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Isolation of Iodide-Oxidizing Bacteria from Iodide-Rich Natural Gas Brines and Seawaters

Microbial Ecology volume 49, pages 547–557 (2005)Cite this article

Abstract

Iodide-oxidizing bacteria (IOB), which oxidize iodide (I−) to molecular iodine (I2), were isolated from iodide-rich (63 μM to 1.2 mM) natural gas brine waters collected from several locations. Agar media containing iodide and starch were prepared, and brine waters were spread directly on the media. The IOB, which appeared as purple colonies, were obtained from 28 of the 44 brine waters. The population sizes of IOB in the brines were 102 to 105 colony-forming units (CFU) mL−1. However, IOB were not detected in natural seawaters and terrestrial soils (fewer than 10 CFU mL−1 and 102 CFU g wet weight of soils−1, respectively). Interestingly, after the enrichment with 1 mM iodide, IOB were found in 6 of the 8 seawaters with population sizes of 103 to 105 CFU mL−1. 16S rDNA sequencing and phylogenetic analyses showed that the IOB strains are divided into two groups within the α-subclass of the Proteobacteria. One of the groups was phylogenetically most closely related to Roseovarius tolerans with sequence similarities between 94% and 98%. The other group was most closely related to Rhodothalassium salexigens, although the sequence similarities were relatively low (89% to 91%). The iodide-oxidizing reaction by IOB was mediated by an extracellular enzyme protein that requires oxygen. Radiotracer experiments showed that IOB produce not only I2 but also volatile organic iodine, which were identified as diiodomethane (CH2I2) and chloroiodomethane (CH2ClI). These results indicate that at least two types of IOB are distributed in the environment, and that they are preferentially isolated in environments in which iodide levels are very high. It is possible that IOB oxidize iodide in the natural environment, and they could significantly contribute to the biogeochemical cycling of iodine.

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References

  1. Allgaier M, Uphoff H, Felske A, Wagner-Dobler I (2003) Aerobic anoxygenic photosynthesis in Roseobacter clade bacteria from diverse marine habitats. Appl Environ Microbiol 69: 5051–5059

    Article  PubMed  Google Scholar 

  2. Almeida M, Filipe S, Humanes M, Maia MF, Melo R, Severino N, da, Silva JA, Frausto da, Silva JJ, Wever R (2001) Vanadium haloperoxidases from brown algae of the Laminariaceae family. Phytochemistry 57: 633–642

    Article  PubMed  Google Scholar 

  3. Amachi S, Kamagata Y, Kanagawa T, Muramatsu Y (2001) Bacteria mediate methylation of iodine in marine and terrestrial environments. Appl Environ Microbiol 67: 2718–2722

    Article  PubMed  Google Scholar 

  4. Amachi S, Kasahara M, Fujii T, Shinoyama H, Hanada S, Kamagata Y, Bam-nai T, Muramatsu Y (2004) Radiotracer experiments on biological volatilization of organic iodine from coastal seawaters. Geomicrobiology J 21: 481–488

    Article  Google Scholar 

  5. Amachi S, Kasahara M, Hanada S, Kamagata Y, Shinoyama H, Fujii T, Muramatsu Y (2003) Microbial participation in iodine volatilization from soils. Environ Sci Technol 37: 3885–3890

    Article  PubMed  Google Scholar 

  6. Amachi S, Muramatsu Y, Kamagata Y (2000) Radioanalytical determination of biogenic volatile iodine emitted from aqueous environmental samples. J Radioanal Nucl Chem 246: 337–341

    Article  Google Scholar 

  7. Behrens, H (1982) New insights into the chemical behavior of radioiodine in aquatic environments. In: Environmental Migration of Long-Lived Radionuclides, Proceedings of an International Symposium, International Atomic Energy Agency, Vienna. pp 27–40

  8. Bors J, Martens R (1992) The contribution of microbial biomass to the adsorption of radioiodide in soils. J Environ Radioact 15: 35–49

    Article  Google Scholar 

  9. Buraglio N, Aldahan A, Possnert G, Vintersved I (2001) 129I from the nuclear reprocessing facilities traced in precipitation and runoff in northern Europe. Environ Sci Technol 35: 1579–1586

    Article  PubMed  Google Scholar 

  10. Cohen BL (1985) The origin of I in soil and the 129I problem. Health Phys 49: 279–285

    PubMed  Google Scholar 

  11. Councell TB, Landa ER, Lovley DR (1997) Microbial reduction of iodate. Water, Air Soil Pollution 100: 99–106

    Google Scholar 

  12. Doudoroff M, Palleroni NJ (1974) Genus, I: Pseudomonas Migura 1894. In: Buchanan RE, Gibbons NE, Cowan ST, Holt JG, Liston J, Murray GE, Niven CF, Ravin AW, Stanier RY (Eds). Bergey’s Manual of Determinative Bacteriology, 8th ed, Williams & Wilkins, Baltimore, pp 217–243

