1887

Abstract

The goal of this project was to isolate representative Fe(III)-reducing bacteria from kaolin clays that may influence iron mineralogy in kaolin. Two novel dissimilatory Fe(III)-reducing bacteria, strains G12 and G13, were isolated from sedimentary kaolin strata in Georgia (USA). Cells of strains G12 and G13 were motile, non-spore-forming regular rods, 1–2 μm long and 0.6 μm in diameter. Cells had one lateral flagellum. Phylogenetic analyses using the 16S rRNA gene sequence of the novel strains demonstrated their affiliation to the genus . Strain G12 was most closely related to (94.7 %) and (94.1 %). Strain G13 was most closely related to (95.3 %) and (95.1 %). Based on phylogenetic analyses and phenotypic differences between the novel isolates and other closely related species of the genus , the isolates are proposed as representing two novel species, sp. nov. (type strain G12=ATCC BAA-1139=JCM 12999) and sp. nov. (type strain G13=ATCC BAA-1140=DSM 17153=JCM 13000). Another isolate, strain R7, was derived from a primary kaolin deposit in Russia. The cells of strain R7 were motile, spore-forming, slightly curved rods, 0.6×2.0–6.0 μm in size and with up to six peritrichous flagella. Strain R7 was capable of reducing Fe(III) only in the presence of a fermentable substrate. 16S rRNA gene sequence analysis demonstrated that this isolate is unique, showing less than 92 % similarity to bacteria of the phyletic group, including ‘’ (90.2 %), (90.6 %), (90.9 %) and (91.5 %). On the basis of phylogenetic analysis and physiological tests, strain R7 is proposed to represent a novel genus and species, gen. nov., sp. nov. (type strain R7=DSM 17108=ATCC BAA-1133), in the group.

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2007-01-01
2024-11-05
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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 [CrossRef]
    [Google Scholar]
  2. Avakyan Z. A., Platov Y. T., Khaliullova R. A., Turova E. S., Karavaiko G. I., Maslennikova G. N., Vodyanitskii Y. N. 1997; Method of bleaching of argillaceous ceramic materials . Russian Federation Patent no: 2083527
    [Google Scholar]
  3. Balch W. E., Fox G. E., Magrum L. J., Woese C. R., Wolfe R. S. 1979; Methanogens: reevaluation of a unique biological group. Microbiol Rev 43:260–296
    [Google Scholar]
  4. Beveridge T. J. 1999; Structures of Gram-negative cell walls and their derived membrane vesicles. J Bacteriol 181:4725–4733
    [Google Scholar]
  5. Bhushan B., Halasz A., Hawari J. 2006; Effect of iron(III), humic acids and anthraquinone-2,6-disulfonate on biodegradation of cyclic nitramines by Clostridium sp. EDB2. J Appl Microbiol 100:555–563 [CrossRef]
    [Google Scholar]
  6. Biebl H., Schwab-Hanisch H., Sproer C., Lunsdorf H. 2000; Propionispora vibrioides , nov. gen., nov. sp., a new Gram-negative, spore-forming anaerobe that ferments sugar alcohols. Arch Microbiol 174:239–247 [CrossRef]
    [Google Scholar]
  7. Borch T., Inskeep W. P., Harwood J. A., Gerlach R. 2005; Impact of ferrihydrite and anthraquinone-2,6-disulfonate on the reductive transformation of 2,4,6-trinitrotoluene by a Gram-positive fermenting bacterium. Environ Sci Technol 39:7126–7133 [CrossRef]
    [Google Scholar]
  8. Caccavo F., Lonergan D. J., Lovley D. R., Davis M., Stolz J. F., McInerney M. J. 1994; Geobacter sulfurreducens sp. nov., a hydrogen- and acetate-oxidizing dissimilatory metal-reducing microorganism. Appl Environ Microbiol 60:3752–3759
