Extremophiles

, Volume 13, Issue 4, pp 695–705 | Cite as

Enrichment and isolation of Bacillus beveridgei sp. nov., a facultative anaerobic haloalkaliphile from Mono Lake, California, that respires oxyanions of tellurium, selenium, and arsenic

  • S. M. Baesman
  • J. F. Stolz
  • T. R. Kulp
  • Ronald S. Oremland
Original Paper

Abstract

Mono Lake sediment slurries incubated with lactate and tellurite [Te(IV)] turned progressively black with time because of the precipitation of elemental tellurium [Te(0)]. An enrichment culture was established from these slurries that demonstrated Te(IV)-dependent growth. The enrichment was purified by picking isolated black colonies from lactate/Te(IV) agar plates, followed by repeated streaking and picking. The isolate, strain MLTeJB, grew in aqueous Te(IV)-medium if provided with a small amount of sterile solid phase material (e.g., agar plug; glass beads). Strain MLTeJB grew at high concentrations of Te(IV) (~8 mM) by oxidizing lactate to acetate plus formate, while reducing Te(IV) to Te(0). Other electron acceptors that were found to sustain growth were tellurate, selenate, selenite, arsenate, nitrate, nitrite, fumarate and oxygen. Notably, growth on arsenate, nitrate, nitrite and fumarate did not result in the accumulation of formate, implying that in these cases lactate was oxidized to acetate plus CO2. Strain MLTeJB is a low G + C Gram positive motile rod with pH, sodium, and temperature growth optima at 8.5–9.0, 0.5–1.5 M, and 40°C, respectively. The epithet Bacillus beveridgei strain MLTeJBT is proposed.

Keywords

Alkaliphile ecology, systematics Anaerobic bacteria Halophile: ecology, biotechnology, phylogeny, genetics, taxonomy, enzymes Isolation and characterization Metal oxidation and reduction Alkaliphiles: systematics, ecology, phylogeny 

