Skip to main content
  • ASM
    • Antimicrobial Agents and Chemotherapy
    • Applied and Environmental Microbiology
    • Clinical Microbiology Reviews
    • Clinical and Vaccine Immunology
    • EcoSal Plus
    • Eukaryotic Cell
    • Infection and Immunity
    • Journal of Bacteriology
    • Journal of Clinical Microbiology
    • Journal of Microbiology & Biology Education
    • Journal of Virology
    • mBio
    • Microbiology and Molecular Biology Reviews
    • Microbiology Resource Announcements
    • Microbiology Spectrum
    • Molecular and Cellular Biology
    • mSphere
    • mSystems
  • Log in
  • My alerts
  • My Cart

Main menu

  • Home
  • Articles
    • Current Issue
    • Accepted Manuscripts
    • COVID-19 Special Collection
    • Archive
    • Minireviews
  • For Authors
    • Submit a Manuscript
    • Scope
    • Editorial Policy
    • Submission, Review, & Publication Processes
    • Organization and Format
    • Errata, Author Corrections, Retractions
    • Illustrations and Tables
    • Nomenclature
    • Abbreviations and Conventions
    • Publication Fees
    • Ethics Resources and Policies
  • About the Journal
    • About AEM
    • Editor in Chief
    • Editorial Board
    • For Reviewers
    • For the Media
    • For Librarians
    • For Advertisers
    • Alerts
    • RSS
    • FAQ
  • Subscribe
    • Members
    • Institutions
  • ASM
    • Antimicrobial Agents and Chemotherapy
    • Applied and Environmental Microbiology
    • Clinical Microbiology Reviews
    • Clinical and Vaccine Immunology
    • EcoSal Plus
    • Eukaryotic Cell
    • Infection and Immunity
    • Journal of Bacteriology
    • Journal of Clinical Microbiology
    • Journal of Microbiology & Biology Education
    • Journal of Virology
    • mBio
    • Microbiology and Molecular Biology Reviews
    • Microbiology Resource Announcements
    • Microbiology Spectrum
    • Molecular and Cellular Biology
    • mSphere
    • mSystems

User menu

  • Log in
  • My alerts
  • My Cart

Search

  • Advanced search
Applied and Environmental Microbiology
publisher-logosite-logo

Advanced Search

  • Home
  • Articles
    • Current Issue
    • Accepted Manuscripts
    • COVID-19 Special Collection
    • Archive
    • Minireviews
  • For Authors
    • Submit a Manuscript
    • Scope
    • Editorial Policy
    • Submission, Review, & Publication Processes
    • Organization and Format
    • Errata, Author Corrections, Retractions
    • Illustrations and Tables
    • Nomenclature
    • Abbreviations and Conventions
    • Publication Fees
    • Ethics Resources and Policies
  • About the Journal
    • About AEM
    • Editor in Chief
    • Editorial Board
    • For Reviewers
    • For the Media
    • For Librarians
    • For Advertisers
    • Alerts
    • RSS
    • FAQ
  • Subscribe
    • Members
    • Institutions
Microbial Ecology

Thiols in Nitric Oxide Synthase-Containing Nocardia sp. Strain NRRL 5646

Sungwon Lee, Hélène Bergeron, Peter C. K. Lau, John P. N. Rosazza
Sungwon Lee
1Division of Medicinal and Natural Products Chemistry, College of Pharmacy, and Center for Biocatalysis and Bioprocessing, The University of Iowa, Iowa City, Iowa 52242
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Hélène Bergeron
2Biotechnology Research Institute, National Research Council Canada, 6100 Royalmount Ave., Montreal, Quebec H4P 2R2, Canada
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Peter C. K. Lau
2Biotechnology Research Institute, National Research Council Canada, 6100 Royalmount Ave., Montreal, Quebec H4P 2R2, Canada
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
John P. N. Rosazza
1Division of Medicinal and Natural Products Chemistry, College of Pharmacy, and Center for Biocatalysis and Bioprocessing, The University of Iowa, Iowa City, Iowa 52242
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: john-rosazza@uiowa.edu
DOI: 10.1128/AEM.02809-06
  • Article
  • Figures & Data
  • Info & Metrics
  • PDF
Loading

ABSTRACT

Mycothiol (MSH) [1-d-myo-inosityl-2-(N-acetyl-l-cysteinyl)amido-2-deoxy-α-d-glucopyranoside], isolated as the bimane derivative, was established to be the major thiol in Nocardia sp. strain NRRL 5646, a species most closely related to Nocardia brasiliensis strain DSM 43758T. Thiol formation and detection of MSH-dependent formaldehyde dehydrogenase activity in cell extracts are relevant to the possible modulation of nitric oxide toxicity generated by strain NRRL 5646.

