NanoSIP: NanoSIMS Applications for Microbial Biology.
FIB
FISH
Isotope assimilation
Metal imaging
NanoSIMS
O− ion source
SEM
Sample preparation
Single-cell biology
TEM
Journal
Methods in molecular biology (Clifton, N.J.)
ISSN: 1940-6029
Titre abrégé: Methods Mol Biol
Pays: United States
ID NLM: 9214969
Informations de publication
Date de publication:
2022
2022
Historique:
entrez:
31
10
2021
pubmed:
1
11
2021
medline:
7
1
2022
Statut:
ppublish
Résumé
High-resolution imaging with secondary ion mass spectrometry (nanoSIMS) has become a standard method in systems biology and environmental biogeochemistry and is broadly used to decipher ecophysiological traits of environmental microorganisms, metabolic processes in plant and animal tissues, and cross-kingdom symbioses. When combined with stable isotope-labeling-an approach we refer to as nanoSIP-nanoSIMS imaging offers a distinctive means to quantify net assimilation rates and stoichiometry of individual cell-sized particles in both low- and high-complexity environments. While the majority of nanoSIP studies in environmental and microbial biology have focused on nitrogen and carbon metabolism (using
Identifiants
pubmed: 34718993
doi: 10.1007/978-1-0716-1585-0_6
doi:
Types de publication
Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
91-136Informations de copyright
© 2022. Springer Science+Business Media, LLC, part of Springer Nature.
Références
Mayali X, Weber PK, Brodie EL, Mabery S, Hoeprich PD, Pett-Ridge J (2012) High-throughput isotopic analysis of RNA microarrays to quantify microbial resource use. ISME J 6(6):1210–1221
pubmed: 22158395
doi: 10.1038/ismej.2011.175
Adamczyk J, Hesselsoe M, Iversen N, Horn M, Lehner A, Nielsen PH, Schloter M, Roslev P, Wagner M (2003) The isotope array, a new tool that employs substrate-mediated labeling of rRNA for determination of microbial community structure and function. Appl Environ Microbiol 69(11):6875–6887
pmcid: 262286
doi: 10.1128/AEM.69.11.6875-6887.2003
pubmed: 262286
Ouverney CC, Fuhrman JA (1999) Combined microautoradiography-16S rRNA probe technique for determination of radioisotope uptake by specific microbial cell types in situ. Appl Environ Microbiol 65(4):1746–1752
pubmed: 10103276
pmcid: 91246
doi: 10.1128/AEM.65.4.1746-1752.1999
Jehmlich N, Schmidt F, Taubert M, Seifert J, Bastida F, von Bergen M, Richnow H-H, Vogt C (2010) Protein-based stable isotope probing. Nat Protoc 5(12):1957–1966
pubmed: 21127489
doi: 10.1038/nprot.2010.166
Murrell JC, Whiteley AS (2011) Stable isotope probing and related technologies. ASM Press, Washington, DC, p 345
Koch BJ, McHugh TA, Hayer M, Schwartz E, Blazewicz SJ, Dijkstra P, van Gestel N, Marks JC, Mau RL, Morrissey EM, Pett-Ridge J, Hungate BA (2018) Estimating taxon-specific population dynamics in diverse microbial communities. Ecosphere 9(1):e02090–e02015
doi: 10.1002/ecs2.2090
Hillion F, Daigne B, Girard F, Slodzian G (1993) A new high performance instrument: the CAMECA NanoSIMS 50. In: Benninghoven A et al (eds) Secondary ion mass spectrometry: SIMS IX, vol 254-257. John Wiley & Sons, Chichester
Ghosal S, Leighton TJ, Wheeler KE, Hutcheon ID, Weber PK (2010) Spatially resolved characterization of water and ion incorporation in Bacillus spores. Appl Environ Microbiol 76(10):3275–3282
pubmed: 20348293
pmcid: 2869133
doi: 10.1128/AEM.02485-09
Orphan VJ, House CH, Hinrichs K-U, McKeegan KD, DeLong EF (2001) Methane-consuming archaea revealed by directly coupled isotopic and phylogenetic analysis. Science 293(5529):484–487
