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

Volumn 14, Issue 11, 2012, Pages 2851-2869

  Behrens, Sebastian ^a   Kappler, Andreas ^a   Obst, Martin ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MASS SPECTROMETRY; MICROBIOLOGY; NITROGEN FIXATION; SCANNING TRANSMISSION ELECTRON MICROSCOPY; SHORT SURVEY; X RAY;

ENVIRONMENTAL MICROBIOLOGY; MICROSCOPY, ELECTRON, SCANNING TRANSMISSION; NITROGEN FIXATION; SPECTROMETRY, MASS, SECONDARY ION; X-RAYS;

EID: 84868002629     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2012.02724.x     Document Type: Short Survey

References (100)

1. Behrens, S., Loesekann, T., Pett-Ridge, J., Weber, P.K., Ng, W.-O., Stevenson, B.S., etal. (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.
2. 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.
3. 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.
4. 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.
5. Bluhm, H., Andersson, K., Araki, T., Benzerara, K., Brown, G.E., Dynes, J.J., etal. (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.
6. 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.
7. 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.
8. Byrne, M.E., Ball, D.A., Guerquin-Kern, J.-L., Rouiller, I., Wu, T.-D., Downing, K.H., etal. (2010) Desulfovibrio magneticus RS-1 contains an iron- and phosphorus-rich organelle distinct from its bullet-shaped magnetosomes. PNAS 107: 12263-12268.
9. Castaing, R., and Slodzian, G. (1962) Microanalyse par émission ionique secondaire (microanalysis by secondary ion emission). J Microsc 1: 395-410.
10. 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.
11. 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.
12. 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.
13. Cockell, C.S., van Calsteren, P., Mosselmans, J.F.W., Franchi, I.A., Gilmour, I., Kelly, L., etal. (2010) Microbial endolithic colonization and the geochemical environment in young seafloor basalts. Chem Geol 279: 17-30.
14. Davey, M.E., and O'Toole, G.A. (2000) Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64: 847-867.
15. 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.
16. 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.
17. 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.
18. 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.
19. 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.
20. 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.
21. Falkowski, P.G., Fenchel, T., and Delong, E.F. (2008) The microbial engines that drive Earth's biogeochemical cycles. Science 320: 1034-1039.
22. Fayek, M., Utsunomiya, S., Pfiffner, S.M., White, D.C., Riciputi, L.R., Ewing, R.C., etal. (2005) The application of HRTEM techniques and nanosims to chemically and isotopically characterize Geobacter sulfurreducens surfaces. Can Mineral 43: 1631-1641.
23. 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.
24. Finzi-Hart, J.A., Pett-Ridge, J., Weber, P.K., Popa, R., Fallon, S.J., Gunderson, T., etal. (2009) Fixation and fate of C and N in the cyanobacterium Trichodesmium using nanometer-scale secondary ion mass spectrometry. PNAS 106: 6345-6350.
25. 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.
26. 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.
27. 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.
28. 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.
29. 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.
30. 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.
31. Ghorai, S., and Tivanski, A.V. (2010) Hygroscopic behavior of individual submicrometer particles studied by X-ray spectromicroscopy. Anal Chem 82: 9289-9298.
32. Gianoncelli, A., Kaulich, B., Alberti, R., Klatka, T., Longoni, A., de Marco, A., etal. (2009) Simultaneous soft X-ray transmission and emission microscopy. Nucl Instrum Methods Phys Res A 608: 195-198.
33. Grovenor, C.R.M., Smart, K.E., Kilburn, M.R., Shore, B., Dilworth, J.R., Martin, B., etal. (2006) Specimen preparation for NanoSIMS analysis of biological materials. Appl Surf Sci 252: 6917-6924.
34. 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.
35. 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.
36. Halm, H., Musat, N., Lam, P., Langlois, R., Musat, F., Peduzzi, S., etal. (2009) Co-occurrence of denitrification and nitrogen fixation in a meromictic lake, Lake Cadagno (Switzerland). Environ Microbiol 11: 1945-1958.
37. 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.
38. 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.
39. 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.
40. 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.
41. Herrmann, A.M., Ritz, K., Nunan, N., Clode, P.L., Pett-Ridge, J., Kilburn, M.R., etal. (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.
42. 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.
43. 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.
44. 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.
45. 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.
46. 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.
47. 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.
48. 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.
49. 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.
50. 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.
51. Kaulich, B., Bacescu, D., Cocco, D., Susini, J., Salome, M., Dhez, O., etal. (2003) Twinmic: a European twin microscope station combining full-field imaging and scanning microscopy. J Phys IV 104: 103-107.
