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Volume 165, Issue 4

Apocarotenoids produced from β-carotene by dioxygenases from Mucor circinelloides Free

Abstract

Mucor circinelloides exhibits the complex sexual behaviour that is induced in other Mucoromycotina by a family of apocarotenoids called trisporoids. The genome of M. circinelloides contains four genes encoding putative carotenoid cleavage dioxygenases. The gene products of two of them were sufficient to convert β-carotene into the precursors of three families of apocarotenoids, both in vitro and in the Escherichia coli heterologous in vivo system. The first of these products, CarS, cleaved the C40 β-carotene into the C15 precursor of cyclofarnesoids and a C25 apocarotenal that was converted by the second enzyme, AcaA, into the C18 precursor of trisporoids and the C7 precursor of methylhexanoids. Apocarotenoids were not found in single or mixed cultures of the two strains of opposite sex, whose interaction readily produced zygospores, the sexual fusion cells.

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Keyword(s): apocarotenoids , carotenoid cleavage oxygenases , carotenoids , Mucor , sexual interactions and trisporoids
© 2019 The Authors
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2019-02-14
2024-04-20
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References

  1. Michelius PA. Nova Plantarum Genera Florentia: Typis Bernardi Paperinii; 1729
     [Google Scholar]
  2. Hoffmann K, Pawłowska J, Walther G, Wrzosek M, de Hoog GS et al. The family structure of the Mucorales: a synoptic revision based on comprehensive multigene-genealogies. Persoonia 2013; 30:57–76 [View Article][PubMed]
     [Google Scholar]
  3. van TP. Nouvelles recherches sur les Mucorinées. Ann des Sci Nat Bot 1875; 6:5–175
     [Google Scholar]
  4. Nicolás FE, Navarro-Mendoza MI, Pérez-Arques C, López-García S, Navarro E et al. Molecular tools for carotenogenesis analysis in the mucoral Mucor circinelloides. Methods Mol Biol 2018; 1852:221–237 [View Article][PubMed]
     [Google Scholar]
  5. van HR, Roncero MIG. High frequency transformation of Mucor with recombinant plasmid DNA. Carlsberg Res Commun 1984; 49:691–702
     [Google Scholar]
  6. Nyilasi I, Acs K, Papp T, Nagy E, Vágvölgyi C. Agrobacterium tumefaciens-mediated transformation of Mucor circinelloides. Folia Microbiol 2005; 50:415–420 [View Article][PubMed]
     [Google Scholar]
  7. Gutiérrez A, López-García S, Garre V. High reliability transformation of the basal fungus Mucor circinelloides by electroporation. J Microbiol Methods 2011; 84:442–446 [View Article][PubMed]
     [Google Scholar]
  8. Navarro E, Lorca-Pascual JM, Quiles-Rosillo MD, Nicolás FE, Garre V et al. A negative regulator of light-inducible carotenogenesis in Mucor circinelloides. Mol Genet Genomics 2001; 266:463–470 [View Article][PubMed]
     [Google Scholar]
  9. Ruiz-Vázquez RM, Nicolás FE, Torres-Martínez S, Garre V. Distinct RNAi pathways in the regulation of physiology and development in the fungus Mucor circinelloides. Adv Genet 2015; 91:55–102 [View Article][PubMed]
     [Google Scholar]
  10. Nicolás FE, Garre V. RNA Interference in Fungi: Retention and Loss. Microbiol Spectr 2016; 4:657–671
     [Google Scholar]
  11. Li CH, Cervantes M, Springer DJ, Boekhout T, Ruiz-Vazquez RM et al. Sporangiospore size dimorphism is linked to virulence of Mucor circinelloides. PLoS Pathog 2011; 7:e1002086 [View Article][PubMed]
     [Google Scholar]
  12. Burgeff H. Untersuchungen über Sexualität und Parasitismus bei Mucorineen. Bot Abh 1924; 4:1–135
     [Google Scholar]
  13. Austin DG, Bu'lock JD, Winstanley DJ. Trisporic acid biosynthesis and carotenogenesis in Blakesleea trispora. Biochem J 1969; 113:34P [View Article]
     [Google Scholar]
  14. Sutter RP. Mutations affecting sexual development in Phycomyces blakesleeanus. Proc Natl Acad Sci USA 1975; 72:127–130 [View Article][PubMed]
     [Google Scholar]
  15. Caglioti L, Cainelli G, Camerino B, Mondelli R, Prieto A et al. The structure of trisporic-C acid. Tetrahedron 1966; 22:175–187 [View Article]
     [Google Scholar]
  16. Sutter RP. Sexual development. In Cerdá-Olmedo E, Lipson ED. (editors) Phycomyces Cold Spring Harbor, New York: Cold Spring Harbor Laboratory; 1987 pp. 317–336
     [Google Scholar]
  17. Govind NS, Cerda-Olmedo E. Sexual activation of carotenogenesis in phycomyces blakesleeanus. Microbiology 1986; 132:2775–2780 [View Article]
     [Google Scholar]
  18. Schimek C, Kleppe K, Saleem AR, Voigt K, Burmester A et al. Sexual reactions in Mortierellales are mediated by the trisporic acid system. Mycol Res 2003; 107:736–747 [View Article][PubMed]
     [Google Scholar]
