1887

Abstract

sp. strain NB4-1Y was isolated from vermicompost using bis-(3-pentafluorophenylpropyl)-sulfide as the sole added sulfur source and was found to have a broad capacity for metabolizing organosulfur compounds. NB4-1Y is closely related to and was found to metabolize 6 : 2 fluorotelomer sulfonate (6 : 2 FTS) to 5 : 3 fluorotelomer acid (5 : 3 acid) via 6 : 2 fluorotelomer acid (6 : 2 FTCA), 6 : 2 unsaturated fluorotelomer acid (6 : 2 FTUCA) and 5 : 3 unsaturated fluorotelomer acid (5 : 3 Uacid). Given that the molecular and biochemical basis for the microbial metabolism of poly- and per-fluorinated compounds has yet to be examined, we undertook to investigate 6 : 2 FTS metabolism in NB4-1Y. To this end, a whole-genome shotgun sequence was prepared and two-dimensional differential in-gel electrophoresis was used to compare proteomes of MgSO- and 6 : 2 FTS-grown cells. Of the three putative alkanesulfonate monooxygenases, four nitrilotriacetate monooxygenases and one taurine dioxygenase located in the draft genome, two nitrilotriacetate monooxygenases were differentially expressed in the presence of 6 : 2 FTS. It is hypothesized that these two enzymes may be responsible for 6 : 2 FTS desulfonation. In addition, a differentially expressed putative double bond reductase may be involved in the reduction of 5 : 3 Uacid to 5 : 3 acid. Other proteins differentially expressed during 6 : 2 FTS metabolism included a sulfate ABC transporter ATP-binding protein and two alkyl hydroperoxide reductases. This work establishes a foundation for future studies on the molecular biology and biochemistry of poly- and per-fluorinated compound metabolism in bacteria.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.068932-0
2013-08-01
2019-10-23
Loading full text...

Full text loading...

/deliver/fulltext/micro/159/8/1618.html?itemId=/content/journal/micro/10.1099/mic.0.068932-0&mimeType=html&fmt=ahah

References

  1. Altschul S. F. , Gish W. , Miller W. , Myers E. W. , Lipman D. J. . ( 1990; ). Basic local alignment search tool. . J Mol Biol 215:, 403–410.[PubMed] [CrossRef]
    [Google Scholar]
  2. Arenskötter M. , Bröker D. , Steinbüchel A. . ( 2004; ). Biology of the metabolically diverse genus Gordonia. . Appl Environ Microbiol 70:, 3195–3204. [CrossRef] [PubMed]
    [Google Scholar]
  3. Autry A. , Fitzgerald J. . ( 1990; ). Sulfonate-S – a major form of forest soil organic sulfur. . Biol Fertil Soils 10:, 50–56.
    [Google Scholar]
  4. Bollinger J. M. , Price J. C. , Hoffart L. M. , Barr E. W. , Krebs C. . ( 2005; ). Mechanism of taurine: α-ketoglutarate dioxygenase (TauD) from Escherichia coli. . Eur J Inorg Chem 2005:, 4245–4254. [CrossRef]
    [Google Scholar]
  5. Chevreux B. , Wetter T. , Suhai S. . ( 1999; ). Genome sequence assembly using trace signals and additional sequence information. . Computer Science and Biology: Proceedings of the German Conference of Bioinformatics (GCB) 99:, 45–56.
    [Google Scholar]
  6. Clarke B. O. , Smith S. R. . ( 2011; ). Review of ‘emerging’ organic contaminants in biosolids and assessment of international research priorities for the agricultural use of biosolids. . Environ Int 37:, 226–247. [CrossRef] [PubMed]
    [Google Scholar]
  7. Cook A. M. , Smits T. H. M. , Denger K. . ( 2008; ). Sulfonates and Organotrophic Sulfite Metabolism. Edited by Dahl C. , Friedrich C. G. . . Berlin:: Springer-Verlag Berlin;.