52. 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.
53. Kilcoyne, A.L.D., Tyliszczak, T., Steele, W.F., Fakra, S., Hitchcock, P., Franck, K., etal. (2003) Interferometer-controlled scanning transmission X-ray microscopes at the Advanced Light Source. J Synchrotron Radiat 10: 125-136.
54. Kirz, J., and Rarback, H. (1985) Soft-X-ray microscopes. Rev Sci Instrum 56: 1-13.
55. Kirz, J., Jacobsen, C., and Howells, M. (1995) Soft-X-ray microscopes and their biological applications. Q Rev Biophys 28: 33-130.
56. Lam, K.P., Hitchcock, A.P., Obst, M., Lawrence, J.R., Swerhone, G.D.W., Leppard, G.G., etal. (2010) Characterizing magnetism of individual magnetosomes by X-ray magnetic circular dichroism in a scanning transmission X-ray microscope. Chem Geol 270: 110-116.
57. 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.
58. 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.
59. Lechene, C., Hillion, F., McMahon, G., Benson, D., Kleinfeld, A., Kampf, J.P., etal. (2006) High-resolution quantitative imaging of mammalian and bacterial cells using stable isotope mass spectrometry. J Biol 5: 20. doi:10.1186/jbiol42.
60. 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.
61. 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.
62. Lin, Y., Trouillon, R., Safina, G., and Ewing, A.G. (2011) Chemical analysis of single cells. Anal Chem 83: 4369-4392.
63. 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.
64. Miot, J., Benzerara, K., Morin, G., Kappler, A., Bernard, S., Obst, M., etal. (2009a) Iron biomineralization by anaerobic neutrophilic iron-oxidizing bacteria. Geochim Cosmochim Acta 73: 696-711.
65. Miot, J., Benzerara, K., Obst, M., Kappler, A., Hegler, F., Schadler, S., etal. (2009b) Extracellular iron biomineralization by photoautotrophic iron-oxidizing bacteria. Appl Environ Microbiol 75: 5586-5591.
66. Moore, K.L., Schröder, M., Wu, Z., Martin, B.G.H., Hawes, C.R., McGrath, S.P., etal. (2011) High-resolution secondary ion mass spectrometry reveals the contrasting subcellular distribution of arsenic and silicon in rice roots. Plant Physiol 156: 913-924.
67. 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.
68. Musat, N., Halm, H., Winterholler, B., Hoppe, P., Peduzzi, S., Hillion, F., etal. (2008) A single-cell view on the ecophysiology of anaerobic phototrophic bacteria. PNAS 105: 17861-17866.
69. 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.
70. 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.
71. 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.
72. Norlund, K.L.I., Southam, G., Tyliszczak, T., Hu, Y., Karunakaran, C., Obst, M., etal. (2009) Microbial architecture of environmental sulfur processes: a novel syntrophic sulfur-metabolizing consortia. Environ Sci Technol 43: 8781-8786.
73. 3 (aragonite-like) by cyanobacteria: a STXM study of the influence of EPS on the nucleation process. Geochim Cosmochim Acta 73: 4180-4198.
74. Obst, M., Wang, J., and Hitchcock, A.P. (2009b) Soft X-ray spectro-tomography study of cyanobacterial biomineral nucleation. Geobiology 7: 577-591.
75. 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.
76. 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.
77. 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.
78. 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.
79. 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.
80. 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.
81. 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.
82. Popa, R., Weber, P.K., Pett-Ridge, J., Finzi, J.A., Fallon, S.J., Hutcheon, I.D., etal. (2007) Carbon and nitrogen fixation and metabolite exchange in and between individual cells of Anabaena oscillarioides. ISME J 1: 354-360.
83. 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.
84. 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.
85. 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.
86. 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.
87. Thieme, J., McNulty, I., Vogt, S., and Paterson, D. (2007) X-ray spectromicroscopy - a tool for environmental sciences. Environ Sci Technol 41: 6885-6889.
88. 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.
89. 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.
90. 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.
91. 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.
92. 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.
93. Tourna, M., Stieglmeier, M., Spang, A., Könneke, M., Schintlmeister, A., Urich, T., etal. (2011) Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. PNAS 108: 8420-8425.
94. 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.
95. Wang, J., Zhou, J., Fang, H., Sham, T.-K., Karunakaran, C., Lu, Y., etal. (2011) Effect of humidity on individual SnO(2) coated carbon nanotubes studied by in situ STXM. J Electron Spectros Relat Phenomena 184: 296-300.
96. Warwick, T., Franck, K., Kortright, J.B., Meigs, G., Moronne, M., Myneni, S., etal. (1998) A scanning transmission x-ray microscope for materials science spectromicroscopy at the advanced light source. Rev Sci Instrum 69: 2964-2973.
97. Watrous, J.D., and Dorrestein, P.C. (2011) Imaging mass spectrometry in microbiology. Nat Rev Microbiol 9: 683-694.
98. 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.
99. 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.
100. Winograd, N., and Garrison, B.J. (2010) Biological cluster mass spectrometry. Annu Rev Phys Chem 61: 305-322.