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

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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.

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References

  • 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 143:1181–1189

    Article  Google Scholar 

  • 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 73:2135–2143

    Article  PubMed  CAS  Google Scholar 

  • 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 1164–1165

  • 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 72:4950–4956

    Article  PubMed  CAS  Google Scholar 

  • Fisher JC, Hollibaugh JT (2008) Selenate-dependent anaerobic arsenite oxidation by a bacterium from Mono Lake, California. Appl Environ Microbiol 74:2588–2594

    Article  PubMed  CAS  Google Scholar 

  • 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 67:1117–1127

    Article  CAS  Google Scholar 

  • 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 20:587–602

    Article  CAS  Google Scholar 

  • 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 51:1124–1126

    PubMed  CAS  Google Scholar 

  • Hobbie JE, Daley RL, Jaspar S (1977) Use of nuclepore filters for counting bacteria for fluorescent microscopy. Appl Environ Microbiol 33:1225–1228

    PubMed  CAS  Google Scholar 

  • 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 70:2741–2747

    Article  PubMed  CAS  Google Scholar 

  • 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 72:2043–2049

    Article  PubMed  CAS  Google Scholar 

  • Huber R, Sacher M, Vollmann A, Huber H, Rose D (2000) Respiration of arsenate and selenate by hyperthermophilic archaea. Sys Appl Microbiol 23:305–314

    CAS  Google Scholar 

  • Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ (1998) Multiple sequence alignment with Clustal X. Trends Biochem Sci 23:403–405

    Article  PubMed  CAS  Google Scholar 

  • 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 68:3678–3701

    Article  CAS  Google Scholar 

  • 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 104:20410–20415

    Article  PubMed  CAS  Google Scholar 

  • Liu A, Garcia-Dominguez E, Rhine E, Young LY (2004) A novel arsenate respiring isolate that can utilize aromatic substrates. FEMS Microbiol Ecol 48:323–332

    Article  CAS  PubMed  Google Scholar 

  • Moscoso H, Saavedra C, Loyola C, Pichuantes S, Vásquez C (1998) Biochemical characterization of tellurite-reducing activities of Bacillus stearothermophilus V. Res Microbiol 149:389–397

    Article  PubMed  CAS  Google Scholar 

  • 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 63:4713–4720

    PubMed  Google Scholar 

  • 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 74:7163–7173

    Article  PubMed  CAS  Google Scholar 

  • Oremland RS, Umberger C, Culbertson CW, Smith RL (1984) Denitrification in San Francisco Bay intertidal sediments. Appl Environ Microbiol 47:1106–1112

    PubMed  CAS  Google Scholar 

  • 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 60:3011–3019

    PubMed  CAS  Google Scholar 

  • Oremland RS, Stolz JF, Hollibaugh JT (2004) The microbial arsenic cycle in Mono Lake, California. FEMS Microbiol Ecol 48:15–27

    Article  CAS  PubMed  Google Scholar 

  • 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 19:155603–155616

    Article  CAS  Google Scholar 

  • 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)

  • 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 68:4613–4622

    Article  CAS  Google Scholar 

  • 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 8:238–242

    Google Scholar 

  • Smith RL, Strohmaier FE, Oremland RS (1985) Isolation of anaerobic oxalate degrading bacteria from freshwater lake sediments. Arch Microbiol 14:8–13

    Article  Google Scholar 

  • Solorzano L (1969) Determination of ammonia in natural waters by the phenolhypochlorite method. Limnol Oceanogr 14:799–801

    Article  CAS  Google Scholar 

  • 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 8:1902–1908

    Article  CAS  Google Scholar 

  • Stefani FD, Hoogenboom JP, Barkai E (2009) Beyond quantum jumps: blinking nano scale light emitters. Physics Today 62:34–39

    Article  CAS  Google Scholar 

  • 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 1–14

    Google Scholar 

  • Stolz JF, Oremland RS (1999) Bacterial respiration of selenium and arsenic. FEMS Microbiol Rev 23:615–627

