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Linking environmental processes to the in situ functioning of microorganisms by high-resolution secondary ion mass spectrometry (NanoSIMS) and scanning transmission X-ray microscopy (STXM)

  1. Sebastian Behrens1,*,
  2. Andreas Kappler1,
  3. Martin Obst2

Article first published online: 12 MAR 2012

DOI: 10.1111/j.1462-2920.2012.02724.x

Issue

Environmental Microbiology

Environmental Microbiology

Volume 14, Issue 11, pages 2851–2869, November 2012

Additional Information

How to Cite

Behrens, S., Kappler, A. and Obst, M. (2012), Linking environmental processes to the in situ functioning of microorganisms by high-resolution secondary ion mass spectrometry (NanoSIMS) and scanning transmission X-ray microscopy (STXM). Environmental Microbiology, 14: 2851–2869. doi: 10.1111/j.1462-2920.2012.02724.x

Author Information

  1. 1

    Geomicrobiology/Microbial Ecology

  2. 2

    Environmental Analytical Microscopy, Center for Applied Geosciences, University of Tübingen, Tübingen, Germany.

* E-mail sebastian.behrens@ifg.uni-tuebingen.de; Tel. (+49) 7071 2975496; Fax (+49) 7071 295059.

Publication History

  1. Issue published online: 24 OCT 2012
  2. Article first published online: 12 MAR 2012
  3. Received 8 November, 2011; revised 20 January, 2012; accepted 11 February, 2012.

