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Volume 159, Issue Pt_8

Genomic and proteomic characterization of sp. NB4-1Y in relation to 6 : 2 fluorotelomer sulfonate biodegradation Free

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.

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2013-08-01
2024-04-20
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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 [View Article][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 [View Article]
     [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 [View Article][PubMed]
     [Google Scholar]
  7. Cook A. M., Smits T. H. M., Denger K. ( 2008). Sulfonates and Organotrophic Sulfite Metabolism 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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][PubMed]
     [Google Scholar]
  13. Ellis H. R. ( 2010). The FMN-dependent two-component monooxygenase systems. Arch Biochem Biophys 497:1–12 [View Article][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 [View Article][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 [View Article][PubMed]
     [Google Scholar]
  16. Felsenstein J. ( 1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791 [View Article]
     [Google Scholar]
  17. Froemel T., Knepper T. P. ( 2010). Biodegradation of fluorinated alkyl substances. Perfluorinated Alkylated Substances161–177 Whitacre D. M., DeVoogt P. New York: Springer;
     [Google Scholar]
  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 [View Article][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 [View Article][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 [View Article][PubMed]
     [Google Scholar]
  21. Karp P. D., Paley S., Romero P. ( 2002). The Pathway Tools software. Bioinformatics 18:Suppl 1S225–S232 [View Article][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 [View Article]
     [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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][PubMed]
     [Google Scholar]
  33. Murphy C. D. ( 2010). Biodegradation and biotransformation of organofluorine compounds. Biotechnol Lett 32:351–359 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article]
     [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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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 [View Article][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]
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Genomic and proteomic characterization of Gordonia sp. NB4-1Y in relation to 6 : 2 fluorotelomer sulfonate biodegradation
Microbiology 159, 1618 (2013); https://doi.org/10.1099/mic.0.068932-0
/content/journal/micro/10.1099/mic.0.068932-0
/content/journal/micro/10.1099/mic.0.068932-0
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