    Article  PubMed  CAS  Google Scholar 

  • 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 171:19–30

    Article  PubMed  CAS  Google Scholar 

  • Swofford DL (1998) PAUP*. Phylogenetic analysis using parsimony (*and other methods) version 4, Sinauer Associates, Sunderland, MA

  • Thauer RK, Jungermann K, Decker K (1977) Energy conservation in chemotrophic anaerobic bacteria. Microbiol Rev 4:100–180

    Google Scholar 

  • 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 14:2530–2535

    Article  CAS  Google Scholar 

  • 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 134:286–294

    Article  CAS  Google Scholar 

  • Woods TL, Garrels RM (1987) Thermodynamic values at low temperature for inorganic materials: an uncritical summary. Oxford University Press, New York

    Google Scholar 

  • 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 20:947–952

    Article  CAS  Google Scholar 

  • 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 295:69–74

    Article  CAS  Google Scholar 

  • 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 6:2804–2808

    Article  CAS  Google Scholar 

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Acknowledgments

R. Bansal for 16S rRNA gene cloning and sequencing and J. Patterson for transmission electron microscopy. We are grateful to J. T. Hollibaugh for providing his dataset of other dissolved constituents of this ecosystem and thank S. E. Hoeft for advice in the choice of buffers for the pH experiments and L. G. Miller for technical assistance. This work was funded in part by the USGS and by a grant from the NASA Exobiology Program.

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Authors and Affiliations

  1. U.S. Geological Survey, 345 Middlefield Road, Menlo Park, CA, 94025, USA

    S. M. Baesman, T. R. Kulp & Ronald S. Oremland

  2. Department of Biological Sciences, Duquesne University, Pittsburgh, PA, 15282, USA

    J. F. Stolz

Authors
  1. S. M. Baesman
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  2. J. F. Stolz
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  3. T. R. Kulp
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  4. Ronald S. Oremland
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Correspondence to Ronald S. Oremland.

Additional information

Communicated by T. Matsunaga.

Appendix 1: Description of Bacillus beveridgei, sp. nov.

Appendix 1: Description of Bacillus beveridgei, sp. nov.

Bacillus beveridgei (bev.er.rig’.ei.N.L. gen.n. beveridgei of Beveridge, named in honor of the memory of Professor Terry J. Beveridge for his broad contributions and teaching in the realm of Geomicrobiology, with specific reference to his research on the formation of mineral phases by microorganisms). Cells are Gram positive, motile rods with a peritrichous flagellum (0.25 × 1.3–2.6 μm) and have a DNA G + C content of 46.8%. Colonies on agar are round, smooth, 4–28 mm in diameter and appear dark black when grown on Te-oxyanions due to precipitation of Te(0). Haloalkaliphilic, with growth optimal at pH 9.0 and 0.5–1.5 M sodium chloride. Meso-thermophilic with a temperature optimum at 40°C. Facultative anaerobe, able to grow in air and with 5% v/v headspace O2, but cells are not microaerophilic. Anaerobic growth demonstrated with Te(VI), Te(IV), Se(VI), Se(IV), As(V), nitrate, nitrite, trimethylamine oxide, and fumarate as electron acceptors. Growth on nitrate is via dissimilatory reduction to ammonia. Electron donors include lactate, pyruvate, glucose and galactose, starch and complex substances like yeast extract. Growth on glucose, starch and yeast extract does not require the presence of an electron acceptor and can be fermentative. The type strain, MLTeJBT (DSMZ = DSM 22320; ATCC = BAA-1786) was isolated from Mono Lake, an alkaline hypersaline soda lake in California, USA.

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Baesman, S.M., Stolz, J.F., Kulp, T.R. et al. Enrichment and isolation of Bacillus beveridgei sp. nov., a facultative anaerobic haloalkaliphile from Mono Lake, California, that respires oxyanions of tellurium, selenium, and arsenic. Extremophiles 13, 695–705 (2009). https://doi.org/10.1007/s00792-009-0257-z

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