    [Google Scholar]
  9. 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]
  10. Ciofu O., Beveridge T. J., Kadurugamuwa J. L., Walther-Rasmussen J., Hoiby N. 2000; Chromosomal β -lactamase is packaged into membrane vesicles and secreted from Pseudomonas aeruginosa . J Antimicrob Chemother 45:9–13
    [Google Scholar]
  11. Cline J. D. 1969; Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr 14:454–458 [CrossRef]
    [Google Scholar]
  12. Coates J. D., Phillips E. J., Lonergan D. J., Jenter H., Lovley D. R. 1996; Isolation of Geobacter species from diverse sedimentary environments. Appl Environ Microbiol 62:1531–1536
    [Google Scholar]
  13. Coates J. D., Bhupathiraju V. K., Achenbach L. A., McInerney M. J., Lovley D. R. 2001; Geobacter hydrogenophilus, Geobacter chapellei and Geobacter grbiciae , three new, strictly anaerobic, dissimilatory Fe(III)-reducers. Int J Syst Evol Microbiol 51:581–588
    [Google Scholar]
  14. Collins M. D., Lawson P. A., Willems A., Cordoba J. J., Fernandez-Garayzabal J., Garcia P., Cai J., Hippe H., Farrow J. A. E. 1994; The phylogeny of the genus Clostridium : proposal of five new genera and eleven new species combinations. Int J Syst Bacteriol 44:812–826 [CrossRef]
    [Google Scholar]
  15. Dobbin P. S., Carter J. P., San Juan C. G.-S., von Hobe M., Powell A. K., Richardson D. J. 1999; Dissimilatory Fe(III) reduction by Clostridium beijerinckii isolated from freshwater sediment using Fe(III) maltol enrichment. FEMS Microbiol Lett 176:131–138 [CrossRef]
    [Google Scholar]
  16. Dorward D. W., Garon C. F., Judd R. C. 1989; Export and intercellular transfer of DNA via membrane blebs of Neisseria gonorrhoeae . J Bacteriol 171:2499–2505
    [Google Scholar]
  17. Dorward D. W., Garon C. F. 1990; DNA is packaged within membrane-derived vesicles of Gram-negative but not Gram-positive bacteria. Appl Environ Microbiol 56:1960–1962
    [Google Scholar]
  18. Elzea Kogel J., Pickering S. M. Jr, Shelobolina E. S., Chowns T. M., Yuan J., Avant D. M. Jr 2002 The Georgia Kaolins: Geology and Utilization Littleton, CO, USA: Society for Mining, Metallurgy, and Exploration;
    [Google Scholar]
  19. Forsberg C. W., Beveridge T. J., Hellstrom A. 1981; Cellulase and xylanase release from Bacteroides succinogenes and its importance in the rumen environment. Appl Environ Microbiol 42:886–896
    [Google Scholar]
  20. Gonzalez J. M., Saiz-Jimenez C. 2002; A fluorimetric method for the estimation of G+C mol% content in microorganisms by thermal denaturation temperature. Environ Microbiol 4:770–773 [CrossRef]
    [Google Scholar]
  21. Gonzalez J. M., Saiz-Jimenez C. 2004 Using the iCycler iQ® Detection System to Estimate Microbial DNA base composition from Melting Curves Hercules, CA, USA: Bio-Rad Laboratories, Inc;
    [Google Scholar]
  22. Grenier D., Mayrand D. 1987; Functional characterization of extracellular vesicles produced by Bacteroides gingivalis . Infect Immun 55:111–117
    [Google Scholar]
  23. Hobbie J. E., Daley R. J., Jasper S. 1977; Use of nuclepore filters for counting bacteria by fluorescence microscopy. Appl Environ Microbiol 33:1225–1228
    [Google Scholar]
  24. Hungate R. E. 1969; A roll tube method for cultivation of strict anaerobes. Methods Microbiol 3B:117–132
    [Google Scholar]
