1887

Abstract

Sixteen yeasts with sequenced genomes belonging to the ascomycete subphyla Saccharomycotina and Taphrinomycotina were assayed for their ability to utilize a variety of primary, secondary, tertiary and quartenary aliphatic amines as nitrogen sources. The results support a previously proposed pathway of quaternary amine catabolism whereby glycine betaine is first converted into choline, which is then cleaved to release trimethylamine, followed by stepwise demethylation of trimethylamine to release free ammonia. There were only a few instances of utilization of -methylated glycine species (sarcosine and ,-dimethylglycine), which suggests that this pathway is not intact in any of the species tested. The ability to utilize choline as a sole nitrogen source correlated strongly with the presence of a putative Rieske non-haem iron protein homologous to bacterial ring-hydroxylating oxygenases and plant choline monooxygenases. Deletion of the gene encoding the Rieske non-haem iron protein in the yeast abolished its ability to utilize choline as the sole nitrogen source, but did not affect its ability to use methylamine, dimethylamine, trimethylamine, ethylamine, diethylamine, ethanolamine or glycine as nitrogen sources. The gene was named for putative choline monooxygenase 1. A bioinformatic survey of eukaryotic genomes showed that homologues are found throughout the eukaryotic domain.

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2014-05-01
2020-01-21
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References