    [Google Scholar]
  8. Dinglasan M. J. A. , Ye Y. , Edwards E. A. , Mabury S. A. . ( 2004; ). Fluorotelomer alcohol biodegradation yields poly- and perfluorinated acids. . Environ Sci Technol 38:, 2857–2864. [CrossRef] [PubMed]
    [Google Scholar]
  9. Drzyzga O. . ( 2012; ). The strengths and weaknesses of Gordonia: a review of an emerging genus with increasing biotechnological potential. . Crit Rev Microbiol 38:, 300–316. [CrossRef] [PubMed]
    [Google Scholar]
  10. Eichhorn E. , van der Ploeg J. R. , Kertesz M. A. , Leisinger T. . ( 1997; ). Characterization of alpha-ketoglutarate-dependent taurine dioxygenase from Escherichia coli. . J Biol Chem 272:, 23031–23036. [CrossRef] [PubMed]
    [Google Scholar]
  11. 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]
  12. Eichhorn E. , Davey C. A. , Sargent D. F. , Leisinger T. , Richmond T. J. . ( 2002; ). Crystal structure of Escherichia coli alkanesulfonate monooxygenase SsuD. . J Mol Biol 324:, 457–468. [CrossRef] [PubMed]
    [Google Scholar]
  13. Ellis H. R. . ( 2010; ). The FMN-dependent two-component monooxygenase systems. . Arch Biochem Biophys 497:, 1–12. [CrossRef] [PubMed]
    [Google Scholar]
  14. 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]
  15. Erwin K. N. , Nakano S. , Zuber P. . ( 2005; ). Sulfate-dependent repression of genes that function in organosulfur metabolism in Bacillus subtilis requires Spx. . J Bacteriol 187:, 4042–4049. [CrossRef] [PubMed]
    [Google Scholar]
  16. Felsenstein J. . ( 1985; ). Confidence limits on phylogenies: an approach using the bootstrap. . Evolution 39:, 783–791. [CrossRef]
    [Google Scholar]
  17. Froemel T. , Knepper T. P. . ( 2010; ). Biodegradation of fluorinated alkyl substances. . In Reviews of Environmental Contamination and Toxicology, Vol 208, Perfluorinated Alkylated Substances, pp. 161–177. Edited by Whitacre D. M. , DeVoogt P. . . New York:: Springer;.
  18. Hemmerich C. , Buechlein A. , Podicheti R. , Revanna K. V. , Dong Q. . ( 2010; ). An Ergatis-based prokaryotic genome annotation web server. . Bioinformatics 26:, 1122–1124. [CrossRef] [PubMed]
    [Google Scholar]
  19. Higgins C. P. , Field J. A. , Criddle C. S. , Luthy R. G. . ( 2005; ). Quantitative determination of perfluorochemicals in sediments and domestic sludge. . Environ Sci Technol 39:, 3946–3956. [CrossRef] [PubMed]
    [Google Scholar]
  20. Kahnert A. , Vermeij P. , Wietek C. , James P. , Leisinger T. , Kertesz M. A. . ( 2000; ). The ssu locus plays a key role in organosulfur metabolism in Pseudomonas putida S-313. . J Bacteriol 182:, 2869–2878. [CrossRef] [PubMed]
    [Google Scholar]
  21. Karp P. D. , Paley S. , Romero P. . ( 2002; ). The Pathway Tools software. . Bioinformatics 18: (Suppl 1), S225–S232. [CrossRef] [PubMed]
    [Google Scholar]
  22. 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]
  23. Key B. D. , Howell R. D. , Criddle C. S. . ( 1998; ). Defluorination of organofluorine sulfur compounds by Pseudomonas sp. strain D2. . Environ Sci Technol 32:, 2283–2287. [CrossRef]
    [Google Scholar]
  24. Kieser T. , Bibb M. J. , Buttner M. J. , Chater K. F. , Hopwood D. A. . ( 2000; ). Practical Streptomyces Genetics. Norwich, UK:: John Innes Foundation;.
