechnol 19:1542–1546

    Article  CAS  PubMed  Google Scholar 

  • Shumskaya M, Wurtzel ET (2013) The carotenoid biosynthetic pathway: thinking in all dimensions. Plant Sci 208:58–63

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Song GH, Kim SH, Choi BH, Han SJ, Lee PC (2013) Heterologous carotenoid-biosynthetic enzymes: functional complementation and effects on carotenoid profiles in Escherichia coli. Appl Environ Microbiol 79:610–618

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Takaichi S, Mochimaru M (2007) Carotenoids and carotenogenesis in cyanobacteria: unique ketocarotenoids and carotenoid glycosides. Cell Mol Life Sci 64:2607–2619

    Article  CAS  PubMed  Google Scholar 

  • Takaichi S, Maoka T, Takasaki K, Hanada S (2010) Carotenoids of Gemmatimonas aurantiaca (Gemmatimonadetes): identification of a novel carotenoid, deoxyoscillol 2-rhamnoside, and proposed biosynthetic pathway of oscillol 2,2′-dirhamnoside. Microbiology 156:757–763

    Article  CAS  PubMed  Google Scholar 

  • Takeuchi M, Hamana K, Hiraishi A (2001) Proposal of the genus Sphingomonas sensu stricto and three new genera, Sphingobium, Novosphingobium and Sphingopyxis, on the basis of phylogenetic and chemotaxonomic analyses. Int J Syst Evol Microbiol 51:1405–1417

    CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  Google Scholar 

  • Tao L, Yao H, Cheng Q (2007) Genes from a Dietzia sp. for synthesis of C40 and C50 β-cyclic carotenoids. Gene 386:90–97

    Article  CAS  PubMed  Google Scholar 

  • Walter MH, Strack D (2011) Carotenoids and their cleavage products: biosynthesis and functions. Nat Prod Rep 28:663–692

    Article  CAS  PubMed  Google Scholar 

  • Yabuuchi E, Yano I, Oyaizu H, Hashimoto Y, Ezaki T, Yamamoto H (1990) Proposals of Sphingomonas paucimobilis gen. nov. and comb. nov., Sphingomonas parapaucimobilis sp. nov., Sphingomonas yanoikuyae sp. nov., Sphingomonas adhaesiva sp. nov., Sphingomonas capsulata comb. nov., and two genospecies of the genus Sphingomonas. Microbiol Immunol 34:99–119

    Article  CAS  PubMed  Google Scholar 

  • Yi T, Han CK, Srinivasan S, Lee K, Kim M (2010) Sphingomonas humi sp. nov., isolated from soil. J Microbiol 48:165–169

    Article  PubMed  Google Scholar 

  • Zhu L, Wu X, Li O, Chen Y, Qian C, Teng Y, Tao X, Gao H (2011) Cloning and knockout of phytoene desaturase gene in Sphingomonas elodea ATCC 31461 for economic recovery of gellan gum. J Ind Microbiol Biotechnol 38:1507–1513

    Article  CAS  PubMed  Google Scholar 

  • Zhu L, Wu X, Li O, Qian C, Gao H (2012) Cloning and characterization of genes involved in nostoxanthin biosynthesis of Sphingomonas elodea ATCC 31461. PLoS One 7:e35099. doi:10.1371/journal.pone.0035099

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

Sphingomonas sp. PB304 was kindly provided by Prof. Kyung-Ho Kim. This work was supported by the National Research Foundation of Korea grants funded by the Korean Government (2014029244; NRF-2013R1A1A2007127).

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The authors have no conflict of interest to declare.

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Correspondence to Pyung Cheon Lee.

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Kim, S.H., Kim, J.H., Lee, B.Y. et al. The astaxanthin dideoxyglycoside biosynthesis pathway in Sphingomonas sp. PB304. Appl Microbiol Biotechnol 98, 9993–10003 (2014). https://doi.org/10.1007/s00253-014-6050-7

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