pubmed: 11463914
doi: 10.1126/science.1061338
Smart K, Kilburn M, Salter C, Smith J, Grovenor C (2007) NanoSIMS and EPMA analysis of nickel localisation in leaves of the hyperaccumulator plant Alyssum lesbiacum. Int J Mass Spectrom 260(2–3):107–114
doi: 10.1016/j.ijms.2006.08.011
Stadermann FJ, Walker RM, Zinner E (1999) Nanosims: the next generation ion probe for the microanalysis of extraterrestrial material. Meteorit Planet Sci 34:A111–A112
Guerquin-Kern J-L, Hillion F, Madelmont J-C, Labarre P, Papon J, Croisy A (2004) Ultra-structural cell distribution of the melanoma marker iodobenzamide: improved potentiality of SIMS imaging in life sciences. BioMed Eng. http://www.biomedical-engineering-online.com/content/3/1/10
Kraft ML, Fishel SF, Marxer CG, Weber PK, Hutcheon ID, Boxer SG (2006) Quantitative analysis of supported membrane composition using the NanoSIMS. Appl Surf Sci 252(19):6950–6956
doi: 10.1016/j.apsusc.2006.02.116
Moreau JW, Weber PK, Martin MC, Gilbert B, Hutcheon ID, Banfield JF (2007) Extracellular proteins limit the dispersal of biogenic nanoparticles. Science 316:1600–1603
pubmed: 17569859
doi: 10.1126/science.1141064
Peteranderl R, Lechene C (2004) Measure of carbon and nitrogen stable isotope ratios in cultured cells. J Am Soc Mass Spectrom 15(4):478–485
pubmed: 15047053
doi: 10.1016/j.jasms.2003.11.019
Wainwright M, Weber PK, Smith JB, Hutcheon ID, Klyce B, Wickramasinghe NC, Narlikar JV, Rajaratnam P (2004) Studies on bacteria-like particles sampled from the stratosphere. Aeorobiologia 20:237–240
doi: 10.1007/s10453-004-1188-x
Galli Marxner C, Kraft ML, Weber PK, Hutcheon I, Boxer SG (2005) Supported membrane composition analysis by secondary ion mass spectrometry with high lateral resolution. Biophys J 88:2965–2975
doi: 10.1529/biophysj.104.057257
Dekas AE, Poretsky RS, Orphan VJ (2009) Deep-sea archaea fix and share nitrogen in methane-consuming microbial consortia. Science 326(5951):422–426
pubmed: 19833965
doi: 10.1126/science.1178223
Halm H, Musat N, Lam P, Langlois R, Musat F, Peduzzi S, Lavik G, Schubert CJ, Sinha B, LaRoche J, Kuypers MMM (2009) Co-occurrence of denitrification and nitrogen fixation in a meromictic lake, Lake Cadagno (Switzerland). Environ Microbiol 11(8):2190–2190
doi: 10.1111/j.1462-2920.2009.01955.x
Musat N, Halm H, Winterholler B, Hoppe P, Peduzzi S, Hillion F, Horreard F, Amann R, Jørgensen BB, Kuypers MMM (2008) A single-cell view on the ecophysiology of anaerobic phototrophic bacteria. Proc Natl Acad Sci 105(46):17861–17866
pubmed: 19004766
pmcid: 2582579
doi: 10.1073/pnas.0809329105
Quintana C, Wu TD, Delatour B, Dhenain M, Guerquin-Kern JL, Croisy A (2007) Morphological and chemical studies of pathological human and mice brain at the subcellular level: correlation between light, electron, and NanoSIMS microscopies. Microsc Res Tech 70(4):281–295
pubmed: 17465396
doi: 10.1002/jemt.20403
Behrens S, Losekann T, Pett-Ridge J, Weber PK, Ng W, Stevenson BS, Hutcheon ID, Relman DA, Spormann AM (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(10):3143
pubmed: 18359832
pmcid: 2394947
doi: 10.1128/AEM.00191-08
Finzi-Hart J, Pett-Ridge J, Weber P, Popa R, Fallon SJ, Gunderson T, Hutcheon I, Nealson K, Capone DG (2008) Fixation and fate of carbon and nitrogen in Trichodesmium IMS101 using nanometer resolution secondary ion mass spectrometry (NanoSIMS). PNAS 106:6345–6350