Nocardia sp. strain NRRL 5646 contains the first nitric oxide (NO) synthase (NOS) enzyme system found in the bacterial world (3). This enzyme catalyzes a complex process by which arginine is oxidized to NO and citrulline. The roles of this novel Nocardia NOS system have been investigated (3, 16, 17, 21, 31). One facet of this work that became interesting was an evaluation of possible roles of thiols in modulating NO toxicity, serving as stable storage forms for NO, or in trafficking of NO (11, 18, 28, 36). Evidence is gathered in this study that thiols are produced by Nocardia sp. strain NRRL 5646, and mycothiol (MSH) in particular may play an important role in the detoxification, if not the pathogenicity and regulation, of NO in NOS-containing bacteria (15, 26, 27). In this regard, Nocardia sp. strain NRRL 5646 represents a prototype counterpart model of glutathione (GSH) and S-nitrosoglutathione metabolism in eukaryotes (4, 6, 9-11, 13, 18, 19, 32).

For analysis, Nocardia sp stain. NRRL 5646 was grown in soybean flour-glucose medium in a two-stage process (3, 16, 17, 31). Cells harvested after 48 h from fully grown second-stage cultures were pelleted by centrifugation (8,000 × g for 20 min) and subjected to French pressure homogenization (12,000 lb/in2) and subsequent centrifugation (100,000 × g for 60 min). Extracts filtered through 0.22-μm Millex-GV membranes were used for determinations of protein (1), thiols such as cysteine, GSH, and nitrosothiols (RSNO) formed when thiols react with NO produced by NOS in this organism.

HgCl2 converted RSNO in cell extracts to thiols plus nitrogen oxides that reacted with 2,3-diaminonaphthalene to form 2,3-naphthotriazole, a product determined by fluorescence spectrometry (12, 20). Analyses showed 2.50 ± 0.17 pmol NO2−/g (dry weight) of cells, reflective of RSNO concentrations present in cell extracts. Analysis of the same extracts by Ellman's method (7) using 5,5′-dithio-bis(2-nitrobenzoic acid) indicated that 3.04 ± 0.02 μmol thiol/g (dry weight) of cells were present in Nocardia cell extracts. Although individual RSNO could not be identified, Nocardia contained RSNO corresponding to about 1/1,000 of the total measured thiols.

Specific Nocardia thiols were determined by N-(1-pyrenyl) maleimide (NPM) (29, 33) and monobromobimane (mBBr) (25) derivatization and subsequent high-performance liquid chromatography (HPLC) analysis. A modified NPM derivatization/HPLC method (33) showed that γ-glutamyl-l-cysteine was the only cell extract component that corresponded to standards, and its concentration was estimated to be 0.14 ± 0.03 μmol/g (dry weight) of cells. Nocardia thiols were also measured using a modified mBBr derivatization/HPLC method (25) to show bimane-derivatized totals of 2.2 ± 0.2 μmol of MSH (see Fig. 2), 0.14 ± 0.02 μmol of γ-glutamyl-l-cysteine, and 0.067 ± 0.008 μmol l-cysteine per gram (dry weight) of cells. γ-Glutamyl-l-cysteine and MSH-bimane (MSmB) derivatives nearly coeluted with a reagent-derived peak.

MSmB (Fig. 1) was isolated from 106 g of Nocardia cells that were extracted with aqueous acetonitrile and reacted with mBBr (23, 33). Half the extract was subjected to preparative HPLC, where peaks eluting at 25.3 min were pooled and dried to give 3.9 mg of >98% pure (HPLC) MSmB for spectral analysis. High-resolution mass spectrometry gave m/z 699.2171 for C27H40N4O14SNa, [MNa+] (calculated 699.2159), and an optical rotation of [α]25D + 26° (c 0.1, H2O).