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References

  • Behrens, S., Loesekann, T., Pett-Ridge, J., Weber, P.K., Ng, W.-O., Stevenson, B.S., et al. (2008) Linking microbial phylogeny to metabolic activity at the single-cell level by using enhanced element labeling-catalyzed reporter deposition fluorescence in situ hybridization (EL-FISH) and NanoSIMS. Appl Environ Microbiol 74: 3143–3150.
  • Benzerara, K., Menguy, N., Guyot, F., Skouri, F., de Luca, G., Barakat, M., and Heulin, T. (2004a) Biologically controlled precipitation of calcium phosphate by Ramlibacter tataouinensis. Earth Planet Sci Lett 228: 439–449.
  • Benzerara, K., Yoon, T.H., Tyliszczak, T., Constantz, B., Spormann, A.M., and Brown, G.E. (2004b) Scanning transmission X-ray microscopy study of microbial calcification. Geobiology 2: 249–259.
    Direct Link:
  • Benzerara, K., Yoon, T.H., Menguy, N., Tyliszczak, T., and Brown, G.E. (2005) Nanoscale environments associated with bioweathering of a Mg-Fe-pyroxene. PNAS 102: 979–982.
  • Bluhm, H., Andersson, K., Araki, T., Benzerara, K., Brown, G.E., Dynes, J.J., et al. (2006) Soft X-ray microscopy and spectroscopy at the molecular environmental science beamline at the Advanced Light Source. J Electron Spectros Relat Phenomena 150: 86–104.
  • Borch, T., Kretzschmar, R., Kappler, A., Cappellen, P.V., Ginder-Vogel, M., Voegelin, A., and Campbell, K. (2010) Biogeochemical redox processes and their impact on contaminant dynamics. Environ Sci Technol 44: 15–23.
  • Boxer, S.G., Kraft, M.L., and Weber, P.K. (2009) Advances in imaging secondary ion mass spectrometry for biological samples. Annu Rev Biophys 38: 53–74.
  • Byrne, M.E., Ball, D.A., Guerquin-Kern, J.-L., Rouiller, I., Wu, T.-D., Downing, K.H., et al. (2010) Desulfovibrio magneticus RS-1 contains an iron- and phosphorus-rich organelle distinct from its bullet-shaped magnetosomes. PNAS 107: 12263–12268.
  • Castaing, R., and Slodzian, G. (1962) Microanalyse par émission ionique secondaire (microanalysis by secondary ion emission). J Microsc 1: 395–410.
  • Chan, C.S., Fakra, S.C., Edwards, D.C., Emerson, D., and Banfield, J.F. (2009) Iron oxyhydroxide mineralization on microbial extracellular polysaccharides. Geochim Cosmochim Acta 73: 3807–3818.
  • Chan, C.S., Fakra, S.C., Emerson, D., Fleming, E.J., and Edwards, K.J. (2011) Lithotrophic iron-oxidizing bacteria produce organic stalks to control mineral growth: implications for biosignature formation. ISME J 5: 717–727.
  • Clode, P.L., Kilburn, M.R., Jones, D.L., Stockdale, E.A., Cliff, J.B., III, Herrmann, A.M., and Murphy, D.V. (2009) In situ mapping of nutrient uptake in the rhizosphere using nanoscale secondary ion mass spectrometry. Plant Physiol 151: 1751–1757.
  • Cockell, C.S., van Calsteren, P., Mosselmans, J.F.W., Franchi, I.A., Gilmour, I., Kelly, L., et al. (2010) Microbial endolithic colonization and the geochemical environment in young seafloor basalts. Chem Geol 279: 17–30.
  • Davey, M.E., and O'Toole, G.A. (2000) Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64: 847–867.
  • Dekas, A.E., Poretsky, R.S., and Orphan, V.J. (2009) Deep-sea archaea fix and share nitrogen in methane-consuming microbial consortia. Science 326: 422–426.
  • Deldon, C., Hanselmann, K.W., Peduzzi, R., and Zullig, H. (1985) Phototrophic bacteria in the redox transition zone of Lago Cadagno, a meromictic, alpine lake. Experientia 41: 554–554.
  • Dohnalkova, A.C., Marshall, M.J., Arey, B.W., Williams, K.H., Buck, E.C., and Fredrickson, J.K. (2011) Imaging hydrated microbial extracellular polymers: comparative analysis by electron microscopy. Appl Environ Microbiol 77: 1254–1262.
