1887

Abstract

A denitrifying bacterium, designated strain FS, was isolated from anoxic digested sludge on oestradiol [17-oestra-1,3,5(10)-triene-3,17-diol] or testosterone (17-hydroxyandrost-4-en-3-one) as the sole source of carbon and energy with nitrate as the electron acceptor. Strain FS represents the first known bacterium to grow anaerobically on both oestradiol (C-18) and testosterone (C-19). Steroidal hormones were degraded completely by nitrate reduction to dinitrogen monoxide, which was further reduced to dinitrogen in stationary-phase cultures. Gram-negative cells were slightly curved rods, 0.3–0.5×0.6–1.6 μm in size, motile, non-fermentative, non-spore-forming and catalase- and oxidase-positive, showing optimal growth at pH 7.0, 28 °C and 0.1 % (w/v) NaCl. Beside steroidal hormones, the bacterium utilized only a narrow range of organic substrates with nitrate as the electron acceptor, including several fatty acids and glutamate. No aerobic or anaerobic growth occurred on liquid or solid complex media. Phylogenetic analysis of the 16S rRNA gene sequence showed that strain FS has no known close relatives and represents a distinct lineage within the . Together with the genera , , and (less than 88 % 16S rRNA gene sequence similarity to strain FS), it forms a phylogenetic cluster separated from the families , and . The quinone system of strain FS consisted exclusively of ubiquinone Q-8. The dominant polar lipids were diphosphatidylglycerol and phosphatidylethanolamine. Spermidine in combination with putrescine and traces of -homospermidine were the basic polyamines. The major fatty acids detected in testosterone- or heptanoate-grown cells were C and C 8, minor hydroxylated fatty acids were C 3-OH and C 3-OH. The G+C content of the DNA was 61.9 mol%. Based on the high 16S rRNA gene sequence divergence and different phenotypic properties from previously described gammaproteobacteria in combination with chemotaxonomic data, strain FS is considered to represent a new genus and species, for which the name gen. nov., sp. nov. is proposed. The type strain of is FS (=DSM 18526 =JCM 14622).

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2008-09-01
2024-04-19
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References

  1. Altenburger, P., Kämpfer, P., Makristathis, A., Lubitz, W. & Busse, H.-J.(1996). Classification of bacteria isolated from a medieval wall painting. J Biotechnol 47, 39–52.[CrossRef] [Google Scholar]
  2. Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W. & Lipman, D. J.(1997). Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25, 3389–3402.[CrossRef] [Google Scholar]
  3. Andersen, H. R., Siegrist, H., Halling-Sørensen, B. & Ternes, T. A.(2003). Fate of estrogens in a municipal sewage treatment plant. Environ Sci Technol 37, 4021–4026.[CrossRef] [Google Scholar]
  4. Auling, G., Busse, H.-J., Pilz, F., Webb, L., Kneifel, H. & Claus, D.(1991). Rapid differentiation by polyamine analysis of Xanthomonas strains from phytopathogenic pseudomonads and other members of the class Proteobacteria interacting with plants. Int J Syst Bacteriol 41, 223–228.[CrossRef] [Google Scholar]
  5. Bradford, M. M.(1976). A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248–254.[CrossRef] [Google Scholar]
  6. Bruce, R. A., Achenbach, L. A. & Coates, J. D.(1999). Reduction of (per)chlorate by a novel organism isolated from paper mill waste. Environ Microbiol 1, 319–329.[CrossRef] [Google Scholar]
  7. Busse, H.-J. & Auling, G.(1988). Polyamine pattern as a chemotaxonomic marker within the Proteobacteria. Syst Appl Microbiol 11, 1–8.[CrossRef] [Google Scholar]
  8. Cashion, P., Holder-Franklin, M. A., McCully, J. & Franklin, M.(1977). A rapid method for the base ratio determination of bacterial DNA. Anal Biochem 81, 461–466.[CrossRef] [Google Scholar]
  9. Colucci, M. S., Bork, H. & Topp, E.(2001). Persistence of estrogenic hormones in agricultural soils. I. 17β-Estradiol and estrone. J Environ Qual 30, 2070–2076.[CrossRef] [Google Scholar]
  10. Czajka, C. P. & Londry, K. L.(2006). Anaerobic biotransformation of estrogens. Sci Total Environ 367, 932–941.[CrossRef] [Google Scholar]
  11. D'Ans, J. & Lax, E.(1983).Taschenbuch für Chemiker und Physiker, 4th edn, vol. 1, Makroskopische physikalisch-chemische Eigenschaften. Berlin: Springer (in German).