doi: 10.1073/pnas.0810547106
Lechene C, Hillion F, McMahon G, Benson D, Kleinfeld A, Kampf JP, Distel D, Luyten Y, Bonventre J, Hentschel D, Park K, Ito S, Schwartz M, Benichou G, Slodzian G (2006) High-resolution quantitative imaging of mammalian and bacterial cells using stable isotope mass spectrometry. J Biol 5(6):20
pubmed: 17010211
pmcid: 1781526
doi: 10.1186/jbiol42
Popa R, Weber PK, Pett-Ridge J, Finzi JA, Fallon SJ, Hutcheon ID, Nealson KH, Capone DG (2007) Carbon and nitrogen fixation and metabolite exchange in and between individual cells of Anabaena oscillarioides. ISME J 1(4):354–360
pubmed: 18043646
doi: 10.1038/ismej.2007.44
Ghosal S, Fallon SJ, Leighton T, Wheeler KE, Hutcheon ID, Weber PK (2008) Imaging and 3D elemental characterization of intact bacterial spores with high-resolution secondary ion mass spectrometry (NanoSIMS) depth profile analysis. Anal Chem 80(15):5986–5992
pubmed: 18578543
doi: 10.1021/ac8006279
Lechene CP, Luyten Y, McMahon G, Distel DL (2007) Quantitative imaging of nitrogen fixation by individual bacteria within animal cells. Science 317:1563–1566
pubmed: 17872448
doi: 10.1126/science.1145557
Herrmann A, Ritz K, Nunan N, Clode P, Pett-Ridge J, Kilburn M, Murphy D, O’Donnell A, Stockdale E (2007) Nano-scale secondary ion mass spectrometry – a new analytical tool in biogeochemistry and soil ecology: a review article. Soil Biol Biochem 39:1835–1850
doi: 10.1016/j.soilbio.2007.03.011
Mueller CW, Weber PK, Kilburn MR, Hoeschen C, Kleber M, Pett-Ridge J (2013) Advances in the analysis of biogeochemical interfaces: NanoSIMS to investigate soil microenvironments. In: Sparks D (ed) Advances in agronomy. Elsevier, Amsterdam
Renslow RS, Lindemann SR, Cole JK, Zhu Z, Anderton CR (2016) Quantifying element incorporation in multispecies biofilms using nanoscale secondary ion mass spectrometry image analysis. Biointerphases 11(2):02A322
pubmed: 26872582
pmcid: 5848783
doi: 10.1116/1.4941764
Mayali X (2020) NanoSIMS: microscale quantification of biogeochemical activity with large-scale impacts. Annu Rev Mar Sci 12:449–467
doi: 10.1146/annurev-marine-010419-010714
Gao D, Huang X, Tao Y (2016) A critical review of NanoSIMS in analysis of microbial metabolic activities at single-cell level. Crit Rev Biotechnol 36(5):884–890
pubmed: 26177334
doi: 10.3109/07388551.2015.1057550
Zhao F-J, Moore KL, Lombi E, Zhu Y-G (2014) Imaging element distribution and speciation in plant cells. Trends Plant Sci 19(3):183–192
pubmed: 24394523
doi: 10.1016/j.tplants.2013.12.001
Musat N, Musat F, Weber PK, Pett-Ridge J (2016) Tracking microbial interactions with NanoSIMS. Curr Opin Biotechnol 41:114–121
pubmed: 27419912
doi: 10.1016/j.copbio.2016.06.007
Agüi-Gonzalez P, Jähne S, Phan NT (2019) SIMS imaging in neurobiology and cell biology. J Anal At Spectrom 34(7):1355–1368
doi: 10.1039/C9JA00118B
Boxer SG, Kraft ML, Weber PK (2009) Advances in imaging secondary ion mass spectrometry for biological samples. Annu Rev Biophys 38:53–74
pubmed: 19086820
doi: 10.1146/annurev.biophys.050708.133634
Nuñez J, Renslow R, Cliff JB III, Anderton CR (2018) NanoSIMS for biological applications: current practices and analyses. Biointerphases 13(3):03B301
doi: 10.1116/1.4993628
Gorman BL, Kraft ML (2019) High-resolution secondary ion mass spectrometry analysis of cell membranes. ACS Publications, Washington, DC
CAMECA. NanoSIMS 50L: scientific publications. https://www.cameca.com/products/sims/nanosims