  1. Brady B. L..( 1965;). Utilization of amino compounds by yeasts of the genus Saccharomyces.. Antonie van Leeuwenhoek31:95–102 [CrossRef][PubMed]
    [Google Scholar]
  2. Dabrowa N., Howard D. H..( 1981;). Proline uptake in Candida albicans.. J Gen Microbiol127:391–397[PubMed]
    [Google Scholar]
  3. Dohmen R. J., Strasser A. W., Höner C. B., Hollenberg C. P..( 1991;). An efficient transformation procedure enabling long-term storage of competent cells of various yeast genera. Yeast7:691–692 [CrossRef][PubMed]
    [Google Scholar]
  4. Fattakhova A. N., Ofitserov E. N., Garusov A. V..( 1991;). Cytochrome P-450-dependent catabolism of triethanolamine in Rhodotorula mucilaginosa.. Biodegradation2:107–113 [CrossRef][PubMed]
    [Google Scholar]
  5. Frisell W. R., MacKenzie C. G..( 1962;). Separation and purification of sarcosine dehydrogenase and dimethylglycine dehydrogenase. J Biol Chem237:94–98[PubMed]
    [Google Scholar]
  6. Green J., Large P. J..( 1983;). Oxidation of dimethylamine and trimethylamine in methazotrophic yeasts by microsomal mono-oxygenases sensitive to carbon monoxide. Biochem Biophys Res Commun113:900–907 [CrossRef][PubMed]
    [Google Scholar]
  7. Green J., Large P. J..( 1984;). Subcellular localization and properties of partially purified dimethylamine and trimethylamine mono-oxygenase activities in Candida utilis.. J Gen Microbiol130:2577–2588[PubMed]
    [Google Scholar]
  8. Green J., Haywood G. W., Large P. J..( 1982;). More than one amine oxidase is involved in the metabolism of primary amines supplied as nitrogen source. J Gen Microbiol128:991–996
    [Google Scholar]
  9. Hagedorn J..( 1990;). Isolierung und charakterisierung von mutanten im xylosestoffwechsel und entwicklung eines transformationssystems für die hefe Pichia stipitis PhD thesis, Heinrich-Heine-Universität Düsseldorf; Düsseldorf, Germany:
    [Google Scholar]
  10. Haywood G. W., Large P. J..( 1981;). Microbial oxidation of amines. Distribution, purification and properties of two primary-amine oxidases from the yeast Candida boidinii grown on amines as sole nitrogen source. Biochem J199:187–201[PubMed]
    [Google Scholar]
  11. Kawaguchi Y., Honda H., Taniguchi-Morimura J., Iwasaki S..( 1989;). The codon CUG is read as serine in an asporogenic yeast Candida cylindracea.. Nature341:164–166 [CrossRef][PubMed]
    [Google Scholar]
  12. Kweon O., Kim S. J., Baek S., Chae J. C., Adjei M. D., Baek D. H., Kim Y. C., Cerniglia C. E..( 2008;). A new classification system for bacterial Rieske non-heme iron aromatic ring-hydroxylating oxygenases. BMC Biochem9:11 [CrossRef][PubMed]
    [Google Scholar]
  13. Laliberté J., Labbé S..( 2006;). Mechanisms of copper loading on the Schizosaccharomyces pombe copper amine oxidase 1 expressed in Saccharomyces cerevisiae.. Microbiology152:2819–2830 [CrossRef][PubMed]
    [Google Scholar]
  14. Lambou K., Pennati A., Valsecchi I., Tada R., Sherman S., Sato H., Beau R., Gadda G., Latgé J. P..( 2013;). Pathway of glycine betaine biosynthesis in Aspergillus fumigatus.. Eukaryot Cell12:853–863 [CrossRef][PubMed]
    [Google Scholar]
  15. Large P. J..( 1986;). Degradation of organic nitrogen compounds by yeasts. Yeast2:1–34 [CrossRef]
    [Google Scholar]
  16. LaRue T. A., Spencer J. F. T..( 1968;). Utilization of organic nitrogen compounds by yeasts of the genus Saccharomyces.. Antonie van Leeuwenhoek34:153–158 [CrossRef][PubMed]
    [Google Scholar]
  17. Lin Z., Zheng J..( 2010;). Occurrence, characteristics, and applications of fructosyl amine oxidases (amadoriases). Appl Microbiol Biotechnol86:1613–1619 [CrossRef][PubMed]
    [Google Scholar]
  18. Linder T..( 2012;). Genomics of alternative sulfur utilization in ascomycetous yeasts. Microbiology158:2585–2597 [CrossRef][PubMed]
    [Google Scholar]
  19. Maassen N., Freese S., Schruff B., Passoth V., Klinner U..( 2008;). Nonhomologous end joining and homologous recombination DNA repair pathways in integration mutagenesis in the xylose-fermenting yeast Pichia stipitis.. FEMS Yeast Res8:735–743 [CrossRef][PubMed]
    [Google Scholar]
  20. Maeda Y., Oki M., Fujii Y., Hatanaka A., Hojo M., Hirano K., Uchida H..( 2008;). Cloning and expression of three formate oxidase genes from Debaryomyces vanrijiae MH201. Biosci Biotechnol Biochem72:1999–2004 [CrossRef][PubMed]
    [Google Scholar]
  21. Magaña-Schwencke N., Kuznar J., Schwencke J..( 1973;). Imino acid transport in yeast: the uptake of sarcosine. Biochim Biophys Acta318:281–288 [CrossRef][PubMed]
    [Google Scholar]
  22. McNeil J. B., Zhang F., Taylor B. V., Sinclair D. A., Pearlman R. E., Bognar A. L..( 1997;). Cloning, and molecular characterization of the GCV1 gene encoding the glycine cleavage T-protein from Saccharomyces cerevisiae.. Gene186:13–20 [CrossRef][PubMed]
    [Google Scholar]
  23. Mori N., Shirakawa K., Uzura K., Kitamoto Y., Ichikawa Y..( 1988;). Formation of ethylene-glycol and trimethylamine from choline by Candida tropicalis.. FEMS Microbiol Lett51:41–44 [CrossRef]
    [Google Scholar]
  24. Neims A. H., Hellerman L..( 1962;). Specificity of the d-amino acid oxidase in relation to glycine oxidase activity. J Biol Chem237:PC976–PC978[PubMed]
    [Google Scholar]
  25. Rathinasabapathi B., Burnet M., Russell B. L., Gage D. A., Liao P. C., Nye G. J., Scott P., Golbeck J. H., Hanson A. D..( 1997;). Choline monooxygenase, an unusual iron-sulfur enzyme catalyzing the first step of glycine betaine synthesis in plants: prosthetic group characterization and cDNA cloning. Proc Natl Acad Sci U S A94:3454–3458 [CrossRef][PubMed]
    [Google Scholar]
  26. Szamecz B., Urbán G., Rubiera R., Kucsera J., Dorgai L..( 2005;). Identification of four alcohol oxidases from methylotrophic yeasts. Yeast22:669–676 [CrossRef][PubMed]
    [Google Scholar]
  27. van der Walt J. P..( 1962;). Utilization of ethylamine by yeasts. Antonie van Leeuwenhoek28:91–96 [CrossRef][PubMed]
    [Google Scholar]
  28. van Dijken J. P., Bos P..( 1981;). Utilization of amines by yeasts. Arch Microbiol128:320–324 [CrossRef][PubMed]
    [Google Scholar]
  29. Villas-Bôas S. G., Åkesson M., Nielsen J..( 2005;). Biosynthesis of glyoxylate from glycine in Saccharomyces cerevisiae.. FEMS Yeast Res5:703–709 [CrossRef][PubMed]
    [Google Scholar]
  30. Wargo M. J..( 2013;). Homeostasis and catabolism of choline and glycine betaine: lessons from Pseudomonas aeruginosa.. Appl Environ Microbiol79:2112–2120 [CrossRef][PubMed]
    [Google Scholar]
  31. Wargo M. J., Szwergold B. S., Hogan D. A..( 2008;). Identification of two gene clusters and a transcriptional regulator required for Pseudomonas aeruginosa glycine betaine catabolism. J Bacteriol190:2690–2699 [CrossRef][PubMed]
    [Google Scholar]
  32. Zwart K. B., Veenhuis M., Harder W..( 1983;). Significance of yeast peroxisomes in the metabolism of choline and ethanolamine. Antonie van Leeuwenhoek49:369–385[PubMed]
    [Google Scholar]
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