    [Google Scholar]
  25. Kim S. B. , Brown R. , Oldfield C. , Gilbert S. C. , Goodfellow M. . ( 1999; ). Gordonia desulfuricans sp. nov., a benzothiophene-desulphurizing actinomycete. . Int J Syst Bacteriol 49:, 1845–1851. [CrossRef] [PubMed]
    [Google Scholar]
  26. Kim K.-J. , Kim S. , Lee S. , Kang B. S. , Lee H.-S. , Oh T.-K. , Kim M. H. . ( 2006; ). Crystallization and initial crystallographic characterization of the Corynebacterium glutamicum nitrilotriacetate monooxygenase component A. . Acta Crystallogr Sect F Struct Biol Cryst Commun 62:, 1141–1143. [CrossRef] [PubMed]
    [Google Scholar]
  27. Kim M. H. , Wang N. , McDonald T. , Chu K.-H. . ( 2012; ). Biodefluorination and biotransformation of fluorotelomer alcohols by two alkane-degrading Pseudomonas strains. . Biotechnol Bioeng 109:, 3041–3048. [CrossRef] [PubMed]
    [Google Scholar]
  28. Koch D. J. , Rückert C. , Rey D. A. , Mix A. , Pühler A. , Kalinowski J. . ( 2005; ). Role of the ssu and seu genes of Corynebacterium glutamicum ATCC 13032 in utilization of sulfonates and sulfonate esters as sulfur sources. . Appl Environ Microbiol 71:, 6104–6114. [CrossRef] [PubMed]
    [Google Scholar]
  29. Liu J. , Lee L. S. , Nies L. F. , Nakatsu C. H. , Turco R. F. . ( 2007; ). Biotransformation of 8:2 fluorotelomer alcohol in soil and by soil bacteria isolates. . Environ Sci Technol 41:, 8024–8030. [CrossRef] [PubMed]
    [Google Scholar]
  30. Liu J. , Wang N. , Szostek B. , Buck R. C. , Panciroli P. K. , Folsom P. W. , Sulecki L. M. , Bellin C. A. . ( 2010; ). 6-2 Fluorotelomer alcohol aerobic biodegradation in soil and mixed bacterial culture. . Chemosphere 78:, 437–444. [CrossRef] [PubMed]
    [Google Scholar]
  31. Loewen M. , Wania F. , Wang F. , Tomy G. . ( 2008; ). Altitudinal transect of atmospheric and aqueous fluorinated organic compounds in Western Canada. . Environ Sci Technol 42:, 2374–2379. [CrossRef] [PubMed]
    [Google Scholar]
  32. Loganathan B. G. , Sajwan K. S. , Sinclair E. , Senthil Kumar K. , Kannan K. . ( 2007; ). Perfluoroalkyl sulfonates and perfluorocarboxylates in two wastewater treatment facilities in Kentucky and Georgia. . Water Res 41:, 4611–4620. [CrossRef] [PubMed]
    [Google Scholar]
  33. Murphy C. D. . ( 2010; ). Biodegradation and biotransformation of organofluorine compounds. . Biotechnol Lett 32:, 351–359. [CrossRef] [PubMed]
    [Google Scholar]
  34. Nabb D. L. , Szostek B. , Himmelstein M. W. , Mawn M. P. , Gargas M. L. , Sweeney L. M. , Stadler J. C. , Buck R. C. , Fasano W. J. . ( 2007; ). In vitro metabolism of 8-2 fluorotelomer alcohol: interspecies comparisons and metabolic pathway refinement. . Toxicol Sci 100:, 333–344. [CrossRef] [PubMed]
    [Google Scholar]
  35. Newsted J. L. , Beach S. A. , Gallagher S. P. , Giesy J. P. . ( 2008; ). Acute and chronic effects of perfluorobutane sulfonate (PFBS) on the mallard and northern bobwhite quail. . Arch Environ Contam Toxicol 54:, 535–545. [CrossRef] [PubMed]
    [Google Scholar]
  36. Oakes K. D. , Benskin J. P. , Martin J. W. , Ings J. S. , Heinrichs J. Y. , Dixon D. G. , Servos M. R. . ( 2010; ). Biomonitoring of perfluorochemicals and toxicity to the downstream fish community of Etobicoke Creek following deployment of aqueous film-forming foam. . Aquat Toxicol 98:, 120–129. [CrossRef] [PubMed]
    [Google Scholar]