Pett-Ridge J, Weber PK (2012) NanoSIP: NanoSIMS applications for microbial biology. In: Navid A (ed) Microbial systems biology: methods and protocols. Humana, New York, NY
Dekas AE, Parada AE, Mayali X, Fuhrman JA, Wollard J, Weber PK, Pett-Ridge J (2019) Characterizing chemoautotrophy and heterotrophy in marine archaea and bacteria with single-cell multi-isotope nanoSIP. Front Microbiol 10:2682
pubmed: 31920997
pmcid: 6927911
doi: 10.3389/fmicb.2019.02682
Chadwick GL, Otero FJ, Gralnick JA, Bond DR, Orphan VJ (2019) NanoSIMS imaging reveals metabolic stratification within current-producing biofilms. Proc Natl Acad Sci 116(41):20716–20724
pubmed: 31548422
pmcid: 6789570
doi: 10.1073/pnas.1912498116
Volland J-M, Schintlmeister A, Zambalos H, Reipert S, Mozetič P, Espada-Hinojosa S, Turk V, Wagner M, Bright M (2018) NanoSIMS and tissue autoradiography reveal symbiont carbon fixation and organic carbon transfer to giant ciliate host. ISME J 12(3):714–727
pubmed: 29426952
pmcid: 5854253
doi: 10.1038/s41396-018-0069-1
Calabrese F, Voloshynovska I, Musat F, Thullner M, Schlömann M, Richnow HH, Lambrecht J, Müller S, Wick LY, Musat N (2019) Quantitation and comparison of phenotypic heterogeneity among single cells of monoclonal microbial populations. Front Microbiol 10:2814
pubmed: 31921014
pmcid: 6933826
doi: 10.3389/fmicb.2019.02814
Braun PD, Schulz-Vogt HN, Vogts A, Nausch M (2018) Differences in the accumulation of phosphorus between vegetative cells and heterocysts in the cyanobacterium Nodularia spumigena. Sci Rep 8(1):1–6
Gross A, Lin Y, Weber PK, Pett-Ridge J, Silver WL (2020) The role of soil redox conditions in microbial phosphorus cycling in humid tropical forests. Ecology 101(2):e02928
pubmed: 31715005
doi: 10.1002/ecy.2928
Ackerman CM, Weber PK, Xiao T, Thai B, Kuo TJ, Zhang E, Pett-Ridge J, Chang CJ (2018) Multimodal LA-ICP-MS and nanoSIMS imaging enables copper mapping within photoreceptor megamitochondria in a zebrafish model of Menkes disease. Metallomics 10(3):474–485
pubmed: 29507920
pmcid: 5864565
doi: 10.1039/C7MT00349H
Hong-Hermesdorf A, Miethke M, Gallaher SD, Kropat J, Dodani SC, Barupala D, Chan J, Domaille DW, Shirasaki DI, Loo JA, Weber PK, Pett-Ridge J, Stemmler TL, Chang CJ, Merchant SS (2014) Selective sub-cellular visualization of trace metals identifies dynamic sites of Cu accumulation in Chlamydomonas. Nat Chem Biol 10:1034–1042
pubmed: 25344811
pmcid: 4232477
doi: 10.1038/nchembio.1662
Dawson KS, Scheller S, Dillon JG, Orphan VJ (2016) Stable isotope phenotyping via cluster analysis of NanoSIMS data as a method for characterizing distinct microbial ecophysiologies and sulfur-cycling in the environment. Front Microbiol 7:774
pubmed: 27303371
pmcid: 4881376
doi: 10.3389/fmicb.2016.00774
Berry D, Mader E, Lee TK, Woebken D, Wang Y, Zhu D, Palatinszky M, Schintlmeister A, Schmid MC, Hanson BT (2015) Tracking heavy water (D2O) incorporation for identifying and sorting active microbial cells. Proc Natl Acad Sci 112(2):E194–E203
pubmed: 25550518
doi: 10.1073/pnas.1420406112
Kopf SH, McGlynn SE, Green-Saxena A, Guan Y, Newman DK, Orphan VJ (2015) Heavy water and 15 N labelling with N ano SIMS analysis reveals growth rate-dependent metabolic heterogeneity in chemostats. Environ Microbiol 17(7):2542–2556
pubmed: 25655651
pmcid: 4587896
doi: 10.1111/1462-2920.12752
Ploug H, Musat N, Adam B, Moraru CL, Lavik G, Vagner T, Bergman B, Kuypers MMM (2010) Carbon and nitrogen fluxes associated with the cyanobacterium Aphanizomenon sp. in the Baltic Sea. ISME J 4(9):1215–1223