FIG. 1.
  • Open in new tab
  • Download powerpoint
FIG. 1.

Structures of MSH and MSmB.

Nuclear magnetic resonance (NMR) and other spectral properties were comparable with those for MSmB isolated from Streptomyces (23) and Mycobacterium (23) and to MSH recently synthesized in our laboratory (21). NMR spectra contained signals for all structural moieties including d-myo-inositol, d-glucosamine, N-acetyl-l-cysteine, and bimane, and analyses confirmed how these moieties were linked together. Key proton NMR signals corresponding to the 5″-methyl group of N-acetyl-l-cysteine and methyl groups at positions 7b, 9b, and 10b of bimane were clearly evident between 1.8 and 2.5 ppm. One anomeric proton signal for d-glucosamine (5.12 ppm; JH-1 = 3.7 Hz) was consistent with an α-glycosidic linkage. By 13C-NMR, all four methyl groups were observed between 8 and 25 ppm, and the spectrum also showed one anomeric carbon signal at 101.9 ppm for d-glucosamine.

Figure 2 showed that Nocardia sp. strain NRRL 5646 contained MSH as the major low-molecular-weight thiol plus smaller amounts of γ-glutamyl-l-cysteine and l-cysteine. This is the first report of the characterization of MSmB from a NOS-containing species of Nocardia. Nocardia sp. strain NRRL 5646 contained 2.2 μmol/g (dry weight) of cells of MSH. This value is within the MSH range of 2.7 to 19 μmol/g (dry weight) of cells for other nocardioform bacteria (24). The highest levels of MSH occur in mycobacteria, whereas Nocardia asteroides and Nocardia brasiliensis contained 2.8 and 3.5 μmol/g (dry weight) MSH, respectively (24).

FIG. 2.
  • Open in new tab
  • Download powerpoint
FIG. 2.

HPLC chromatogram of mBBr-derivatized thiols in Nocardia sp. strain NRRL 5646 cell extracts. C*, endogenous fluorescent compound from cell extracts; R*, reagent-derived peak.

High concentrations of NO and S-nitrosoglutathione (GSNO) are toxic to bacteria (14, 28). Low-molecular-weight RSNO can disrupt cellular function by the transnitrosation of thiol groups in critical proteins (28, 35). However, bacterial cells have evolved apparent defense mechanisms against NO and RSNO as toxic agents. In Escherichia coli, flavorubredoxin with its associated oxidoreductase and flavohemoglobin convert NO to less noxious nitrous oxide and nitrate, respectively (8, 28). E. coli also contains GSH-dependent formaldehyde dehydrogenase (GS-FAD), a GSNO-metabolizing enzyme (22). GS-FAD is a widely distributed and highly conserved class III alcohol dehydrogenase. The enzyme is also known as GSNO reductase in E. coli, in Saccharomyces cerevisiae, and in mouse macrophages (22). GSNO reductase activity appears to be an inherent property of GS-FAD and a major means of regulating RSNO levels in cells.

MSH-dependent formaldehyde dehydrogenase activity in strain NRRL 5646 was measured using a slight modification of a method described previously by Vanophem et al. (34). Crude MSH solution was prepared by boiling cell extracts for 5 min and removing denatured protein and cell debris by centrifugation (40,000 × g for 30 min). The resulting supernatant was lyophilized and redissolved in 20 mM potassium phosphate buffer (pH 7.2). MSH concentrations in extracts were determined by mBBr derivatization and HPLC analysis. MSH-free cell extracts in 20 mM potassium phosphate buffer (pH 7.2) were prepared by passage over a Pharmacia PD-10 desalting column. For MSH-dependent formaldehyde dehydrogenase determinations, reactions were initiated by adding formaldehyde to MSH-free cell extracts containing 1 mM dithiothreitol, 2.5 mM NAD+, and 55 μM MSH. One unit of enzyme activity produced 1 μmol NADH,H+/min at 25°C. MSH-dependent formaldehyde dehydrogenase activity in Nocardia cell extracts was detected at 0.015 units/mg protein. Enzyme activity was absent without MSH. MSH-dependent formaldehyde dehydrogenase activity is known for Mycobacterium tuberculosis, where MSH-dependent formaldehyde dehydrogenase activity was identified as an S-nitrosomycothiol reductase (35).