  12. Fahrbach, M., Kuever, J., Meinke, R., Kämpfer, P. & Hollender, J.(2006).Denitratisoma oestradiolicum gen. nov., sp. nov., a 17β-oestradiol-degrading, denitrifying betaproteobacterium. Int J Syst Evol Microbiol 56, 1547–1552.[CrossRef] [Google Scholar]
  13. Fujii, K., Satomi, M., Morita, N., Motomura, T., Tanaka, T. & Kikuchi, S.(2003).Novosphingobium tardaugens sp. nov., an oestradiol-degrading bacterium isolated from activated sludge of a sewage treatment plant in Tokyo. Int J Syst Evol Microbiol 53, 47–52.[CrossRef] [Google Scholar]
  14. Gerhardt, P., Murray, R. G. E., Wood, W. A. & Krieg, N. R. (editors)(1994).Methods for General and Molecular Bacteriology. Washington, DC: American Society for Microbiology.
  15. Gregersen, T.(1978). Rapid method for distinction of Gram-negative from Gram-positive bacteria. Eur J Appl Microbiol Biotechnol 5, 123–127.[CrossRef] [Google Scholar]
  16. Guindon, S. & Gascuel, O.(2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52, 696–704.[CrossRef] [Google Scholar]
  17. Hamana, K. & Takeuchi, M.(1998). Polyamine profiles as chemotaxonomic markers within alpha, beta, gamma, delta, and epsilon subclasses of class Proteobacteria: distribution of 2-hydroxyputrescine and homospermidine. Microbiol Cult Collect 14, 1–14. [Google Scholar]
  18. Hamana, K., Okada, M., Saito, T. & Nogi, Y.(2000). Polyamine distribution profiles among some members of the gamma subclass of the class Proteobacteria. Microbiol Cult Collect 16, 51–61. [Google Scholar]
  19. Hamana, K., Sato, W., Gouma, K., Yu, J., Ino, Y., Umemura, Y., Mochizuki, C., Takatsuka, K., Kigure, Y. & other authors(2007). Cellular polyamine catalogues of the five classes of the phylum Proteobacteria: distributions of homospermidine within the class Alphaproteobacteria, hydroxyputrescine within the class Betaproteobacteria, norspermidine within the class Gammaproteobacteria, and spermidine within the classes Deltaproteobacteria and Epsilonproteobacteria. Ann Gunma Health Sci 27, 1–16. [Google Scholar]
  20. Hanselman, T. A., Graetz, D. A. & Wilkie, A. C.(2003). Manure-borne estrogens as potential environmental contaminants: a review. Environ Sci Technol 37, 5471–5478.[CrossRef] [Google Scholar]
  21. Hasegawa, M., Kishino, H. & Yano, T.(1985). Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22, 160–174.[CrossRef] [Google Scholar]
  22. Imhoff, J. F., Süling, J. & Petri, R.(1998). Phylogenetic relationships among the Chromatiaceae, their taxonomic reclassification and description of the new genera Allochromatium, Halochromatium, Isochromatium, Marichromatium, Thiococcus, Thiohalocapsa and Thermochromatium. Int J Syst Bacteriol 48, 1129–1143.[CrossRef] [Google Scholar]
  23. Jacobsen, A.-M., Lorenzen, A., Chapman, R. & Topp, E.(2005). Persistence of testosterone and 17β-estradiol in soils receiving swine manure or municipal biosolids. J Environ Qual 34, 861–871.[CrossRef] [Google Scholar]
  24. Jenkins, R. L., Wilson, E. M., Angus, R. A., Howell, W. M. & Kirk, M.(2003). Androstenedione and progesterone in the sediment of a river receiving paper mill effluent. Toxicol Sci 73, 53–59.[CrossRef] [Google Scholar]
  25. Jenkins, R. L., Wilson, E. M., Angus, R. A., Howell, W. M., Kirk, M., Moore, R., Nance, M. & Brown, A.(2004). Production of androgens by microbial transformation of progesterone in vitro: a model for androgen production in rivers receiving paper mill effluent. Environ Health Perspect 112, 1508–1511.[CrossRef] [Google Scholar]