References

  1. Averèzi C, Truner RJ, Pommier J, Weiner JH, Giordano C, Vermégio (1997) Tellurite reductase activity of nitrate reductase is responsible for basal resistance of Escherichia coli to tellurite. Microbiology 143:1181–1189CrossRefGoogle Scholar
  2. Baesman SN, Bullen TD, Dewald J, Zhang D, Curran S, Islam FS, Beveridge TJ, Oremland RS (2007) Formation of tellurium nanocrystals during anaerobic growth of bacteria that use Te oxyanions as respiratory electron acceptors. Appl Environ Microbiol 73:2135–2143PubMedCrossRefGoogle Scholar
  3. Cooper CW (1972) Tellurium: element and geochemistry. In: Fairbridge RW (ed) The encyclopedia of geochemistry and environmental sciences, van Nostrand Reinhold Co., New York, pp 1164–1165Google Scholar
  4. Csotonyi JT, Stackebrandt E, Yurkov V (2006) Anaerobic respiration on tellurate and other metalloids in bacteria from hydrothermal vent fields in the eastern Pacific Ocean. Appl Environ Microbiol 72:4950–4956PubMedCrossRefGoogle Scholar
  5. Fisher JC, Hollibaugh JT (2008) Selenate-dependent anaerobic arsenite oxidation by a bacterium from Mono Lake, California. Appl Environ Microbiol 74:2588–2594PubMedCrossRefGoogle Scholar
  6. Hein JR, Koschinsky A, Halliday AN (2003) Global occurrence of tellurium-rich ferromanganese crusts and a model for the enrichment of tellurium. Geochim Cosmochim Acta 67:1117–1127CrossRefGoogle Scholar
  7. Herbel MJ, Switzer Blum J, Borglin S, Oremland RS (2003) Reduction of elemental selenium to selenide: experiments with anoxic sediments and bacteria that respire Se-oxyanions. Geomicrobiol J 20:587–602CrossRefGoogle Scholar
  8. Hermann M, Noll KM, Wolfe RS (1986) Improved agar bottle plate for isolation of methanogens or other anaerobes in a defined gas atmosphere. Appl Environ Microbiol 51:1124–1126PubMedGoogle Scholar
  9. Hobbie JE, Daley RL, Jaspar S (1977) Use of nuclepore filters for counting bacteria for fluorescent microscopy. Appl Environ Microbiol 33:1225–1228PubMedGoogle Scholar
  10. Hoeft SE, Kulp TR, Stolz JF, Hollibaugh JT, Oremland RS (2004) Dissimilatory arsenate reduction with sulfide as the electron donor: experiments with Mono Lake water and isolation of strain MLMS-1, a chemoautotrophic arsenate-respirer. Appl Environ Microbiol 70:2741–2747PubMedCrossRefGoogle Scholar
  11. Hollibaugh JT, Budinoff C, Hollibaugh RA, Ransom B, Bano N (2006) Sulfide oxidation coupled to arsenate reduction by a diverse microbial community in a soda lake. Appl Environ Microbiol 72:2043–2049PubMedCrossRefGoogle Scholar
  12. Huber R, Sacher M, Vollmann A, Huber H, Rose D (2000) Respiration of arsenate and selenate by hyperthermophilic archaea. Sys Appl Microbiol 23:305–314Google Scholar
  13. Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ (1998) Multiple sequence alignment with Clustal X. Trends Biochem Sci 23:403–405PubMedCrossRefGoogle Scholar
  14. Kulp TR, Pratt LM (2004) Speciation and weathering of selenium in Upper Cretaceous chalk and shale from South Dakota and Wyoming, USA. Geochim Cosmochim Acta 68:3678–3701CrossRefGoogle Scholar
  15. Lee J-H, Kim M-G, Yoo B, Myung NV, Maeng I, Lee T, Dohnalkova AC, Frederickson JK, Sadowsky MJ, Hur H-G (2007) Biogenic formation of photoactive arsenic-sulfide nanotubes by Shewanella sp. strain HN-41. Proc Natl Acad Sci USA 104:20410–20415PubMedCrossRefGoogle Scholar
  16. Liu A, Garcia-Dominguez E, Rhine E, Young LY (2004) A novel arsenate respiring isolate that can utilize aromatic substrates. FEMS Microbiol Ecol 48:323–332CrossRefPubMedGoogle Scholar
  17. Moscoso H, Saavedra C, Loyola C, Pichuantes S, Vásquez C (1998) Biochemical characterization of tellurite-reducing activities of Bacillus stearothermophilus V. Res Microbiol 149:389–397PubMedCrossRefGoogle Scholar
  18. O’Gara JP, Gomelsky M, Kaplan S (1997) Identification and molecular genetic analysis of multiple loci contributing to high-level tellurite resistance in Rhodobacter sphaeroides 2.4.1. Appl Environ Microbiol 63:4713–4720PubMedGoogle Scholar
  19. Ollivier PRL, Bahrou AS, Marcus S, Cox T, Church TM, Hanson TE (2008) Volatilization and precipitation of tellurium by aerobic, tellurite resistant marine microbes. Appl Environ Microbiol 74:7163–7173PubMedCrossRefGoogle Scholar
  20. Oremland RS, Umberger C, Culbertson CW, Smith RL (1984) Denitrification in San Francisco Bay intertidal sediments. Appl Environ Microbiol 47:1106–1112PubMedGoogle Scholar
  21. Oremland RS, Switzer Blum J, Culbertson CW, Visscher PT, Miller LG, Dowdle P, Strohmaier FE (1994) Isolation, growth and metabolism of an obligately anaerobic, selenate-respiring bacterium, strain SES-3. Appl Environ Microbiol 60:3011–3019PubMedGoogle Scholar