Since its first isolation, Nocardia sp. strain NRRL 5646 has not been subjected to molecular identification by 16S rRNA gene analysis. Near-full-length 16S rRNA gene sequences are considered to be a reliable criterion for species identification in Nocardia (2, 30, 37). Moreover, a variable region that exists within the first 500 bp of the gene has been deemed reliable for species differentiation among members of this genus (5). We amplified a 1.4-kb 16S rRNA gene fragment of Nocardia sp. strain NRRL 5646 using eubacterial primers 27f and 1492R and a conventional PCR technique. Automated fluorescence DNA sequencing established a 1,427-base sequence that was found to have the highest identity (98%) to the corresponding regions of N. brasiliensis strain DSM 43758T (GenBank accession number AF430038.1) and several other N. brasiliensis strains (accessions numbers Z36935, X80608, AY245543, DQ659902, and X80591) by BLAST analysis. No comparative similarities to Rhodococcus species were uncovered. This confirmed the Nocardia designation of strain NRRL 5646 but not at a known species level, since at least 99.2% identity is required for this classification (5). It appears not to be N. brasiliensis, since the signature sequence in the variable region showed a base transversion (149-TTTCAGT-155 in N. brasiliensis versus 146-TTCCAGT-152 in NRRL 5646), a signature sequence that also distinguishes it from Nocardia asteroides, N. farcinica, N. nova, N. otitidiscaviarum, N. pseudobrasiliensis, and N. transvalensis (5). Hence, the 16S sequence of NRRL 5646 most likely represents a new Nocardia species that would require further study, such as a polyphasic approach.

Nucleotide sequence accession number.

The sequence of the 1.4-kb 16S rRNA gene fragment of Nocardia sp. strain NRRL 5646 was deposited in GenBank under accession number DQ925490.

ACKNOWLEDGMENTS

S. Lee thanks the Center for Biocatalysis and Bioprocessing at the University of Iowa for a predoctoral fellowship.

We thank R. C. Fahey of the University of California, San Diego, for an authentic sample of MSmB and helpful advice on MSmB purification.

FOOTNOTES

    • Received 1 December 2006.
    • Accepted 19 February 2007.
  • Copyright © 2007 American Society for Microbiology