  26. Jobling, S., Nolan, M., Tyler, C. R., Brighty, G. & Sumpter, J. P.(1998). Widespread sexual disruption in wild fish. Environ Sci Technol 32, 2498–2506.[CrossRef] [Google Scholar]
  27. Joss, A., Andersen, H., Ternes, T., Richle, P. R. & Siegrist, H.(2004). Removal of estrogens in municipal wastewater treatment under aerobic and anaerobic conditions: consequences for plant optimization. Environ Sci Technol 38, 3047–3055.[CrossRef] [Google Scholar]
  28. Jürgens, M. D., Holthaus, K. I. E., Johnson, A. C., Smith, J. J. L., Hetheridge, M. & Williams, R. J.(2002). The potential for estradiol and ethinylestradiol degradation in English rivers. Environ Toxicol Chem 21, 480–488.[CrossRef] [Google Scholar]
  29. Kämpfer, P. & Kroppenstedt, R. M.(1996). Numerical analysis of fatty acid patterns of coryneform bacteria and related taxa. Can J Microbiol 42, 989–1005.[CrossRef] [Google Scholar]
  30. Kim, M. K., Kim, Y.-J., Cho, D.-H., Yi, T.-H., Soung, N.-K. & Yang, D.-C.(2007).Solimonas soli gen. nov., sp. nov., isolated from soil of a ginseng field. Int J Syst Evol Microbiol 57, 2591–2594.[CrossRef] [Google Scholar]
  31. Kuever, J., Könneke, M., Galushko, A. & Drzyzga, O.(2001). Reclassification of Desulfobacterium phenolicum as Desulfobacula phenolica comb. nov. and description of strain SaxT as Desulfotignum balticum gen. nov., sp. nov. Int J Syst Evol Microbiol 51, 171–177. [Google Scholar]
  32. Layton, A. C., Gregory, B. W., Seward, J. R., Schultz, T. W. & Sayler, G. S.(2000). Mineralization of steroidal hormones by biosolids in wastewater treatment systems in Tennessee U.S.A. Environ Sci Technol 34, 3925–3931.[CrossRef] [Google Scholar]
  33. Levy, H. R. & Talalay, P.(1959). Bacterial oxidation of steroids. I. Ring A dehydrogenations by intact cells. J Biol Chem 234, 2009–2013. [Google Scholar]
  34. Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhukumar, Buchner, A., Lai, T., Steppi, S. & other authors(2004).arb: a software environment for sequence data. Nucleic Acids Res 32, 1363–1371.[CrossRef] [Google Scholar]
  35. Mesbah, M., Premachandran, U. & Whitman, W. B.(1989). Precise measurement of the G+C content of deoxyribonucleic acid by high-performance liquid chromatography. Int J Syst Bacteriol 39, 159–167.[CrossRef] [Google Scholar]
  36. Palleroni, N. J., Port, A. M., Chang, H.-K. & Zylstra, G. J.(2004).Hydrocarboniphaga effusa gen. nov., sp. nov., a novel member of the γ-Proteobacteria active in alkane and aromatic hydrocarbon degradation. Int J Syst Evol Microbiol 54, 1203–1207.[CrossRef] [Google Scholar]
  37. Sih, C. J. & Whitlock, H. W.(1968). Biochemistry of steroids. Annu Rev Biochem 37, 661–694.[CrossRef] [Google Scholar]
  38. Stolz, A., Busse, H.-J. & Kämpfer, P.(2007).Pseudomonas knackmussii sp. nov. Int J Syst Evol Microbiol 57, 572–576.[CrossRef] [Google Scholar]
  39. Stürmeyer, H., Overmann, J., Babenzien, H.-D. & Cypionka, H.(1998). Ecophysiological and phylogenetic studies of Nevskia ramosa in pure culture. Appl Environ Microbiol 64, 1890–1894. [Google Scholar]
  40. Sumpter, J. P. & Johnson, A. C.(2005). Lessons from endocrine disruption and their application to other issues concerning trace organics in the aquatic environment. Environ Sci Technol 39, 4321–4332.[CrossRef] [Google Scholar]
  41. Süßmuth, R., Eberspächer, J., Haag, R. & Springer, W.(1987).Biochemisch-mikrobiologisches Praktikum. Stuttgart: Thieme (in German).