  • Dynes, J.J., Lawrence, J.R., Korber, D.R., Swerhone, G.D.W., Leppard, G.G., and Hitchcock, A.P. (2006a) Quantitative mapping of chlorhexidine in natural river biofilms. Sci Total Environ 369: 369–383.
  • Dynes, J.J., Tyliszczak, T., Araki, T., Lawrence, J.R., Swerhone, G.D.W., Leppard, G.G., and Hitchcock, A.P. (2006b) Speciation and quantitative mapping of metal species in microbial biofilms using scanning transmission X-ray microscopy. Environ Sci Technol 40: 1556–1565.
  • Dynes, J.J., Lawrence, J.R., Korber, D.R., Swerhone, G.D.W., Leppard, G.G., and Hitchcock, A.P. (2009) Morphological and biochemical changes in Pseudomonas fluorescens biofilms induced by sub-inhibitory exposure to antimicrobial agents. Can J Microbiol 55: 163–178.
  • Falkowski, P.G., Fenchel, T., and Delong, E.F. (2008) The microbial engines that drive Earth's biogeochemical cycles. Science 320: 1034–1039.
  • Fayek, M., Utsunomiya, S., Pfiffner, S.M., White, D.C., Riciputi, L.R., Ewing, R.C., et al. (2005) The application of HRTEM techniques and nanosims to chemically and isotopically characterize Geobacter sulfurreducens surfaces. Can Mineral 43: 1631–1641.
  • Fike, D.A., Gammon, C.L., Ziebis, W., and Orphan, V.J. (2008) Micron-scale mapping of sulfur cycling across the oxycline of a cyanobacterial mat: a paired nanoSIMS and CARD-FISH approach. ISME J 2: 749–759.
  • Finzi-Hart, J.A., Pett-Ridge, J., Weber, P.K., Popa, R., Fallon, S.J., Gunderson, T., et al. (2009) Fixation and fate of C and N in the cyanobacterium Trichodesmium using nanometer-scale secondary ion mass spectrometry. PNAS 106: 6345–6350.
  • Fischer, C., Wiggli, M., Schanz, F., Hanselmann, K.W., and Bachofen, R. (1996) Light environment and synthesis of bacteriochlorophyll by populations of Chromatium okenii under natural environmental conditions. FEMS Microbiol Ecol 21: 1–9.
    Direct Link:
  • Fletcher, J.S., Rabbani, S., Henderson, A., Blenkinsopp, P., Thompson, S.P., Lockyer, N.P., and Vickerman, J.C. (2008) A new dynamic in mass spectral imaging of single biological cells. Anal Chem 80: 9058–9064.
  • Fletcher, J.S., Lockyer, N.P., and Vickerman, J.C. (2010) Molecular SIMS imaging; spatial resolution and molecular sensitivity: have we reached the end of the road? Is there light at the end of the tunnel? Surf Interface Anal 43: 253–256.
    Direct Link:
  • Fletcher, J.S., Lockyer, N.P., and Vickerman, J.C. (2011) Developments in molecular SIMS depth profiling and 3D imaging of biological systems using polyatomic primary ions. Mass Spectrom Rev 30: 142–174.
    Direct Link:
  • Foster, R.A., Kuypers, M.M.M., Vagner, T., Paerl, R.W., Musat, N., and Zehr, J.P. (2011) Nitrogen fixation and transfer in open ocean diatom-cyanobacterial symbioses. ISME J 5: 1484–1493.
  • Frache, G., El Adib, B., Audinot, J.N., and Migeon, H.N. (2011) Evaluation of ionization yields under gallium bombardment. Surf Interface Anal 43: 639–642.
    Direct Link:
  • Ghorai, S., and Tivanski, A.V. (2010) Hygroscopic behavior of individual submicrometer particles studied by X-ray spectromicroscopy. Anal Chem 82: 9289–9298.
  • Gianoncelli, A., Kaulich, B., Alberti, R., Klatka, T., Longoni, A., de Marco, A., et al. (2009) Simultaneous soft X-ray transmission and emission microscopy. Nucl Instrum Methods Phys Res A 608: 195–198.
  • Grovenor, C.R.M., Smart, K.E., Kilburn, M.R., Shore, B., Dilworth, J.R., Martin, B., et al. (2006) Specimen preparation for NanoSIMS analysis of biological materials. Appl Surf Sci 252: 6917–6924.
  • Guerquin-Kern, J.-L., Wu, T.-D., Quintana, C., and Croisy, A. (2005) Progress in analytical imaging of the cell by dynamic secondary ion mass spectrometry (SIMS microscopy). Biochim Biophys Acta 1724: 228–238.