REFERENCES

  1. 1.↵
    Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem.72:248-254.
    OpenUrlCrossRefPubMedWeb of Science
  2. 2.↵
    Brown-Elliott, B. A., J. M. Brown, P. S. Conville, and R. J. Wallace, Jr. 2006. Clinical and laboratory features of the Nocardia spp. based on current molecular taxonomy. Clin. Microbiol. Rev.19:259-282.
    OpenUrlAbstract/FREE Full Text
  3. 3.↵
    Chen, Y. J., and J. P. N. Rosazza. 1995. Purification and characterization of nitric oxide synthase (NOSNOC) from a Nocardia species. J. Bacteriol.177:5122-5128.
    OpenUrlAbstract/FREE Full Text
  4. 4.↵
    Clancy, R. M., D. Levartovsky, J. Leszczynska-Piziak, J. Yegudin, and S. B. Abramson. 1994. Nitric oxide reacts with intracellular glutathione and activates the hexose monophosphate shunt in human neutrophils: evidence for S-nitrosoglutathione as a bioactive intermediary. Proc. Natl. Acad. Sci. USA91:3680-3684.
    OpenUrlAbstract/FREE Full Text
  5. 5.↵
    Conville, P. S., S. H. Fischer, C. P. Cartwright, and F. G. Witebsky. 2000. Identification of Nocardia species by restriction endonuclease analysis of an amplified portion of the 16S rRNA gene. J. Clin. Microbiol.38:158-164.
    OpenUrlAbstract/FREE Full Text
  6. 6.↵
    Do, K. Q., B. Benz, G. Grima, U. Gutteck-Amsler, I. Kluge, and T. E. Salt. 1996. Nitric oxide precursor arginine and S-nitrosoglutathione in synaptic and glial function. Neurochem. Int.29:213-224.
    OpenUrlCrossRefPubMed
  7. 7.↵
    Ellman, G. L. 1959. Tissue sulfhydryl groups. Arch. Biochem. Biophys.82:70-77.
    OpenUrlCrossRefPubMedWeb of Science
  8. 8.↵
    Gardner, A. M., R. A. Helmick, and P. R. Gardner. 2002. Flavorubredoxin, an inducible catalyst for nitric oxide reduction and detoxification in Escherichia coli. J. Biol. Chem.277:8172-8177.
    OpenUrlAbstract/FREE Full Text
  9. 9.↵
    Gaston, B., J. Reilly, J. M. Drazen, J. Fackler, P. Ramdev, D. Arnelle, M. E. Mullins, D. J. Sugarbaker, C. Chee, D. J. Singel, J. Loscalzo, and J. S. Stamler. 1993. Endogenous nitrogen oxides and bronchodilator S-nitrosothiols in human airways. Proc. Natl. Acad. Sci. USA90:10957-10961.
    OpenUrlAbstract/FREE Full Text
  10. 10.
    Gaston, B., S. Sears, J. Woods, J. Hunt, M. Ponaman, T. McMahon, and J. S. Stamler. 1998. Bronchodilator S-nitrosothiol deficiency in asthmatic respiratory failure. Lancet351:1317-1319.
    OpenUrlCrossRefPubMedWeb of Science
  11. 11.↵
    Giustarini, D., A. Milzani, R. Colombo, I. Dalle-Donne, and R. Rossi. 2003. Nitric oxide and S-nitrosothiols in human blood. Clin. Chim. Acta330:85-98.
    OpenUrlCrossRefPubMedWeb of Science
  12. 12.↵
    Goldman, R. K., A. A. Vlessis, and D. D. Trunkey. 1998. Nitrosothiol quantification in human plasma. Anal. Biochem.259:98-103.
    OpenUrlCrossRefPubMedWeb of Science
  13. 13.↵
    Gordge, M. P., J. S. Hothersall, G. H. Neild, and A. A. N. Dutra. 1996. Role of a copper(I)-dependent enzyme in the anti-platelet action of S-nitrosoglutathione. Br. J. Pharmacol.119:533-538.
    OpenUrlCrossRefPubMed
  14. 14.↵
    Green, R. M., A. Seth, and N. D. Connell. 2000. A peptide permease mutant of Mycobacterium bovis BCG resistant to the toxic peptides glutathione and S-nitrosoglutathione. Infect. Immun.68:429-436.
    OpenUrlAbstract/FREE Full Text
  15. 15.↵
    Hand, C. E., and J. F. Honek. 2005. Biological chemistry of naturally occurring thiols of microbial and marine origin. J. Nat. Prod.68:293-308.
    OpenUrlCrossRefPubMedWeb of Science
  16. 16.↵
    He, A., D. R. Simpson, L. Daniels, and J. P. N. Rosazza. 2004. Cloning, expression, purification and characterization of Nocardia sp. GTP cyclohydrolase I. Protein Expr. Purif.35:171-180.
    OpenUrlCrossRefPubMedWeb of Science
  17. 17.↵
    He, A., and J. P. N. Rosazza. 2004. GTP cyclohydrolase I: purification, characterization, and effects of inhibition on nitric oxide synthase in Nocardia species. Appl. Environ. Microbiol.69:7507-7513.
    OpenUrlCrossRef
  18. 18.↵
    Hogg, N. 2000. Biological chemistry and clinical potential of S-nitrosothiols. Free Radic. Biol. Med.28:1478-1486.
    OpenUrlCrossRefPubMedWeb of Science
  19. 19.↵
    Kleinman, W. A., and J. P. Richie. 2000. Status of glutathione and other thiols and disulfides in human plasma. Biochem. Pharmacol.60:19-29.
    OpenUrlCrossRefPubMedWeb of Science
  20. 20.↵
    Kostka, P., and J. K. J. Park. 1999. Fluorometric detection of S-nitrosothiols. Methods Enzymol.301:227-235.
    OpenUrlCrossRefPubMedWeb of Science