    Google Scholar 

  13. Drews G, (1981) Rhodospirillum salexigens, spec. nov., an obligatory halophilic phototrophic bacterium. Arch Microbiol 130: 325–327

    Article  Google Scholar 

  14. Farhangrazi ZS, Sinclair R, Yamazaki I, Powers LS (1992) Haloperoxidase activity of Phanerochaete chrysosporium lignin peroxidases H2 and H8. Biochemistry 31: 10763–10768

    Article  PubMed  Google Scholar 

  15. Farrenkopf AM, Dollhopf ME, Chadhain SN, Luther GW, III Nealson KH (1997) Reduction of iodate in seawater by bacterium, Shewanella putrefaciens strain MR-4. Marine Chem 57: 347–354

    Article  Google Scholar 

  16. Fehn U, Snyder GT (2003) Origin of Iodine and 129I in Volcanic and Geothermal Fluids from the North Island of New Zealand: Impact for Subduction Zone Processes. Society of Economic Geologists Special Publication 10: 159–170

    Google Scholar 

  17. Franks SG, Dias RF, Freeman KH, Boles JR, Holba A, Fincannon AL, Jordan ED (2001) Carbon isotopic composition of organic acids in oil field waters, San Joaquin Basin, California, USA. Geochim Cosmochim Acta 65: 1301–1310

    Article  Google Scholar 

  18. Fuge R, Johnson CC (1986) The geochemistry of iodine. Environ Geochem Health 8: 31–54

    Google Scholar 

  19. Furtmuller PG, Jantschko W, Regelsberger G, Jakopitsch C, Arnhold J, Obinger C (2002) Reaction of lactoperoxidase compound I with halides and thiocyanate. Biochemistry 41: 11895–11900

    Article  PubMed  Google Scholar 

  20. Fuse H, Inoue H, Murakami K, Takimura O, Yamaoka Y (2003) Production of free and organic iodine by Roseovarius spp. FEMS Microbiol Lett 229: 189–194

    Article  PubMed  Google Scholar 

  21. Gonzalez JM, Covert JS, Whitman WB, Henriksen JR, Mayer F, Scharf B, Schmitt R, Buchan A, Fuhrman JA, Kiene RP, Moran MA 2003. Silicibacter pomeroyi sp. nov. and Roseovarius nubinhibens sp. nov., dimethylsulfoniopropionate-demethylating bacteria from marine environments. Int J Syst Evol Microbiol 53: 1261–1269

    Article  PubMed  Google Scholar 

  22. Gozlan RS (1968) Isolation of iodine-producing bacteria from aquaria. Antonie Van Leeuwenhoek 34: 226

    PubMed  Google Scholar 

  23. Gozlan RS, Margalith P (1973) Iodide oxidation by a marine bacterium. J Appl Bacteriol 36: 407–417

    PubMed  Google Scholar 

  24. Gozlan RS, Margalith P (1974) Iodide oxidation by Pseudomonas iodooxidans. J Appl Bacteriol 37: 493–499

    PubMed  Google Scholar 

  25. Hiraishi A (1992) Direct automated sequencing of 16S rDNA amplified by polymerase chain reaction from bacterial cultures without DNA purification. Lett Appl Microbiol 15: 210–213

    PubMed  Google Scholar 

  26. Hold GL, Smith EA, Rapp MS, Maas EW, Moore ERB, Stroempl C, Stephen JR, Prosser JI, Birkbeck TH, Gallacher S (2001) Characterisation of bacterial communities associated with toxic and non-toxic dinoflagellates: Alexandrium spp. and Scrippsiella trochoidea. FEMS Microbiol Ecol 37: 161–173

    Article  Google Scholar 

  27. Imhoff JF, Petri R, Suling J (1998) Reclassification of species of the spiral-shaped phototrophic purple non-sulfur bacteria of the alpha-Proteobacteria: description of the new genera Phaeospirillum gen. nov., Rhodovibrio gen. nov., Rhodothalassium gen. nov. and Roseospira gen. nov. as well as transfer of Rhodospirillum fulvum to Phaeospirillum fulvum comb. nov., of Rhodospirillum molischianum to Phaeospirillum molischianum comb. nov., of Rhodospirillum salinarum to Rhodovibrio salexigens. Int J Syst Bacteriol 48: 793–798

    PubMed  Google Scholar 

  28. Jakopitsch C, Regelsberger G, Furtmuller PG, Ruker F, Peschek GA, Obinger C (2001) Catalase-peroxidase from Synechocystis is capable of chlorination and bromination reactions. Biochem Biophys Res Commun 287: 682–687