  42. Talalay, P., Dobson, M. M. & Tapley, D. F.(1952). Oxidative degradation of testosterone by adaptive enzymes. Nature 170, 620–621.[CrossRef] [Google Scholar]
  43. Tamaoka, J. & Komagata, K.(1984). Determination of DNA base composition by reversed-phase high-performance liquid chromatography. FEMS Microbiol Lett 25, 125–128.[CrossRef] [Google Scholar]
  44. Thomas, K. V., Hurst, M. R., Matthiessen, P., McHugh, M., Smith, A. & Waldock, M. J.(2002). An assessment of in vitro androgenic activity and the identification of environmental androgens in United Kingdom estuaries. Environ Toxicol Chem 21, 1456–1461.[CrossRef] [Google Scholar]
  45. Tindall, B. J.(1990a). Lipid composition of Halobacterium lacusprofundi. FEMS Microbiol Lett 66, 199–202.[CrossRef] [Google Scholar]
  46. Tindall, B. J.(1990b). A comparative study of the lipid composition of Halobacterium saccharovorum from various sources. Syst Appl Microbiol 13, 128–130.[CrossRef] [Google Scholar]
  47. Widdel, F. & Bak, F.(1992). Gram-negative mesophilic sulfate-reducing bacteria. In The Prokaryotes. A Handbook on the Biology of Bacteria. Ecophysiology, Isolation, Identification, Applications, 2nd edn, pp. 3352–3378. Edited by A. Balows, H. G. Trüper, M. Dworkin, W. Harder & K. H. Schleifer. New York: Springer.
  48. Yokota, A., Akagawa-Matsushita, M., Hiraishi, A., Katayama, Y., Urakami, T. & Yamasato, K.(1992). Distribution of quinone systems in microorganisms: Gram-negative eubacteria. Bull Jpn Fed Cult Coll 8, 136–171. [Google Scholar]
  49. Yoshimoto, T., Nagai, F., Fujimoto, J., Watanabe, K., Mizukoshi, H., Makino, T., Kimura, K., Saino, H., Sawada, H. & Omura, H.(2004). Degradation of estrogens by Rhodococcus zopfii and Rhodococcus equi isolates from activated sludge in wastewater treatment plants. Appl Environ Microbiol 70, 5283–5289.[CrossRef] [Google Scholar]
  50. Young, C.-C., Kämpfer, P., Ho, M.-J., Busse, H.-J., Huber, B. E., Arun, A. B., Shen, F.-T., Lai, W.-A. & Rekha, P. D.(2007).Arenimonas malthae sp. nov., a gammaproteobacterium isolated from an oil-contaminated site. Int J Syst Evol Microbiol 57, 2790–2793.[CrossRef] [Google Scholar]
  51. Zhou, Y., Zhang, Y.-Q., Zhi, X.-Y., Wang, X., Dong, J., Chen, Y., Lai, R. & Li, W.-J.(2008). Description of Sinobacter flavus gen. nov., sp. nov., and proposal of Sinobacteriaceae fam. nov. Int J Syst Evol Microbiol 58, 184–189.[CrossRef] [Google Scholar]
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