1887

Abstract

Thirteen ascomycetous yeast strains with sequenced genomes were assayed for their ability to grow on chemically defined medium with 16 different sulfur compounds as the only significant source of sulfur. These compounds included sulfoxides, sulfones, sulfonates, sulfamates and sulfate esters. Broad utilization of alternative sulfur sources was observed in (syn. ), , (syn. ), , (syn. ), , (syn. ) and . , and were mainly able to utilize sulfonates and sulfate esters, while and were limited to aromatic sulfate esters. Genome analysis identified several candidate genes with bacterial homologues that had been previously shown to be involved in the utilization of alternative sulfur sources. Analysis of candidate gene promoter sequences revealed a significant overrepresentation of DNA motifs that have been shown to regulate sulfur metabolism in .

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.060285-0
2012-10-01
2019-10-17
Loading full text...

Full text loading...

/deliver/fulltext/micro/158/10/2585.html?itemId=/content/journal/micro/10.1099/mic.0.060285-0&mimeType=html&fmt=ahah

References

  1. Autry A. R. , Fitzgerald J. W. . ( 1990; ). Sulfonate-S – a major form of forest soil organic sulfur. . Biol Fertil Soils 10:, 50–56.
    [Google Scholar]
  2. Bailey T. L. , Boden M. , Buske F. A. , Frith M. , Grant C. E. , Clementi L. , Ren J. Y. , Li W. W. , Noble W. S. . ( 2009; ). meme suite: tools for motif discovery and searching. . Nucleic Acids Res 37: (Web Server issue), W202–W208. [CrossRef] [PubMed]
    [Google Scholar]
  3. Baldi F. , Pepi M. , Fava F. . ( 2003; ). Growth of Rhodosporidium toruloides strain DBVPG 6662 on dibenzothiophene crystals and orimulsion. . Appl Environ Microbiol 69:, 4689–4696. [CrossRef] [PubMed]
    [Google Scholar]
  4. Baxter N. J. , Scanlan J. , De Marco P. , Wood A. P. , Murrell J. C. . ( 2002; ). Duplicate copies of genes encoding methanesulfonate monooxygenase in Marinosulfonomonas methylotropha strain TR3 and detection of methanesulfonate utilizers in the environment. . Appl Environ Microbiol 68:, 289–296. [CrossRef] [PubMed]
    [Google Scholar]
  5. Beil S. , Kehrli H. , James P. , Staudenmann W. , Cook A. M. , Leisinger T. , Kertesz M. A. . ( 1995; ). Purification and characterization of the arylsulfatase synthesized by Pseudomonas aeruginosa PAO during growth in sulfate-free medium and cloning of the arylsulfatase gene (atsA). . Eur J Biochem 229:, 385–394. [CrossRef] [PubMed]
    [Google Scholar]
  6. Boer V. M. , de Winde J. H. , Pronk J. T. , Piper M. D. W. . ( 2003; ). The genome-wide transcriptional responses of Saccharomyces cerevisiae grown on glucose in aerobic chemostat cultures limited for carbon, nitrogen, phosphorus, or sulfur. . J Biol Chem 278:, 3265–3274. [CrossRef] [PubMed]
    [Google Scholar]
  7. Castresana J. . ( 2000; ). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. . Mol Biol Evol 17:, 540–552. [CrossRef] [PubMed]
    [Google Scholar]
  8. Davison J. , Brunel F. , Phanopoulos A. , Prozzi D. , Terpstra P. . ( 1992; ). Cloning and sequencing of Pseudomonas genes determining sodium dodecyl sulfate biodegradation. . Gene 114:, 19–24. [CrossRef] [PubMed]
    [Google Scholar]