  21. 21.↵
    Lee, S., and J. P. N. Rosazza. 2004. First total synthesis of mycothiol and mycothiol disulfide. Org. Lett.6:365-368.
    OpenUrlCrossRefPubMed
  22. 22.↵
    Liu, L. M., A. Hausladen, M. Zeng, L. Que, J. Heitman, and J. S. Stamler. 2001. A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature410:490-494.
    OpenUrlCrossRefPubMedWeb of Science
  23. 23.↵
    Newton, G. L., C. A. Bewley, T. J. Dwyer, R. Horn, Y. Aharonowitz, G. Cohen, J. Davies, D. J. Faulkner, and R. C. Fahey. 1995. The structure of U17 isolated from Streptomyces clavuligerus and its properties as an antioxidant thiol. Eur. J. Biochem.230:821-825.
    OpenUrlCrossRefPubMedWeb of Science
  24. 24.↵
    Newton, G. L., K. Arnold, M. S. Price, C. Sherrill, S. B. Delcardayre, Y. Aharonowitz, G. Cohen, J. Davies, R. C. Fahey, and C. Davis. 1996. Distribution of thiols in microorganisms: mycothiol is a major thiol in most actinomycetes. J. Bacteriol.178:1990-1995.
    OpenUrlAbstract/FREE Full Text
  25. 25.↵
    Newton, G. L., and R. C. Fahey. 1995. Determination of biothiols by bromobimane labeling and high-performance liquid-chromatography. Methods Enzymol.251:148-166.
    OpenUrlCrossRefPubMedWeb of Science
  26. 26.↵
    Newton, G. L., and R. C. Fahey. 2002. Mycothiol biochemistry. Arch. Microbiol.178:388-394.
    OpenUrlCrossRefPubMedWeb of Science
  27. 27.↵
    Newton, G. L., Y. Av-Gay, and R. C. Fahey. 2000. A novel mycothiol-dependent detoxification pathway in mycobacteria involving mycothiol S-conjugate amidase. Biochemistry39:10739-10746.
    OpenUrlCrossRefPubMed
  28. 28.↵
    Poole, R. K. 2005. Nitric oxide and nitrosative stress tolerance in bacteria. Biochem. Soc. Trans.33:176-180.
    OpenUrlCrossRefPubMedWeb of Science
  29. 29.↵
    Ridnour, L. A., R. A. Winters, N. Ercal, and D. R. Spitz. 1999. Measurement of glutathione, glutathione disulfide, and other thiols in mammalian cell and tissue homogenates using high-performance liquid chromatography separation of N-(1-pyrenyl)maleimide derivatives. Methods Enzymol.299:258-267.
    OpenUrlCrossRefPubMedWeb of Science
  30. 30.↵
    Roth, A., S. Andrees, R. M. Kroppenstedt, D. Harmsen, and H. Mauch. 2003. Phylogeny of the genus Nocardia based on reassessed 16S rRNA gene sequences reveals underspeciation and division of strains classified as Nocardia asteroides into three established species and two unnamed taxons. J. Clin. Microbiol.41:851-856.
    OpenUrlAbstract/FREE Full Text
  31. 31.↵
    Son, J. K., and J. P. N. Rosazza. 2000. Cyclic guanosine-3′,5′-monophosphate and biopteridine biosynthesis in Nocardia sp. J. Bacteriol.182:3644-3648.
    OpenUrlAbstract/FREE Full Text
  32. 32.↵
    Spencer, N. Y., H. Zeng, R. P. Patel, and N. Hogg. 2000. Reaction of S-nitrosoglutathione with the heme group of deoxyhemoglobin. J. Biol. Chem.275:36562-36567.
    OpenUrlAbstract/FREE Full Text
  33. 33.↵
    Spies, H. S. C., and D. J. Steenkamp. 1994. Thiols of intracellular pathogens—identification of ovothiol A in Leishmania donovani and structural analysis of a novel thiol from Mycobacterium bovis. Eur. J. Biochem.224:203-213.
    OpenUrlCrossRefPubMedWeb of Science
  34. 34.↵
    Vanophem, P. W., J. Vanbeeumen, and J. A. Duine. 1992. NAD-linked, factor-dependent formaldehyde dehydrogenase or trimeric, zinc-containing, long-chain alcohol dehydrogenase from Amycolatopsis methanolica. Eur. J. Biochem.206:511-518.
    OpenUrlCrossRefPubMedWeb of Science
  35. 35.↵
    Vogt, R. N., D. J. Steenkamp, R. Zheng, and J. S. Blanchard. 2003. The metabolism of nitrosothiols in the mycobacteria: identification and characterization of S-nitrosomycothiol reductase. Biochem. J.374:657-666.
    OpenUrlCrossRefPubMedWeb of Science
  36. 36.↵
    Wang, K., W. Zhang, M. Xian, Y. C. Hou, X. C. Chen, J. P. Cheng, and P. G. Wang. 2000. New chemical and biological aspects of S-nitrosothiols. Curr. Med. Chem.7:821-834.
    OpenUrlPubMed
  37. 37.↵
    Wauters, G., V. Avesani, J. Charlier, M. Janssens, M. Vaneechoutte, and M. Delmee. 2005. Distribution of Nocardia species in clinical samples and their routine rapid identification in the laboratory. J. Clin. Microbiol.43:2624-2628.
    OpenUrlAbstract/FREE Full Text
PreviousNext
Back to top
Download PDF
Citation Tools
Thiols in Nitric Oxide Synthase-Containing Nocardia sp. Strain NRRL 5646
Sungwon Lee, Hélène Bergeron, Peter C. K. Lau, John P. N. Rosazza
Applied and Environmental Microbiology Apr 2007, 73 (9) 3095-3097; DOI: 10.1128/AEM.02809-06