    Article  PubMed  Google Scholar 

  29. Labrenz M, Collins MD, Lawson PA, Tindall BJ, Schumann P, Hirsch P (1999) Roseovarius tolerans gen. nov., sp. nov., a budding bacterium with variable bacteriochlorophyll a production from hypersaline Ekho Lake. Int J Syst Bacteriol 49: 137–147

    PubMed  Google Scholar 

  30. McDonnell G, Russell AD (1999) Antiseptics and disinfectants: activity, action, and resistance. Clin Microbiol Rev 12: 147–179

    PubMed  Google Scholar 

  31. Moran JE, Oktay S, Santschi PH, Schink DR (1999) Atmospheric dispersal of 129iodine from nuclear fuel reprocessing facilities. Environ Sci Technol 33: 2536–2542

    Article  Google Scholar 

  32. Muramatsu Y, Fehn U, Yoshida S (2001) Recycling of iodine in fore-arc areas: evidence from the iodine brines in Chiba, Japan. Earth Planet Sci Lett 192: 583–593

    Article  Google Scholar 

  33. Muramatsu Y, Yoshida S (1999) Effects of microorganisms on the fate of iodine in the soil environment. Geomicrobiol J 16: 85–93

    Article  Google Scholar 

  34. Saito N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425

    PubMed  Google Scholar 

  35. Tsunogai S, Sase T (1969) Formation of iodide-iodine in the ocean. Deep-Sea Res 16: 489–496

    Google Scholar 

  36. Vandecasteele CM Van, Hees M, Hardeman F, Voigt G, Howard BJ (2000) The true absorption of 131I, and its transfer to milk in cows given different stable iodine diets. J Envrion Radioactiv 47: 301–317

    Article  Google Scholar 

  37. Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173: 697–703

    PubMed  Google Scholar 

  38. Wong GTF (1980) The stability of dissolved inorganic species of iodine in seawater. Mar Chem 9: 13–24

    Article  Google Scholar 

  39. Wong GTF (1982) The stability of molecular iodine in seawater. Mar Chem 11: 91–95

    Article  Google Scholar 

  40. Wong GTF (1991) The marine geochemistry of iodine. Rev Aquat Sci 4: 45–73

    Google Scholar 

  41. Wong GTF, Brewer PG (1977) The marine chemistry of iodine in anoxic basins. Geochim Cosmochim Acta 41: 151–159

    Article  Google Scholar 

  42. Wong GTF, Zhang L-S (2003) Seasonal variations in the speciation of dissolved iodine in the Chesapeake Bay. Estuarine Coastal Shelf Sci 56: 1093–1106

    Article  Google Scholar 

  43. Yoshida S, Muramatsu Y, Uchida S (1992) Studies on the sorption of I− (iodide) and IO −3 (iodate) onto andosols. Water, Air, and Soil Pollution 63: 321–329

    Google Scholar 

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Acknowledgments

We thank K. Redeker (Queen’s University of Belfast) for the critical reading of the manuscript; S. Yoshida (National Institute of Radiological Sciences, Japan) and G. Snyder (Rice University) for their valuable comments and kind suggestions throughout this study; K. Kimura (Chiba University), N. Machida (Chiba University), Y. Mishima (Chiba University), and S. Yamazaki (Tokyo Nuclear Service Co.) for their technical support. We are also grateful to the following iodine-producing companies for providing brine samples: Kanto Natural Gas Development Co., Nippoh Chemical Co., Godo-Shigen-Sangyo Co., Ise Chemical Co., Konoura Gas and Water Office, and Teikoku Oil Co. This work was made possible by research grants from the Forum on Iodine Utilization and the Hamaguchi Foundation for the Advancement of Biochemistry to S. A.

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Authors and Affiliations

  1. Department of Bioresources Chemistry, Chiba University, Matsudo-shi, Chiba, 271-8510, Japan

    Seigo Amachi, Yukako Akiyama, Kazumi Miyazaki, Sayaka Yoshiki, Hirofumi Shinoyama & Takaaki Fujii

  2. Department of Chemistry, Gakushuin University, Toshima-ku, Tokyo, 171-8588, Japan

    Yasuyuki Muramatsu

  3. Institute for Biological Resources and Functions, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Ibaraki, 305-8566, Japan

    Satoshi Hanada & Yoichi Kamagata

  4. National Institute of Radiological Sciences, Inage–ku, Chiba–shi, 263-8555, Japan

    Tadaaki Ban-nai

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  1. Seigo Amachi
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Correspondence to Seigo Amachi.

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Amachi, S., Muramatsu, Y., Akiyama, Y. et al. Isolation of Iodide-Oxidizing Bacteria from Iodide-Rich Natural Gas Brines and Seawaters. Microb Ecol 49, 547–557 (2005). https://doi.org/10.1007/s00248-004-0056-0

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  • DOI: https://doi.org/10.1007/s00248-004-0056-0

Keywords

  • Iodine
  • Iodate
  • CH2I2
  • Marine Broth
  • Chiba Prefecture