  22. Oremland RS, Stolz JF, Hollibaugh JT (2004) The microbial arsenic cycle in Mono Lake, California. FEMS Microbiol Ecol 48:15–27CrossRefPubMedGoogle Scholar
  23. Pearce CI, Coker VS, Charnock JM, Pattrick RAD, Mosselmans JFW, Law N, Beveridge TJ, Lloyd JR (2008) Microbial manufacture of chalcogenide-based nanoparticles via the reduction of selenite using Veillonella atypica: an in situ EXAFS study. Nanotechnology 19:155603–155616CrossRefGoogle Scholar
  24. Pearce CI, Pattrick RAD, Law N, Charnock JM, CokerVS, Fellowes JW, Oremland RS, Lloyd JR (2009) Investigating different mechanisms for biogenic selenite transformations: Geobacter sulfurreducens, Shewanella oneidensis and Veillonella atypical. Environ Technol (in press)Google Scholar
  25. Ratheber C, Yurkova N, Stackebrandt E, Beatty JT, Yurkov V (2002) Isolation of tellurite- and selenite-resistant bacteria from hydrothermal vents of the Juan de Fuca Ridge in the Pacific Ocean. Appl Environ Microbiol 68:4613–4622CrossRefGoogle Scholar
  26. Sen S, Bhatta UM, Kumar V, Muthe KP, Bhattacharya S, Gupta SK, Shashwati JV, Yakhmi JV (2008) Synthesis of tellurium nanostructures by physical vapor deposition and their growth mechanism. Crystal Growth Des 8:238–242Google Scholar
  27. Smith RL, Strohmaier FE, Oremland RS (1985) Isolation of anaerobic oxalate degrading bacteria from freshwater lake sediments. Arch Microbiol 14:8–13CrossRefGoogle Scholar
  28. Solorzano L (1969) Determination of ammonia in natural waters by the phenolhypochlorite method. Limnol Oceanogr 14:799–801CrossRefGoogle Scholar
  29. Song J-M, Lin Y-Z, Zhan Y-J, Tian Y-C, Gand L, Yu S-H (2008) Superlong high-quality tellurium nanotubes: synthesis, characterization, and optical property. Crystal Growth Des 8:1902–1908CrossRefGoogle Scholar
  30. Stefani FD, Hoogenboom JP, Barkai E (2009) Beyond quantum jumps: blinking nano scale light emitters. Physics Today 62:34–39CrossRefGoogle Scholar
  31. Stolz JF (1990) Introduction to the phototrophic prokaryotes and ultrastructural techniques used in their study. In: Stolz JF (ed) Structure of phototrophic prokaryotes. CRC Press, Boca Raton, pp 1–14Google Scholar
  32. Stolz JF, Oremland RS (1999) Bacterial respiration of selenium and arsenic. FEMS Microbiol Rev 23:615–627PubMedCrossRefGoogle Scholar
  33. Switzer Blum J, Burns Bind A, Buzzelli J, Stolz JF, Oremland RS (1998) Bacillus arsenicoselenatis sp nov., and Bacillus selenitireducens sp. nov.: two haloalkaliphiles from Mono Lake, California which respire oxyanions of selenium and arsenic. Arch Microbiol 171:19–30PubMedCrossRefGoogle Scholar
  34. Swofford DL (1998) PAUP*. Phylogenetic analysis using parsimony (*and other methods) version 4, Sinauer Associates, Sunderland, MAGoogle Scholar
  35. Thauer RK, Jungermann K, Decker K (1977) Energy conservation in chemotrophic anaerobic bacteria. Microbiol Rev 4:100–180Google Scholar
  36. Ujjall KG, Rao CNR (2004) Controlled synthesis of crystalline tellurium nanorods, nanowires, nanobelts and related structures by a self-seeding solution process. J Mat Chem 14:2530–2535CrossRefGoogle Scholar
  37. Widdel F, Kohring G-W, Mayer F (1983) Studies on the dissimilatory sulfur-reducing bacteria that decompose fatty acids. 3. Characterization of the filamentous gliding Desulfonema limicola, gen. nov., sp. nov. and Desulfonema magnum, sp. nov. Arch Microbiol 134:286–294CrossRefGoogle Scholar
  38. Woods TL, Garrels RM (1987) Thermodynamic values at low temperature for inorganic materials: an uncritical summary. Oxford University Press, New YorkGoogle Scholar
  39. Yuan L, Schmalz H, Xu Y, Miyajima N, Drechsler M, Möller MW, Schacher F, Müller AHE (2008) Room-temperature growth of uniform tellurium nanorods and the assembly of tellurium or Fe3O4 nanoparticles on the nanorods. Adv Mat 20:947–952CrossRefGoogle Scholar
  40. Zhu W, Wang W, Xu H, Zhou L, Zhang L, Shi JJ (2006a) Ultrasonic-induced growth of crystalline tellurium nanorods and related branched structures. J Crystal Growth 295:69–74CrossRefGoogle Scholar
  41. Zhu W, Wang W, Xu H, Zhou L, Zhang L, Shi J (2006b) Controllable, surfactant-free growth of 2D, scroll-like tellurium nanocrystals via a modified polyol process. Crystal Grow Des 6:2804–2808CrossRefGoogle Scholar

Copyright information

© Springer 2009

Authors and Affiliations

  • S. M. Baesman
    • 1
  • J. F. Stolz
    • 2
  • T. R. Kulp
    • 1
  • Ronald S. Oremland
    • 1
  1. 1.U.S. Geological SurveyMenlo ParkUSA
  2. 2.Department of Biological SciencesDuquesne UniversityPittsburghUSA

Personalised recommendations