pubmed: 20428225
doi: 10.1038/ismej.2010.53
Scheller S, Yu H, Chadwick GL, McGlynn SE, Orphan VJ (2016) Artificial electron acceptors decouple archaeal methane oxidation from sulfate reduction. Science 351(6274):703–707
pubmed: 26912857
doi: 10.1126/science.aad7154
Dekas AE, Connon SA, Chadwick GL, Trembath-Reichert E, Orphan VJ (2016) Activity and interactions of methane seep microorganisms assessed by parallel transcription and FISH-NanoSIMS analyses. ISME J 10(3):678–692
pubmed: 26394007
doi: 10.1038/ismej.2015.145
Green-Saxena A, Dekas AE, Dalleska NF, Orphan VJ (2014) Nitrate-based niche differentiation by distinct sulfate-reducing bacteria involved in the anaerobic oxidation of methane. ISME J 8(1):150–163
pubmed: 24008326
doi: 10.1038/ismej.2013.147
Milucka J, Kirf M, Lu L, Krupke A, Lam P, Littmann S, Kuypers MMM, Schubert CJ (2015) Methane oxidation coupled to oxygenic photosynthesis in anoxic waters. ISME J 9(9):1991–2002
pubmed: 25679533
pmcid: 4542029
doi: 10.1038/ismej.2015.12
Marlow JJ, Steele JA, Ziebis W, Thurber AR, Levin LA, Orphan VJ (2014) Carbonate-hosted methanotrophy represents an unrecognized methane sink in the deep sea. Nat Commun 5(1):1–12
doi: 10.1038/ncomms6094
Oswald K, Graf JS, Littmann S, Tienken D, Brand A, Wehrli B, Albertsen M, Daims H, Wagner M, Kuypers MM (2017) Crenothrix are major methane consumers in stratified lakes. ISME J 11(9):2124–2140
pubmed: 28585934
pmcid: 5563964
doi: 10.1038/ismej.2017.77
Foster RA, Kuypers MM, Vagner T, Paerl RW, Musat N, Zehr JP (2011) Nitrogen fixation and transfer in open ocean diatom-cyanobacterial symbioses. ISME J 5(9):1484–1493
pubmed: 21451586
pmcid: 3160684
doi: 10.1038/ismej.2011.26
Thompson AW, Foster RA, Krupke A, Carter BJ, Musat N, Vaulot D, Kuypers MMM, Zehr JP (2012) Unicellular cyanobacterium symbiotic with a single-celled eukaryotic alga. Science 337(6101):1546–1550
pubmed: 22997339
doi: 10.1126/science.1222700
Adam B, Klawonn I, Sveden JB, Bergkvist J, Nahar N, Walve J, Littmann S, Whitehouse MJ, Lavik G, Kuypers MMM, Ploug H (2016) N2-fixation, ammonium release and N-transfer to the microbial and classical food web within a plankton community. ISME J 10(2):450–459
pubmed: 26262817
doi: 10.1038/ismej.2015.126
Berry D, Stecher B, Schintlmeister A, Reichert J, Brugiroux S, Wild B, Wanek W, Richter A, Rauch I, Decker T (2013) Host-compound foraging by intestinal microbiota revealed by single-cell stable isotope probing. Proc Natl Acad Sci 110(12):4720–4725
pubmed: 23487774
pmcid: 3607026
doi: 10.1073/pnas.1219247110
Carpenter KJ, Weber PK, Davisson ML, Pett-Ridge J, Haverty MI, Keeling PJ (2013) Correlated SEM, FIB-SEM, TEM, and NanoSIMS imaging of microbes from the hindgut of a lower termite: methods for in situ functional and ecological studies of uncultivable microbes. Microsc Microanal 19(06):1490–1501
pubmed: 24119340
doi: 10.1017/S1431927613013482
Tai V, Carpenter KJ, Weber PK, Nalepa CA, Perlman SJ, Keeling PJ (2016) Genome evolution and nitrogen-fixation in bacterial ectosymbionts of a protist inhabiting wood-feeding cockroaches. Appl Environ Microbiol. https://doi.org/10.1128/AEM.00611-16
Ceh J, Kilburn MR, Cliff JB, Raina JB, van Keulen M, Bourne DG (2013) Nutrient cycling in early coral life stages: Pocillopora damicornis larvae provide their algal symbiont (Symbiodinium) with nitrogen acquired from bacterial associates. Ecol Evol 3(8):2393–2400