  25. Hurst V. J., Pickering S. M. Jr 1997; Origin and classification of Coastal Plain kaolins, southeastern USA, and the role of groundwater and microbial action. Clays Clay Miner 45:274–285 [CrossRef]
    [Google Scholar]
  26. Kadurugamuwa J. L., Beveridge T. J. 1996; Bacteriolytic effect of membrane vesicles from Pseudomonas aeruginosa on other bacteria including pathogens: conceptually new antibiotics. J Bacteriol 178:2767–2774
    [Google Scholar]
  27. Kadurugamuwa J. L., Mayer A., Messner P., Sara M., Sleytr U. B., Beveridge T. J. 1998; S-layered Aneurinibacillus and Bacillus spp. are susceptible to the lytic action of Pseudomonas aeruginosa membrane vesicles. J Bacteriol 180:2306–2311
    [Google Scholar]
  28. Kane M. D., Breznak J. A. 1991; Acetonema longum gen. nov. sp. nov. an H2/CO2 acetogenic bacterium from the termite, Pterotermes occidentis . Arch Microbiol 156:91–98 [CrossRef]
    [Google Scholar]
  29. Kappler A., Benz M., Schink B., Brune A. 2004; Electron shuttling via humic acids in microbial iron(III) reduction in a freshwater sediment. FEMS Microbiol Ecol 47:85–92 [CrossRef]
    [Google Scholar]
  30. Kashefi K., Lovley D. R. 2000; Reduction of Fe(III), Mn(IV), and toxic metals at 100 °C by Pyrobaculum islandicum . Appl Environ Microbiol 66:1050–1056 [CrossRef]
    [Google Scholar]
  31. Kim G. T., Hyun M. S., Chang I. S., Kim H. J., Park H. S., Kim B. H., Kim S. D., Wimpenny J. W. T., Weightman A. J. 2005; Dissimilatory Fe(III) reduction by an electrochemically active lactic acid bacterium phylogenetically related to Enterococcus gallinarum isolated from submerged soil. J Appl Microbiol 99:978–987 [CrossRef]
    [Google Scholar]
  32. Kobayashi H., Uematsu K., Hirayama H., Horikoshi K. 2000; Novel toluene elimination system in a toluene-tolerant microorganism. J Bacteriol 182:6451–6455 [CrossRef]
    [Google Scholar]
  33. Komadel P., Stucki J. W. 1988; Quantitative assay of minerals for Fe2+ and Fe3+ using 1,10-phenanthroline; III, A rapid photochemical method. Clays Clay Miner 36:379–381 [CrossRef]
    [Google Scholar]
  34. Kuehn M. J., Kesty N. C. 2005; Bacterial outer membrane vesicles and the host-pathogen interaction. Genes Dev 19:2645–2655 [CrossRef]
    [Google Scholar]
  35. Küsel K., Dorsch T., Acker G., Stackebrandt E. 1999; Microbial reduction of Fe(III) in acidic sediments: isolation of Acidiphilium cryptum JF-5 capable of coupling the reduction of Fe(III) to the oxidation of glucose. Appl Environ Microbiol 65:3633–3640
    [Google Scholar]
  36. Lee E.-Y., Cho K.-S., Ryu H. W., Chang Y. K. 1999; Microbial removal of Fe(III) impurities from clay using dissimilatory iron reducers. J Biosci Bioeng 87:397–399 [CrossRef]
    [Google Scholar]
  37. Li Z., Clarke A. J., Beveridge T. J. 1998; Gram-negative bacteria produce membrane vesicles which are capable of killing other bacteria. J Bacteriol 180:5478–5483
    [Google Scholar]
  38. Lovley D. R., Phillips E. J. 1986a; Organic matter mineralization with reduction of ferric iron in anaerobic sediments. Appl Environ Microbiol 51:683–689
    [Google Scholar]
  39. Lovley D. R., Phillips E. J. P. 1986b; Availability of ferric iron for microbial reduction in bottom sediments of the freshwater tidal Potomac River. Appl Environ Microbiol 52:751–757
    [Google Scholar]
  40. Lovley D. R., Phillips E. J. P. 1988; Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl Environ Microbiol 54:1472–1480