  9. de Marco P. , Moradas-Ferreira P. , Higgins T. P. , McDonald I. , Kenna E. M. , Murrell J. C. . ( 1999; ). Molecular analysis of a novel methanesulfonic acid monooxygenase from the methylotroph Methylosulfonomonas methylovora . . J Bacteriol 181:, 2244–2251.[PubMed]
    [Google Scholar]
  10. Eichhorn E. , van der Ploeg J. R. , Leisinger T. . ( 1999; ). Characterization of a two-component alkanesulfonate monooxygenase from Escherichia coli . . J Biol Chem 274:, 26639–26646. [CrossRef] [PubMed]
    [Google Scholar]
  11. Endoh T. , Kasuga K. , Horinouchi M. , Yoshida T. , Habe H. , Nojiri H. , Omori T. . ( 2003; ). Characterization and identification of genes essential for dimethyl sulfide utilization in Pseudomonas putida strain DS1. . Appl Microbiol Biotechnol 62:, 83–91. [CrossRef] [PubMed]
    [Google Scholar]
  12. Endoh T. , Habe H. , Nojiri H. , Yamane H. , Omori T. . ( 2005; ). The σ54-dependent transcriptional activator SfnR regulates the expression of the Pseudomonas putida sfnFG operon responsible for dimethyl sulphone utilization. . Mol Microbiol 55:, 897–911. [CrossRef] [PubMed]
    [Google Scholar]
  13. Faison B. D. , Clark T. M. , Lewis S. N. , Ma C. Y. , Sharkey D. M. , Woodward C. A. . ( 1991; ). Degradation of organic sulfur compounds by a coal-solubilizing fungus. . Appl Biochem Biotechnol 28-29:, 237–251. [CrossRef] [PubMed]
    [Google Scholar]
  14. Fauchon M. , Lagniel G. , Aude J. C. , Lombardia L. , Soularue P. , Petat C. , Marguerie G. , Sentenac A. , Werner M. , Labarre J. . ( 2002; ). Sulfur sparing in the yeast proteome in response to sulfur demand. . Mol Cell 9:, 713–723. [CrossRef] [PubMed]
    [Google Scholar]
  15. Fulton C. K. , Cooper R. A. . ( 2005; ). Catabolism of sulfamate by Mycobacterium sp. CF1. . Environ Microbiol 7:, 378–381. [CrossRef] [PubMed]
    [Google Scholar]
  16. Hagelueken G. , Adams T. M. , Wiehlmann L. , Widow U. , Kolmar H. , Tümmler B. , Heinz D. W. , Schubert W. D. . ( 2006; ). The crystal structure of SdsA1, an alkylsulfatase from Pseudomonas aeruginosa, defines a third class of sulfatases. . Proc Natl Acad Sci U S A 103:, 7631–7636. [CrossRef] [PubMed]
    [Google Scholar]
  17. Hall C. , Brachat S. , Dietrich F. S. . ( 2005; ). Contribution of horizontal gene transfer to the evolution of Saccharomyces cerevisiae . . Eukaryot Cell 4:, 1102–1115. [CrossRef] [PubMed]
    [Google Scholar]
  18. Hansen J. . ( 1999; ). Inactivation of MXR1 abolishes formation of dimethyl sulfide from dimethyl sulfoxide in Saccharomyces cerevisiae . . Appl Environ Microbiol 65:, 3915–3919.[PubMed]
    [Google Scholar]
  19. Harada T. , Spencer B. . ( 1962; ). The effect of sulphate assimilation on the induction of arylsulphatase synthesis in fungi. . Biochem J 82:, 148–156.[PubMed]
    [Google Scholar]
  20. Hébert A. , Forquin-Gomez M. P. , Roux A. , Aubert J. , Junot C. , Loux V. , Heilier J. F. , Bonnarme P. , Beckerich J. M. , Landaud S. . ( 2011; ). Exploration of sulfur metabolism in the yeast Kluyveromyces lactis . . Appl Microbiol Biotechnol 91:, 1409–1423. [CrossRef] [PubMed]
    [Google Scholar]
  21. Hogan D. A. , Auchtung T. A. , Hausinger R. P. . ( 1999; ). Cloning and characterization of a sulfonate/α-ketoglutarate dioxygenase from Saccharomyces cerevisiae . . J Bacteriol 181:, 5876–5879.[PubMed]
    [Google Scholar]