  37. Olsen G. W. , Church T. R. , Miller J. P. , Burris J. M. , Hansen K. J. , Lundberg J. K. , Armitage J. B. , Herron R. M. , Medhdizadehkashi Z. . & other authors ( 2003; ). Perfluorooctanesulfonate and other fluorochemicals in the serum of American Red Cross adult blood donors. . Environ Health Perspect 111:, 1892–1901. [CrossRef] [PubMed]
    [Google Scholar]
  38. Patrauchan M. A. , Florizone C. , Dosanjh M. , Mohn W. W. , Davies J. , Eltis L. D. . ( 2005; ). Catabolism of benzoate and phthalate in Rhodococcus sp. strain RHA1: redundancies and convergence. . J Bacteriol 187:, 4050–4063. [CrossRef] [PubMed]
    [Google Scholar]
  39. Phillips M. M. , Dinglasan-Panlilio M. J. A. , Mabury S. A. , Solomon K. R. , Sibley P. K. . ( 2007; ). Fluorotelomer acids are more toxic than perfluorinated acids. . Environ Sci Technol 41:, 7159–7163. [CrossRef] [PubMed]
    [Google Scholar]
  40. Place B. J. , Field J. A. . ( 2012; ). Identification of novel fluorochemicals in aqueous film-forming foams used by the US military. . Environ Sci Technol 46:, 7120–7127. [CrossRef] [PubMed]
    [Google Scholar]
  41. Rhoads K. R. , Janssen E. M. L. , Luthy R. G. , Criddle C. S. . ( 2008; ). Aerobic biotransformation and fate of N-ethyl perfluorooctane sulfonamidoethanol (N-EtFOSE) in activated sludge. . Environ Sci Technol 42:, 2873–2878. [CrossRef] [PubMed]
    [Google Scholar]
  42. Robbins J. M. , Ellis H. R. . ( 2012; ). Identification of critical steps governing the two-component alkanesulfonate monooxygenase catalytic mechanism. . Biochemistry 51:, 6378–6387. [CrossRef] [PubMed]
    [Google Scholar]
  43. Russell M. H. , Berti W. R. , Szostek B. , Buck R. C. . ( 2008; ). Investigation of the biodegradation potential of a fluoroacrylate polymer product in aerobic soils. . Environ Sci Technol 42:, 800–807. [CrossRef] [PubMed]
    [Google Scholar]
  44. Saitou N. , Nei M. . ( 1987; ). The neighbor-joining method: a new method for reconstructing phylogenetic trees. . Mol Biol Evol 4:, 406–425.[PubMed]
    [Google Scholar]
  45. Scherer H. W. . ( 2009; ). Sulfur in soils. . J Plant Nutr Soil Sci 172:, 326–335. [CrossRef]
    [Google Scholar]
  46. Schröder H. F. . ( 2003; ). Determination of fluorinated surfactants and their metabolites in sewage sludge samples by liquid chromatography with mass spectrometry and tandem mass spectrometry after pressurised liquid extraction and separation on fluorine-modified reversed-phase sorbents. . J Chromatogr A 1020:, 131–151. [CrossRef] [PubMed]
    [Google Scholar]
  47. Schultz M. M. , Barofsky D. F. , Field J. A. . ( 2004; ). Quantitative determination of fluorotelomer sulfonates in groundwater by LC MS/MS. . Environ Sci Technol 38:, 1828–1835. [CrossRef] [PubMed]
    [Google Scholar]
  48. Scott B. F. , Moody C. A. , Spencer C. , Small J. M. , Muir D. C. , Mabury S. A. . ( 2006; ). Analysis for perfluorocarboxylic acids/anions in surface waters and precipitation using GC–MS and analysis of PFOA from large-volume samples. . Environ Sci Technol 40:, 6405–6410. [CrossRef] [PubMed]
    [Google Scholar]
  49. Scott C. , Hilton M. E. , Coppin C. W. , Russell R. J. , Oakeshott J. G. , Sutherland T. D. . ( 2007; ). A global response to sulfur starvation in Pseudomonas putida and its relationship to the expression of low-sulfur-content proteins. . FEMS Microbiol Lett 267:, 184–193. [CrossRef] [PubMed]
    [Google Scholar]
  50. Shoeib M. , Harner T. , Lee S. C. , Lane D. , Zhu J. . ( 2008; ). Sorbent-impregnated polyurethane foam disk for passive air sampling of volatile fluorinated chemicals. . Anal Chem 80:, 675–682. [CrossRef] [PubMed]