    [Google Scholar]
  41. Lovley D. R., Stolz J. F., Nord G. L., Phillips E. J. P. 1987; Anaerobic production of magnetite by a dissimilatory iron-reducing microorganism. Nature 330:252–254 [CrossRef]
    [Google Scholar]
  42. Lovley D. R., Giovannoni S. J., White D. C., Champine J. E., Phillips E. J. P., Gorby Y. A., Goodwin S. 1993; Geobacter metallireducens gen. nov. sp. nov. a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals. Arch Microbiol 159:336–344 [CrossRef]
    [Google Scholar]
  43. Lovley D. R., Holmes D. E., Nevin K. P. 2004; Dissimilatory Fe(III) and Mn(IV) reduction. Adv Microb Physiol 49:219–286
    [Google Scholar]
  44. Manceau A., Lanson B., Drits V. A., Chateigner D., Gates W. P., Wu J., Huo D., Stucki J. W. 2000; Oxidation-reduction mechanism of iron in dioctahedral smectites: I. Crystal chemistry of oxidized reference nontronites. Am Mineral 85:133–152
    [Google Scholar]
  45. Miller T. L., Wolin M. J. 1974; A serum bottle modification of the Hungate technique for cultivating obligate anaerobes. Appl Microbiol 27:985–987
    [Google Scholar]
  46. Osipov G. A., Turova E. S. 1997; Studying species composition of microbial communities with the use of gas chromatography-mass spectrometry: microbial community of kaolin. FEMS Microbiol Rev 20:437–446 [CrossRef]
    [Google Scholar]
  47. Park H. S., Kim B. H., Kim H. S., Kim H. J., Kim G. T., Kim M., Chang I. S., Park Y. K., Chang H. I. 2001; A novel electrochemically active and Fe(III) reducing bacterium phylogenetically related to Clostridium butyricum isolated from a microbial fuel cell. Anaerobe 7:297–306 [CrossRef]
    [Google Scholar]
  48. Phillips E. J. P., Lovley D. R. 1987; Determination of Fe(III) and Fe(II) in oxalate extracts of sediment. Soil Sci Soc Am J 51:938–941 [CrossRef]
    [Google Scholar]
  49. Schauder R., Schink B. 1989; Anaerovibrio glycerini sp. nov., an anaerobic bacterium fermenting glycerol to propionate, cell matter, and hydrogen. Arch Microbiol 152:473–478 [CrossRef]
    [Google Scholar]
  50. Shelobolina E. S., Parfenova E. Y., Avakyan Z. A. 1999; Microorganisms of kaolins and their role in the processes of iron solubilization and transformation. In Biohydrometallurgy and the Environment Toward the Mining of the 21st Century , part A pp  559–568 Edited by Amils A., Ballester A. Amsterdam: Elsevier;
    [Google Scholar]
  51. Shelobolina E. S., Gaw VanPraagh C., Lovley D. R. 2003; Use of ferric and ferrous iron containing minerals for respiration by Desulfitobacterium frappieri . Geomicrobiology J 20:143–156 [CrossRef]
    [Google Scholar]
  52. Shelobolina E. S., Sullivan S., O'Neill K. R., Nevin K. P., Lovley D. R. 2004; Isolation, characterization, and U(VI)-reducing potential of a facultatively anaerobic, acid-resistant bacterium from low-pH, nitrate- and U(VI)-contaminated subsurface sediment and description of Salmonella subterranea sp. nov. Appl Environ Microbiol 70:2959–2965 [CrossRef]
    [Google Scholar]
  53. Shelobolina E. S., Pickering S. M. Jr, Lovley D. R. 2005; Fe-cycle bacteria from industrial clays mined in Georgia, USA. Clays Clay Miner 53:580–586 [CrossRef]
    [Google Scholar]
  54. Solodkii N. F. 1995; Eluvial Kaolin from the Zhuravlinyi Log Deposit as a New Source of High-Quality Material for Fine Ceramics Production . An Analytical Review Moscow: VNIIESM;