  • Gutierrez-Zamora, M.-L., and Manefield, M. (2010) An appraisal of methods for linking environmental processes to specific microbial taxa. Rev Environ Sci Biotechnol 9: 153–185.
  • Halm, H., Musat, N., Lam, P., Langlois, R., Musat, F., Peduzzi, S., et al. (2009) Co-occurrence of denitrification and nitrogen fixation in a meromictic lake, Lake Cadagno (Switzerland). Environ Microbiol 11: 1945–1958.
    Direct Link:
  • Hanhan, S., Smith, A.M., Obst, M., and Hitchcock, A.P. (2009) Optimization of analysis of soft X-ray spectromicroscopy at the Ca 2p edge. J Electron Spectros Relat Phenomena 173: 44–49.
  • Heister, K., Höschen, C., Pronk, G.J., Mueller, C.W., and Kögel-Knabner, I. (2011) NanoSIMS as a tool for characterizing soil model compounds and organomineral associations in artificial soils. J. Soils Sediments 12: 35–47.
  • Henke, B.L., Gullikson, E.M., and Davis, J.C. (1993) X-ray interactions – photoabsorption, scattering, transmission, and reflection at E=50-30,000 eV, Z=1-92. At Data Nucl Data Tables 54: 181–342.
  • Herrmann, A.M., Clode, P.L., Fletcher, I.R., Nunan, N., Stockdale, E.A., O'Donnell, A.G., and Murphy, D.V. (2007a) A novel method for the study of the biophysical interface in soils using nano-scale secondary ion mass spectrometry. Rapid Commun Mass Spectrom 21: 29–34.
    Direct Link:
  • Herrmann, A.M., Ritz, K., Nunan, N., Clode, P.L., Pett-Ridge, J., Kilburn, M.R., et al. (2007b) Nano-scale secondary ion mass spectrometry – a new analytical tool in biogeochemistry and soil ecology: a review article. Soil Biol Biochem 39: 1835–1850.
  • Hitchcock, A.P., Morin, C., Tyliszczak, T., Koprinarov, I.N., Ikeura-Sekiguchi, H., Lawrence, J.R., and Leppard, G.G. (2002) Soft X-ray microscopy of soft matter – hard information from two softs. Surf Rev Lett 9: 193–201.
  • Hitchcock, A.P., Dynes, J.J., Johansson, G., Wang, J., and Botton, G. (2008a) Comparison of NEXAFS microscopy and TEM-EELS for studies of soft matter. Micron 39: 311–319.
  • Hitchcock, A.P., Johansson, G.A., Mitchell, G.E., Keefe, M.H., and Tyliszcak, T. (2008b) 3-D chemical imaging using angle-scan nanotomography in a soft X-ray scanning transmission X-ray microscope. Appl Phys A Mat Sci Process 92: 447–452.
  • Hitchcock, A.P., Dynes, J.J., Lawrence, J.R., Obst, M., Swerhone, G.D.W., Korber, D.R., and Leppard, G.G. (2009) Soft X-ray spectromicroscopy of nickel sorption in a natural river biofilm. Geobiology 7: 432–453.
    Direct Link:
  • Hitchcock, A.P., Tylisczcak, T., Obst, M., Swerhone, G.D.W., and Lawrence, J.R. (2010) Improving sensitivity in soft X-ray STXM using low energy X-ray fluorescence. Microsc Microanal 16: 924–925.
  • Huang, W.E., Stoecker, K., Griffiths, R., Newbold, L., Daims, H., Whiteley, A.S., and Wagner, M. (2007) Raman-FISH: combining stable-isotope Raman spectroscopy and fluorescence in situ hybridization for the single cell analysis of identity and function. Environ Microbiol 9: 1878–1889.
    Direct Link:
  • Hunter, R.C., Hitchcock, A.P., Dynes, J.J., Obst, M., and Beveridge, T.J. (2008) Mapping the speciation of iron in Pseudomonas aeruginosa biofilms using scanning transmission X-ray microscopy. Environ Sci Technol 42: 8766–8772.
  • Ishihara, M., Ebata, S., Kumondai, K., Mibuka, R., Uchino, K., and Yurimoto, H. (2010) Ultra-high performance multi-turn TOF-SIMS system with a femto-second laser for post-ionization: investigation of the performance in linear mode. Surf Interface Anal 42: 1598–1602.
    Direct Link:
  • Johansson, G.A., Tyliszczak, T., Mitchell, G.E., Keefe, M.H., and Hitchcock, A.P. (2007) Three-dimensional chemical mapping by scanning transmission X-ray spectromicroscopy. J Synchrotron Radiat 14: 395–402.
    Direct Link:
  • Kaulich, B., Bacescu, D., Cocco, D., Susini, J., Salome, M., Dhez, O., et al. (2003) Twinmic: a European twin microscope station combining full-field imaging and scanning microscopy. J Phys IV 104: 103–107.
  • Kaznatcheev, K.V., Karunakaran, C., Lanke, U.D., Urquhart, S.G., Obst, M., and Hitchcock, A.P. (2007) Soft X-ray spectromicroscopy beamline at the CLS: commissioning results. Nucl Instrum Methods Phys Res A 582: 96–99.
  • Kilcoyne, A.L.D., Tyliszczak, T., Steele, W.F., Fakra, S., Hitchcock, P., Franck, K., et al. (2003) Interferometer-controlled scanning transmission X-ray microscopes at the Advanced Light Source. J Synchrotron Radiat 10: 125–136.
    Direct Link:
  • Kirz, J., and Rarback, H. (1985) Soft-X-ray microscopes. Rev Sci Instrum 56: 1–13.
  • Kirz, J., Jacobsen, C., and Howells, M. (1995) Soft-X-ray microscopes and their biological applications. Q Rev Biophys 28: 33–130.
  • Lam, K.P., Hitchcock, A.P., Obst, M., Lawrence, J.R., Swerhone, G.D.W., Leppard, G.G., et al. (2010) Characterizing magnetism of individual magnetosomes by X-ray magnetic circular dichroism in a scanning transmission X-ray microscope. Chem Geol 270: 110–116.
  • Lawrence, J.R., Swerhone, G.D.W., Leppard, G.G., Araki, T., Zhang, X., West, M.M., and Hitchcock, A.P. (2003) Scanning transmission X-ray, laser scanning, and transmission electron microscopy mapping of the exopolymeric matrix of microbial biofilms. Appl Environ Microbiol 69: 5543–5554.
  • Lawrence, J.R., Dynes, J.J., Korber, D.R., Swerhone, G.D.W., Leppard, G.G., and Hitchcock, A.P. (2011) Monitoring the fate of copper nanoparticles in river biofilms using scanning transmission X-ray microscopy (STXM). Chem Geol. (in press). doi:10.1016/j.chemgeo.2011.07.013.
  • Lechene, C., Hillion, F., McMahon, G., Benson, D., Kleinfeld, A., Kampf, J.P., et al. (2006) High-resolution quantitative imaging of mammalian and bacterial cells using stable isotope mass spectrometry. J Biol 5: 20. doi:10.1186/jbiol42.
  • Lechene, C.P., Luyten, Y., McMahon, G., and Distel, D.L. (2007) Quantitative imaging of nitrogen fixation by individual bacteria within animal cells. Science 317: 1563–1566.
  • Li, T., Wu, T.-D., Mazeas, L., Toffin, L., Guerquin-Kern, J.-L., Leblon, G., and Bouchez, T. (2008) Simultaneous analysis of microbial identity and function using NanoSIMS. Environ Microbiol 10: 580–588.
    Direct Link:
  • Lin, Y., Trouillon, R., Safina, G., and Ewing, A.G. (2011) Chemical analysis of single cells. Anal Chem 83: 4369–4392.
  • Metzner, R., Schneider, H.U., Breuer, U., and Schroeder, W.H. (2008) Imaging nutrient distributions in plant tissue using time-of-flight secondary ion mass spectrometry and scanning electron microscopy. Plant Physiol 147: 1774–1787.
  • Miot, J., Benzerara, K., Morin, G., Kappler, A., Bernard, S., Obst, M., et al. (2009a) Iron biomineralization by anaerobic neutrophilic iron-oxidizing bacteria. Geochim Cosmochim Acta 73: 696–711.
  • Miot, J., Benzerara, K., Obst, M., Kappler, A., Hegler, F., Schadler, S., et al. (2009b) Extracellular iron biomineralization by photoautotrophic iron-oxidizing bacteria. Appl Environ Microbiol 75: 5586–5591.
  • Moore, K.L., Schröder, M., Wu, Z., Martin, B.G.H., Hawes, C.R., McGrath, S.P., et al. (2011) High-resolution secondary ion mass spectrometry reveals the contrasting subcellular distribution of arsenic and silicon in rice roots. Plant Physiol 156: 913–924.