  19. Sahadevan Y, Richter-Fecken M, Kaerger K, Voigt K, Boland W. Early and late trisporoids differentially regulate β-carotene production and gene transcript levels in the mucoralean fungi Blakeslea trispora and Mucor mucedo. Appl Environ Microbiol 2013; 79:7466–7475 [View Article][PubMed]
     [Google Scholar]
  20. Polaino S, Herrador MM, Cerdá-Olmedo E, Barrero AF. Splitting of beta-carotene in the sexual interaction of Phycomyces. Org Biomol Chem 2010; 8:4229–4231 [View Article][PubMed]
     [Google Scholar]
  21. Polaino S, Gonzalez-Delgado JA, Arteaga P, Herrador MM, Barrero AF et al. Apocarotenoids in the sexual interaction of Phycomyces blakesleeanus. Org Biomol Chem 2012; 10:3002 [View Article][PubMed]
     [Google Scholar]
  22. Alcalde E, Medina HR, Herrador MM, Barrero AF, Cerdá-Olmedo E. Cyclofarnesoids and methylhexanoids produced from β-carotene in Phycomyces blakesleeanus. Phytochemistry 2016; 124:38–45 [View Article][PubMed]
     [Google Scholar]
  23. Medina HR, Cerdá-Olmedo E, Al-Babili S. Cleavage oxygenases for the biosynthesis of trisporoids and other apocarotenoids in Phycomyces. Mol Microbiol 2011; 82:199–208 [View Article][PubMed]
     [Google Scholar]
  24. Tagua VG, Medina HR, Martín-Domínguez R, Eslava AP, Corrochano LM et al. A gene for carotene cleavage required for pheromone biosynthesis and carotene regulation in the fungus Phycomyces blakesleeanus. Fungal Genet Biol 2012; 49:398–404 [View Article][PubMed]
     [Google Scholar]
  25. Barrero AF, Herrador MM, Arteaga P, Gil J, González JA et al. New apocarotenoids and β-carotene cleavage in Blakeslea trispora. Org Biomol Chem 2011; 9:7190–7195 [View Article][PubMed]
     [Google Scholar]
  26. Sui X, Kiser PD, Lintig J, Palczewski K. Structural basis of carotenoid cleavage: from bacteria to mammals. Arch Biochem Biophys 2013; 539:203–213 [View Article][PubMed]
     [Google Scholar]
  27. Ahrazem O, Gómez-Gómez L, Rodrigo MJ, Avalos J, Limón MC. Carotenoid cleavage oxygenases from microbes and photosynthetic organisms: features and functions. Int J Mol Sci 2016; 17:1781 [View Article][PubMed]
     [Google Scholar]
  28. Corrochano LM, Kuo A, Marcet-Houben M, Polaino S, Salamov A et al. Expansion of signal transduction pathways in fungi by extensive genome duplication. Curr Biol 2016; 26:1577–1584 [View Article][PubMed]
     [Google Scholar]
  29. Poliakov E, Gentleman S, Cunningham FX, Miller-Ihli NJ, Redmond TM. Key role of conserved histidines in recombinant mouse beta-carotene 15,15'-monooxygenase-1 activity. J Biol Chem 2005; 280:29217–29223 [View Article][PubMed]
     [Google Scholar]
  30. Takahashi Y, Moiseyev G, Chen Y, Ma JX. Identification of conserved histidines and glutamic acid as key residues for isomerohydrolase activity of RPE65, an enzyme of the visual cycle in the retinal pigment epithelium. FEBS Lett 2005; 579:5414–5418 [View Article][PubMed]
     [Google Scholar]
  31. Hundle B, Alberti M, Nievelstein V, Beyer P, Kleinig H et al. Functional assignment of Erwinia herbicola Eho10 carotenoid genes expressed in Escherichia coli. Mol Gen Genet 1994; 245:406–416 [View Article][PubMed]
     [Google Scholar]
  32. Prado-Cabrero A, Scherzinger D, Avalos J, Al-Babili S. Retinal biosynthesis in fungi: characterization of the carotenoid oxygenase CarX from Fusarium fujikuroi. Eukaryot Cell 2007; 6:650–657 [View Article][PubMed]
     [Google Scholar]
  33. Estrada AF, Maier D, Scherzinger D, Avalos J, Al-Babili S. Novel apocarotenoid intermediates in Neurospora crassa mutants imply a new biosynthetic reaction sequence leading to neurosporaxanthin formation. Fungal Genet Biol 2008; 45:1497–1505 [View Article][PubMed]
     [Google Scholar]
  34. Rodríguez-Romero J, Corrochano LM. Regulation by blue light and heat shock of gene transcription in the fungus Phycomyces: proteins required for photoinduction and mechanism for adaptation to light. Mol Microbiol 2006; 61:1049–1059 [View Article]
     [Google Scholar]
  35. Scherzinger D, Al-Babili S. In vitro characterization of a carotenoid cleavage dioxygenase from Nostoc sp. PCC 7120 reveals a novel cleavage pattern, cytosolic localization and induction by highlight. Mol Microbiol 2008; 69:231–244 [View Article][PubMed]
     [Google Scholar]
  36. Lavallie ER, Diblasio EA, Kovacic S, Grant KL, Schendel PF et al. A thioredoxin gene fusion expression system that circumvents inclusion body formation in the E. coli cytoplasm. Biotechnology 1993; 11:187–193[PubMed]
     [Google Scholar]
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Apocarotenoids produced from β-carotene by dioxygenases from Mucor circinelloides
Microbiology 165, 433 (2019); https://doi.org/10.1099/mic.0.000762
/content/journal/micro/10.1099/mic.0.000762
/content/journal/micro/10.1099/mic.0.000762
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