    [Google Scholar]
  55. Stankewich J. P., Cosenza B. J., Shigo A. L. 1971; Clostridium quercicolum , sp. nov., isolated from discolored tissues in living oak trees. Antonie van Leeuwenhoek 37:299–302 [CrossRef]
    [Google Scholar]
  56. Straub K., Hanzlik M., Buchholz-Cleven B. E. 1998; The use of biologically produced ferrihydrite for the isolation of novel iron-reducing bacteria. Syst Appl Microbiol 21:442–449 [CrossRef]
    [Google Scholar]
  57. Strömpl C., Tindall B. J., Jarvis G. N., Lünsdorf H., Moore E. R. B., Hippe H. 1999; A re-evaluation of the taxonomy of the genus Anaerovibrio , with the reclassification of Anaerovibrio glycerini as Anaerosinus glycerini gen.nov., comb. nov., and Anaerovibrioburkinabensis as Anaeroarcus burkinensis [corrig.] gen. nov., comb. nov. Int J Syst Bacteriol 49:1861–1872 [CrossRef]
    [Google Scholar]
  58. Strömpl C., Tindall B. J., Lünsdorf H., Wong T.-Y., Moore E. R., Hippe H. 2000; Reclassification of Clostridium quercicolum as Dendrosporobacter quercicolus gen. nov., comb. nov. Int J Syst Evol Microbiol 50:101–106 [CrossRef]
    [Google Scholar]
  59. Stucki J. W. 1981; The quantitative assay of minerals for Fe2+ and Fe3+ using 1,10-phenanthroline: II. A photochemical method. Soil Sci Soc Am J 45:638–641 [CrossRef]
    [Google Scholar]
  60. Sung Y., Fletcher K. E., Ritalahiti K. M., Apkarian R. P., Ramos-Hernandez N., Sanford R. A., Mesbah N. M., Loffler F. E. 2006; Geobacter lovleyi sp nov strain SZ, a novel metal-reducing and tetrachloroethene-dechlorinating bacterium. Appl Environ Microbiol 72:2775–2782 [CrossRef]
    [Google Scholar]
  61. Swofford D. 1998 paup*: Phylogenetic analysis using parsimony (*and other methods), version 4 Sunderland, MA: Sinauer Associates;
    [Google Scholar]
  62. Turova E. S., Avakyan Z. A., Karavaiko G. I. 1996; The role of a bacterial community in transformation of iron minerals in kaolin. Microbiology (English translation of Mikrobiologiya ) 65:837–843
    [Google Scholar]
  63. Vodyanitskii Y. N., Turova E. S., Avakyan Z. A., Karavaiko G. I. 1997; Studying anaerobiosis in a model experiment with kaolin. Eurasian Soil Sci 30:747–757
    [Google Scholar]
  64. Wensink J., Witholt B. 1981; Outer-membrane vesicles released by normally growing Escherichia coli contain very little lipoprotein. Eur J Biochem 116:331–335 [CrossRef]
    [Google Scholar]
  65. Whitchurch C. B., Tolker-Nielsen T., Ragas P. C., Mattick J. S. 2002; Extracellular DNA required for bacterial biofilm formation. Science 295:1487 [CrossRef]
    [Google Scholar]
  66. Woo P. C. Y., Teng J. L. L., Leung K. W., Lau S. K. P., Woo G. K. S., Wong A. C. Y., Wong M. K. M., Yuen K. Y. 2005; Anaerospora hongkongensis gen. nov. sp. nov. a novel genus and species with ribosomal DNA operon heterogeneity isolated from an intravenous drug abuser with pseudobacteremia. Microbiol Immunol 49:31–39 [CrossRef]
    [Google Scholar]
  67. Yaron S., Kolling G. L., Simon L., Matthews K. R. 2000; Vesicle-mediated transfer of virulence genes from Escherichia coli O157: H7 to other enteric bacteria. Appl Environ Microbiol 66:4414–4420 [CrossRef]
    [Google Scholar]
  68. Zhou L., Srisatjaluk R., Justus D. E., Doyle R. J. 1998; On the origin of membrane vesicles in Gram-negative bacteria. FEMS Microbiol Lett 163:223–228 [CrossRef]
    [Google Scholar]
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