  • Mueller, C.W., Kölbl, A., Hoeschen, C., Hillion, F., Heister, K., Herrmann, A.M., and Kögel-Knabner, I. (2012) Submicron scale imaging of soil organic matter dynamics using NanoSIMS – from single particles to intact aggregates. Org Geochem 42: 1476–1488.
  • Musat, N., Halm, H., Winterholler, B., Hoppe, P., Peduzzi, S., Hillion, F., et al. (2008) A single-cell view on the ecophysiology of anaerobic phototrophic bacteria. PNAS 105: 17861–17866.
  • Musat, N., Adam, B., and Kuypers, M.M.M. (2011) Nano-secondary ions mass spectrometry (nanoSIMS) coupled with in situ hybridization for ecological research. In Stable Isotope Probing and Related Technologies. Murrell, J., and Whiteley, A. (eds). Washington, DC, USA: American Society for Microbiology, pp. 295–303.
  • Neu, T.R., Manz, B., Volke, F., Dynes, J.J., Hitchcock, A.P., and Lawrence, J.R. (2010) Advanced imaging techniques for assessment of structure, composition and function in biofilm systems. FEMS Microbiol Ecol 72: 1–21.
    Direct Link:
  • Neufeld, J.D., Wagner, M., and Murrell, J.C. (2007) Who eats what, where and when? Isotope-labelling experiments are coming of age. ISME J 1: 103–110.
  • Norlund, K.L.I., Southam, G., Tyliszczak, T., Hu, Y., Karunakaran, C., Obst, M., et al. (2009) Microbial architecture of environmental sulfur processes: a novel syntrophic sulfur-metabolizing consortia. Environ Sci Technol 43: 8781–8786.
  • Obst, M., Dynes, J.J., Lawrence, J.R., Swerhone, G.D.W., Benzerara, K., Karunakaran, C., et al. (2009a) Precipitation of amorphous CaCO3 (aragonite-like) by cyanobacteria: a STXM study of the influence of EPS on the nucleation process. Geochim Cosmochim Acta 73: 4180–4198.
  • Obst, M., Wang, J., and Hitchcock, A.P. (2009b) Soft X-ray spectro-tomography study of cyanobacterial biomineral nucleation. Geobiology 7: 577–591.
    Direct Link:
  • Orphan, V.J., and House, C.H. (2009) Geobiological investigations using secondary ion mass spectrometry: microanalysis of extant and paleo-microbial processes. Geobiology 7: 360–372.
    Direct Link:
  • Orphan, V.J., House, C.H., Hinrichs, K.-U., McKeegan, K.D., and DeLong, E.F. (2001) Methane-consuming archaea revealed by directly coupled isotopic and phylogenetic analysis. Science 293: 484–487.
  • Orphan, V.J., House, C.H., Hinrichs, K.-U., McKeegan, K.D., and DeLong, E.F. (2002) Multiple archaeal groups mediate methane oxidation in anoxic cold seep sediments. PNAS 99: 7663–7668.
  • Orphan, V.J., Turk, K.A., Green, A.M., and House, C.H. (2009) Patterns of (15)N assimilation and growth of methanotrophic ANME-2 archaea and sulfate-reducing bacteria within structured syntrophic consortia revealed by FISH-SIMS. Environ Microbiol 11: 1777–1791.
    Direct Link:
  • Pantke, C., Obst, M., Benzerara, K., Morin, G., Ona-Nguema, G., Dippon, U., and Kappler, A. (2012) Green rust formation during Fe(II) oxidation by the nitrate-reducing Acidovorax sp. strain BoFeN1. Environ Sci Technol 46: 1439–1446.
  • Ploug, H., Adam, B., Musat, N., Kalvelage, T., Lavik, G., Wolf-Gladrow, D., and Kuypers, M.M.M. (2011) Carbon, nitrogen and O2 fluxes associated with the cyanobacterium Nodularia spumigena in the Baltic Sea. ISME J 5: 1549–1558.
  • Polerecky, L., Adam, B., Milucka, J., Musat, N., Vagner, T., and Kuypers, M.M.M. (2012) Look@NanoSIMS – a tool for the analysis of nanoSIMS data in environmental microbiology. Environ Microbiol. (in press). doi:10.1111/j.1462-2920.2011.02681.x.
    Direct Link:
  • Popa, R., Weber, P.K., Pett-Ridge, J., Finzi, J.A., Fallon, S.J., Hutcheon, I.D., et al. (2007) Carbon and nitrogen fixation and metabolite exchange in and between individual cells of Anabaena oscillarioides. ISME J 1: 354–360.