  22. Ichinose H. , Nakamizo M. , Wariishi H. , Tanaka H. . ( 2002; ). Metabolic response against sulfur-containing heterocyclic compounds by the lignin-degrading basidiomycete Coriolus versicolor . . Appl Microbiol Biotechnol 58:, 517–526. [CrossRef] [PubMed]
    [Google Scholar]
  23. Kahnert A. , Kertesz M. A. . ( 2000; ). Characterization of a sulfur-regulated oxygenative alkylsulfatase from Pseudomonas putida S-313. . J Biol Chem 275:, 31661–31667. [CrossRef] [PubMed]
    [Google Scholar]
  24. Katoh K. , Kuma K. , Toh H. , Miyata T. . ( 2005; ). mafft version 5: improvement in accuracy of multiple sequence alignment. . Nucleic Acids Res 33:, 511–518. [CrossRef] [PubMed]
    [Google Scholar]
  25. Kertesz M. A. . ( 2000; ). Riding the sulfur cycle – metabolism of sulfonates and sulfate esters in Gram-negative bacteria. . FEMS Microbiol Rev 24:, 135–175.[PubMed]
    [Google Scholar]
  26. Kertesz M. A. , Mirleau P. . ( 2004; ). The role of soil microbes in plant sulphur nutrition. . J Exp Bot 55:, 1939–1945. [CrossRef] [PubMed]
    [Google Scholar]
  27. Kertesz M. A. , Schmidt-Larbig K. , Wüest T. . ( 1999; ). A novel reduced flavin mononucleotide-dependent methanesulfonate sulfonatase encoded by the sulfur-regulated msu operon of Pseudomonas aeruginosa . . J Bacteriol 181:, 1464–1473.[PubMed]
    [Google Scholar]
  28. Kurtzman C. P. . ( 2011; ). Discussion of teleomorphic and anamorphic ascomycetous yeasts and yeast-like taxa. . In The Yeasts: a Taxonomic Study, , 4th edn., pp. 293–307. Edited by Kurtzman C. P. , Fell J. W. , Boekhout T. . . Amsterdam:: Elsevier;. [CrossRef]
    [Google Scholar]
  29. Lavoie H. , Hogues H. , Mallick J. , Sellam A. , Nantel A. , Whiteway M. . ( 2010; ). Evolutionary tinkering with conserved components of a transcriptional regulatory network. . PLoS Biol 8:, e1000329. [CrossRef] [PubMed]
    [Google Scholar]
  30. Lee T. A. , Jorgensen P. , Bognar A. L. , Peyraud C. , Thomas D. , Tyers M. . ( 2010; ). Dissection of combinatorial control by the Met4 transcriptional complex. . Mol Biol Cell 21:, 456–469. [CrossRef] [PubMed]
    [Google Scholar]
  31. Mirleau P. , Wogelius R. , Smith A. , Kertesz M. A. . ( 2005; ). Importance of organosulfur utilization for survival of Pseudomonas putida in soil and rhizosphere. . Appl Environ Microbiol 71:, 6571–6577. [CrossRef] [PubMed]
    [Google Scholar]
  32. Murakami-Nitta T. , Kirimura K. , Kino K. . ( 2003; ). Oxidative degradation of dimethyl sulfoxide by Cryptococcus humicolus WU-2, a newly isolated yeast. . J Biosci Bioeng 95:, 109–111.[PubMed] [CrossRef]
    [Google Scholar]
  33. Myette J. R. , Soundararajan V. , Behr J. , Shriver Z. , Raman R. , Sasisekharan R. . ( 2009; ). Heparin/heparan sulfate N-sulfamidase from Flavobacterium heparinum: structural and biochemical investigation of catalytic nitrogen-sulfur bond cleavage. . J Biol Chem 284:, 35189–35200. [CrossRef] [PubMed]
    [Google Scholar]
  34. Neuberg C. , Kurono K. . ( 1923; ). Über die enzymatische Spaltung der Phenolätherschwefelsäure. . Biochem Z 140:, 295–298.
    [Google Scholar]
  35. Ohama T. , Suzuki T. , Mori M. , Osawa S. , Ueda T. , Watanabe K. , Nakase T. . ( 1993; ). Non-universal decoding of the leucine codon CUG in several Candida species. . Nucleic Acids Res 21:, 4039–4045. [CrossRef] [PubMed]
    [Google Scholar]