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
Print

Alerts
Sign In to Email Alerts with your Email Address
Email

Thank you for sharing this Applied and Environmental Microbiology article.

NOTE: We request your email address only to inform the recipient that it was you who recommended this article, and that it is not junk mail. We do not retain these email addresses.

Enter multiple addresses on separate lines or separate them with commas.
Thiols in Nitric Oxide Synthase-Containing Nocardia sp. Strain NRRL 5646
(Your Name) has forwarded a page to you from Applied and Environmental Microbiology
(Your Name) thought you would be interested in this article in Applied and Environmental Microbiology.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Share
Thiols in Nitric Oxide Synthase-Containing Nocardia sp. Strain NRRL 5646
Sungwon Lee, Hélène Bergeron, Peter C. K. Lau, John P. N. Rosazza
Applied and Environmental Microbiology Apr 2007, 73 (9) 3095-3097; DOI: 10.1128/AEM.02809-06
del.icio.us logo Digg logo Reddit logo Twitter logo CiteULike logo Facebook logo Google logo Mendeley logo
  • Top
  • Article
    • ABSTRACT
    • Nucleotide sequence accession number.
    • ACKNOWLEDGMENTS
    • FOOTNOTES
    • REFERENCES
  • Figures & Data
  • Info & Metrics
  • PDF

KEYWORDS

cysteine
Glycopeptides
Inositol
Nocardia

Related Articles

Cited By...

About

  • About AEM
  • Editor in Chief
  • Editorial Board
  • Policies
  • For Reviewers
  • For the Media
  • For Librarians
  • For Advertisers
  • Alerts
  • RSS
  • FAQ
  • Permissions
  • Journal Announcements

Authors

  • ASM Author Center
  • Submit a Manuscript
  • Article Types
  • Ethics
  • Contact Us

Follow #AppEnvMicro

@ASMicrobiology

       

ASM Journals

ASM journals are the most prominent publications in the field, delivering up-to-date and authoritative coverage of both basic and clinical microbiology.

About ASM | Contact Us | Press Room

 

ASM is a member of

Scientific Society Publisher Alliance

 

American Society for Microbiology
1752 N St. NW
Washington, DC 20036
Phone: (202) 737-3600

Copyright © 2021 American Society for Microbiology | Privacy Policy | Website feedback

 

Print ISSN: 0099-2240; Online ISSN: 1098-5336