  • Schanz, F., and Stalder, S. (1998) Phytoplankton summer dynamics and sedimentation in the thermally stratified Lake Cadagno. Documenta dell'Istituto Italiano di Idrobiologia 63: 71–76.
  • Schanz, F., Fischer-Romero, C., and Bachofen, R. (1998) Photosynthetic production and photoadaptation of phototrophic sulfur bacteria in Lake Cadagno (Switzerland). Limnol Oceanogr 43: 1262–1269.
  • Templeton, A., and Knowles, E. (2009) Microbial transformations of minerals and metals: recent advances in geomicrobiology derived from synchrotron-based X-ray spectroscopy and X-ray microscopy. In Annual Review of Earth and Planetary Sciences. Jeanloz, R., and Freeman, K.H. (eds). Palo Alto, CA, USA: Annual Reviews, pp. 367–391.
  • Thieme, J., Schneider, G., and Knochel, C. (2003) X-ray tomography of a microhabitat of bacteria and other soil colloids with sub-100 nm resolution. Micron 34: 339–344.
  • Thieme, J., McNulty, I., Vogt, S., and Paterson, D. (2007) X-ray spectromicroscopy – a tool for environmental sciences. Environ Sci Technol 41: 6885–6889.
  • Toner, B., Fakra, S., Villalobos, M., Warwick, T., and Sposito, G. (2005) Spatially resolved characterization of biogenic manganese oxide production within a bacterial biofilm. Appl Environ Microbiol 71: 1300–1310.
  • Tonolla, M., Demarta, A., Peduzzi, R., and Hahn, D. (1999) In situ analysis of phototrophic sulfur bacteria in the chemocline of meromictic Lake Cadagno (Switzerland). Appl Environ Microbiol 65: 1325–1330.
  • Tonolla, M., Peduzzi, S., Hahn, D., and Peduzzi, R. (2003) Spatio-temporal distribution of phototrophic sulfur bacteria in the chemocline of meromictic Lake Cadagno (Switzerland). FEMS Microbiol Ecol 43: 89–98.
    Direct Link:
  • Tonolla, M., Peduzzi, S., Demarta, A., Peduzzi, R., and Hahn, D. (2004) Phototropic sulfur and sulfate-reducing bacteria in the chemocline of meromictic Lake Cadagno, Switzerland. J Limnol 63: 161–170.
  • Tonolla, M., Peduzzi, R., and Hahn, D. (2005) Long-term population dynamics of phototrophic sulfur bacteria in the chemocline of Lake Cadagno, Switzerland. Appl Environ Microbiol 71: 3544–3550.
  • Tourna, M., Stieglmeier, M., Spang, A., Könneke, M., Schintlmeister, A., Urich, T., et al. (2011) Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. PNAS 108: 8420–8425.
  • Wagner, M. (2009) Single-cell ecophysiology of microbes as revealed by raman microspectroscopy or secondary ion mass spectrometry imaging. Annu Rev Microbiol 63: 411–429.
  • Wang, J., Zhou, J., Fang, H., Sham, T.-K., Karunakaran, C., Lu, Y., et al. (2011) Effect of humidity on individual SnO(2) coated carbon nanotubes studied by in situ STXM. J Electron Spectros Relat Phenomena 184: 296–300.
  • Warwick, T., Franck, K., Kortright, J.B., Meigs, G., Moronne, M., Myneni, S., et al. (1998) A scanning transmission x-ray microscope for materials science spectromicroscopy at the advanced light source. Rev Sci Instrum 69: 2964–2973.
  • Watrous, J.D., and Dorrestein, P.C. (2011) Imaging mass spectrometry in microbiology. Nat Rev Microbiol 9: 683–694.
  • Webb, H.K., Truong, V.K., Hasan, J., Crawford, R.J., and Ivanova, E.P. (2011) Physico-mechanical characterisation of cells using atomic force microscopy – current research and methodologies. J Microbiol Methods 86: 131–139.
  • Willingham, D., Kucher, A., and Winograd, N. (2008) Molecular depth profiling and imaging using cluster ion beams with femtosecond laser postionization. Appl Surf Sci 255: 831–833.
  • Winograd, N., and Garrison, B.J. (2010) Biological cluster mass spectrometry. Annu Rev Phys Chem 61: 305–322.
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