    [Google Scholar]
  51. Sinclair E. , Kannan K. . ( 2006; ). Mass loading and fate of perfluoroalkyl surfactants in wastewater treatment plants. . Environ Sci Technol 40:, 1408–1414. [CrossRef] [PubMed]
    [Google Scholar]
  52. Suja F. , Pramanik B. K. , Zain S. M. . ( 2009; ). Contamination, bioaccumulation and toxic effects of perfluorinated chemicals (PFCs) in the water environment: a review paper. . Water Sci Technol 60:, 1533–1544. [CrossRef] [PubMed]
    [Google Scholar]
  53. Tamura K. , Nei M. , Kumar S. . ( 2004; ). Prospects for inferring very large phylogenies by using the neighbor-joining method. . Proc Natl Acad Sci U S A 101:, 11030–11035. [CrossRef] [PubMed]
    [Google Scholar]
  54. Tamura K. , Peterson D. , Peterson N. , Stecher G. , Nei M. , Kumar S. . ( 2011; ). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. . Mol Biol Evol 28:, 2731–2739. [CrossRef] [PubMed]
    [Google Scholar]
  55. van Berkel W. J. H. , Kamerbeek N. M. , Fraaije M. W. . ( 2006; ). Flavoprotein monooxygenases, a diverse class of oxidative biocatalysts. . J Biotechnol 124:, 670–689. [CrossRef] [PubMed]
    [Google Scholar]
  56. van der Ploeg J. R. , Cummings N. J. , Leisinger T. , Connerton I. F. . ( 1998; ). Bacillus subtilis genes for the utilization of sulfur from aliphatic sulfonates. . Microbiology 144:, 2555–2561. [CrossRef] [PubMed]
    [Google Scholar]
  57. van der Ploeg J. R. , Eichhorn E. , Leisinger T. . ( 2001; ). Sulfonate-sulfur metabolism and its regulation in Escherichia coli. . Arch Microbiol 176:, 1–8. [CrossRef] [PubMed]
    [Google Scholar]
  58. Van Hamme J. D. , Fedorak P. M. , Foght J. M. , Gray M. R. , Dettman H. D. . ( 2004; ). Use of a novel fluorinated organosulfur compound to isolate bacteria capable of carbon-sulfur bond cleavage. . Appl Environ Microbiol 70:, 1487–1493. [CrossRef] [PubMed]
    [Google Scholar]
  59. Wang N. , Szostek B. , Folsom P. W. , Sulecki L. M. , Capka V. , Buck R. C. , Berti W. R. , Gannon J. T. . ( 2005a; ). Aerobic biotransformation of 14C-labeled 8-2 telomer B alcohol by activated sludge from a domestic sewage treatment plant. . Environ Sci Technol 39:, 531–538. [CrossRef] [PubMed]
    [Google Scholar]
  60. Wang N. , Szostek B. , Buck R. C. , Folsom P. W. , Sulecki L. M. , Capka V. , Berti W. R. , Gannon J. T. . ( 2005b; ). Fluorotelomer alcohol biodegradation-direct evidence that perfluorinated carbon chains breakdown. . Environ Sci Technol 39:, 7516–7528. [CrossRef] [PubMed]
    [Google Scholar]
  61. Wang N. , Liu J. , Buck R. C. , Korzeniowski S. H. , Wolstenholme B. W. , Folsom P. W. , Sulecki L. M. . ( 2011; ). 6:2 fluorotelomer sulfonate aerobic biotransformation in activated sludge of waste water treatment plants. . Chemosphere 82:, 853–858. [CrossRef] [PubMed]
    [Google Scholar]
  62. Xu Y. R. , Mortimer M. W. , Fisher T. S. , Kahn M. L. , Brockman F. J. , Xun L. Y. . ( 1997; ). Cloning, sequencing, and analysis of a gene cluster from Chelatobacter heintzii ATCC 29600 encoding nitrilotriacetate monooxygenase and NADH:flavin mononucleotide oxidoreductase. . J Bacteriol 179:, 1112–1116.[PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.068932-0
Loading
/content/journal/micro/10.1099/mic.0.068932-0
Loading

Data & Media loading...

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