doi: 10.1002/ece3.642
Pernice M, Dunn SR, Tonk L, Dove S, Domart-Coulon I, Hoppe P, Schintlmeister A, Wagner M, Meibom A (2015) A nanoscale secondary ion mass spectrometry study of dinoflagellate functional diversity in reef-building corals. Environ Microbiol 17(10):3570–3580
pubmed: 24902979
doi: 10.1111/1462-2920.12518
Wangpraseurt D, Pernice M, Guagliardo P, Kilburn MR, Clode PL, Polerecky L, Kühl M (2016) Light microenvironment and single-cell gradients of carbon fixation in tissues of symbiont-bearing corals. ISME J 10(3):788–792
pubmed: 26241503
doi: 10.1038/ismej.2015.133
Lema KA, Clode PL, Kilburn MR, Thornton R, Willis BL, Bourne DG (2016) Imaging the uptake of nitrogen-fixing bacteria into larvae of the coral Acropora millepora. ISME J 10(7):1804–1808
pubmed: 26696324
doi: 10.1038/ismej.2015.229
Kopp C, Domart-Coulon I, Barthelemy D, Meibom A (2016) Nutritional input from dinoflagellate symbionts in reef-building corals is minimal during planula larval life stage. Sci Adv 2(3):e1500681
pubmed: 27051861
pmcid: 4820372
doi: 10.1126/sciadv.1500681
Yang S-H, Tandon K, Lu C-Y, Wada N, Shih C-J, Hsiao SS-Y, Jane W-N, Lee T-C, Yang C-M, Liu C-T (2019) Metagenomic, phylogenetic, and functional characterization of predominant endolithic green sulfur bacteria in the coral Isopora palifera. Microbiome 7(1):1–13
doi: 10.1186/s40168-018-0616-z
Samo TJ, Kimbrel JA, Nilson DJ, Pett-Ridge J, Weber PK, Mayali X (2018) Attachment between heterotrophic bacteria and microalgae influences symbiotic microscale interactions. Environ Microbiol 20(2):4385–4400
pubmed: 30022580
doi: 10.1111/1462-2920.14357
de-Bashan LE, Mayali X, Bebout BM, Weber PK, Detweiler AM, Hernandez J-P, Prufert-Bebout L, Bashan Y (2016) Establishment of stable synthetic mutualism without co-evolution between microalgae and bacteria demonstrated by mutual transfer of metabolites (NanoSIMS isotopic imaging) and persistent physical association (fluorescent in situ hybridization). Algal Res 15:179–186
doi: 10.1016/j.algal.2016.02.019
Alonso C, Musat N, Adam B, Kuypers M, Amann R (2012) HISH–SIMS analysis of bacterial uptake of algal-derived carbon in the Río de la Plata estuary. Syst Appl Microbiol 35(8):541–548
pubmed: 23026312
doi: 10.1016/j.syapm.2012.08.004
Leroy C, Jauneau A, Martinez Y, Cabin-Flaman A, Gibouin D, Orivel J, Séjalon-Delmas N (2017) Exploring fungus–plant N transfer in a tripartite ant–plant–fungus mutualism. Ann Bot 120(3):417–426
pmcid: 5591417
doi: 10.1093/aob/mcx064
pubmed: 5591417
Lee JZ, Burow LC, Woebken D, Everroad RC, Kubo MD, Spormann AM, Weber PK, Pett-Ridge J, Bebout BM, Hoehler TM (2014) Fermentation couples chloroflexi and sulfate-reducing bacteria to cyanobacteria in hypersaline microbial mats. Front Microbiol 5:61
pubmed: 24616716
pmcid: 3935151
Nuccio EE, Hodge A, Pett-Ridge J, Herman DJ, Weber PK, Firestone MK (2013) An arbuscular mycorrhizal fungus significantly modifies the soil bacterial community and nitrogen cycling during litter decomposition. Environ Microbiol 15(6):1870–1881
pubmed: 23360621
doi: 10.1111/1462-2920.12081
Kaiser C, Kilburn MR, Clode PL, Fuchslueger L, Koranda M, Cliff JB, Solaiman ZM, Murphy DV (2015) Exploring the transfer of recent plant photosynthates to soil microbes: mycorrhizal pathway vs direct root exudation. New Phytol 205(4):1537–1551
pubmed: 25382456
doi: 10.1111/nph.13138