  36. Ohshiro T. , Kojima T. , Torii K. , Kawasoe H. , Izumi Y. . ( 1999; ). Purification and characterization of dibenzothiophene (DBT) sulfone monooxygenase, an enzyme involved in DBT desulfurization, from Rhodococcus erythropolis D-1. . J Biosci Bioeng 88:, 610–616. [CrossRef] [PubMed]
    [Google Scholar]
  37. Osterås M. , Boncompagni E. , Vincent N. , Poggi M. C. , Le Rudulier D. . ( 1998; ). Presence of a gene encoding choline sulfatase in Sinorhizobium meliloti bet operon: choline-O-sulfate is metabolized into glycine betaine. . Proc Natl Acad Sci U S A 95:, 11394–11399. [CrossRef] [PubMed]
    [Google Scholar]
  38. Petti A. A. , McIsaac R. S. , Ho-Shing O. , Bussemaker H. J. , Botstein D. . ( 2012; ). Combinatorial control of diverse metabolic and physiological functions by transcriptional regulators of the yeast sulfur assimilation pathway. . Mol Biol Cell 23:, 3008–3024. [CrossRef] [PubMed]
    [Google Scholar]
  39. 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 A 94:, 3454–3458. [CrossRef] [PubMed]
    [Google Scholar]
  40. Ronquist F. , Huelsenbeck J. P. . ( 2003; ). MrBayes 3: Bayesian phylogenetic inference under mixed models. . Bioinformatics 19:, 1572–1574. [CrossRef] [PubMed]
    [Google Scholar]
  41. Schlenk D. , Bevers R. J. , Vertino A. M. , Cerniglia C. E. . ( 1994; ). P450 catalysed S-oxidation of dibenzothiophene by Cunninghamella elegans . . Xenobiotica 24:, 1077–1083. [CrossRef] [PubMed]
    [Google Scholar]
  42. Scott H. S. , Blanch L. , Guo X. H. , Freeman C. , Orsborn A. , Baker E. , Sutherland G. R. , Morris C. P. , Hopwood J. J. . ( 1995; ). Cloning of the sulphamidase gene and identification of mutations in Sanfilippo A syndrome. . Nat Genet 11:, 465–467. [CrossRef] [PubMed]
    [Google Scholar]
  43. Sood N. , Lal B. . ( 2009; ). Isolation of a novel yeast strain Candida digboiensis TERI ASN6 capable of degrading petroleum hydrocarbons in acidic conditions. . J Environ Manage 90:, 1728–1736. [CrossRef] [PubMed]
    [Google Scholar]
  44. Thomas D. , Surdin-Kerjan Y. . ( 1997; ). Metabolism of sulfur amino acids in Saccharomyces cerevisiae . . Microbiol Mol Biol Rev 61:, 503–532.[PubMed]
    [Google Scholar]
  45. Till A. R. . ( 2010; ). Sulphur and Sustainable Agriculture. Paris, France:: International Fertilizer Industry Association;.
    [Google Scholar]
  46. Uria-Nickelsen M. R. , Leadbetter E. R. , Godchaux W. III . ( 1993; ). Sulfonate-sulfur assimilation by yeasts resembles that of bacteria. . FEMS Microbiol Lett 114:, 73–77. [CrossRef] [PubMed]
    [Google Scholar]
  47. van der Ploeg J. R. , Weiss M. A. , Saller E. , Nashimoto H. , Saito N. , Kertesz M. A. , Leisinger T. . ( 1996; ). Identification of sulfate starvation-regulated genes in Escherichia coli: a gene cluster involved in the utilization of taurine as a sulfur source. . J Bacteriol 178:, 5438–5446.[PubMed]
    [Google Scholar]
  48. Van Hamme J. D. , Wong E. T. , Dettman H. , Gray M. R. , Pickard M. A. . ( 2003; ). Dibenzyl sulfide metabolism by white rot fungi. . Appl Environ Microbiol 69:, 1320–1324. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.060285-0
Loading
/content/journal/micro/10.1099/mic.0.060285-0
Loading

Data & Media loading...

Supplements

Supplementary figure legends and Table S1 

PDF

Figs S1 - S13 

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error