Kuga Y, Sakamoto N, Yurimoto H (2014) Stable isotope cellular imaging reveals that both live and degenerating fungal pelotons transfer carbon and nitrogen to orchid protocorms. New Phytol 202(2):594–605
pubmed: 24494717
doi: 10.1111/nph.12700
Pett-Ridge J, Firestone MK (2017) Using stable isotopes to explore root-microbe-mineral interactions in soil. Rhizosphere 3:244–253
doi: 10.1016/j.rhisph.2017.04.016
Hestrin R, Hammer EC, Mueller CW, Lehmann J (2019) Synergies between mycorrhizal fungi and soil microbial communities increase plant nitrogen acquisition. Commun Biol 2(1):1–9
doi: 10.1038/s42003-019-0481-8
Gorka S, Dietrich M, Mayerhofer W, Gabriel R, Wiesenbauer J, Martin V, Zheng Q, Imai B, Prommer J, Weidinger M (2019) Rapid transfer of plant photosynthates to soil bacteria via ectomycorrhizal hyphae and its interaction with nitrogen availability. Front Microbiol 10:168
pubmed: 30863368
pmcid: 6399413
doi: 10.3389/fmicb.2019.00168
Worrich A, Stryhanyuk H, Musat N, König S, Banitz T, Centler F, Frank K, Thullner M, Harms H, Richnow H-H (2017) Mycelium-mediated transfer of water and nutrients stimulates bacterial activity in dry and oligotrophic environments. Nat Commun 8(1):1–9
doi: 10.1038/ncomms15472
Bougoure J, Ludwig M, Brundrett M, Cliff J, Clode P, Kilburn M, Grierson P (2014) High-resolution secondary ion mass spectrometry analysis of carbon dynamics in mycorrhizas formed by an obligately myco-heterotrophic orchid. Plant Cell Environ 37(5):1223–1230
pubmed: 24237204
doi: 10.1111/pce.12230
Hill PW, Broughton R, Bougoure J, Havelange W, Newsham KK, Grant H, Murphy DV, Clode P, Ramayah S, Marsden KA (2019) Angiosperm symbioses with non-mycorrhizal fungal partners enhance N acquisition from ancient organic matter in a warming maritime Antarctic. Ecol Lett 22(12):2111–2119
pubmed: 31621153
pmcid: 6899649
doi: 10.1111/ele.13399
Mergelov N, Mueller CW, Prater I, Shorkunov I, Dolgikh A, Zazovskaya E, Shishkov V, Krupskaya V, Abrosimov K, Cherkinsky A (2018) Alteration of rocks by endolithic organisms is one of the pathways for the beginning of soils on Earth. Sci Rep 8(1):1–15
doi: 10.1038/s41598-018-21682-6
Kopittke PM, Dalal RC, Hoeschen C, Li C, Menzies NW, Mueller CW (2020) Soil organic matter is stabilized by organo-mineral associations through two key processes: the role of the carbon to nitrogen ratio. Geoderma 357:113974
doi: 10.1016/j.geoderma.2019.113974
Keiluweit M, Bougoure JJ, Zeglin LH, Myrold DD, Weber PK, Pett-Ridge J, Kleber M, Nico PS (2012) Nano-scale investigation of the association of microbial nitrogen residues with iron (hydr)oxides in a forest soil O-horizon. Geochim Cosmochim Acta 95:213–226
doi: 10.1016/j.gca.2012.07.001
Keiluweit M, Bougoure JJ, Nico PS, Pett-Ridge J, Weber PK, Kleber M (2015) Mineral protection of soil carbon counteracted by root exudates. Nat Clim Chang 5(6):588–595
doi: 10.1038/nclimate2580
Morrison KD, Misra R, Williams LB (2016) Unearthing the antibacterial mechanism of medicinal clay: a geochemical approach to combating antibiotic resistance. Sci Rep 6:19043
pubmed: 26743034
pmcid: 4705759
doi: 10.1038/srep19043
Londono SC, Hartnett HE, Williams LB (2017) Antibacterial activity of aluminum in clay from the Colombian Amazon. Environ Sci Technol 51(4):2401–2408
pubmed: 28121138
doi: 10.1021/acs.est.6b04670
Eichorst SA, Strasser F, Woyke T, Schintlmeister A, Wagner M, Woebken D (2015) Advancements in the application of NanoSIMS and Raman microspectroscopy to investigate the activity of microbial cells in soils. FEMS Microbiol Ecol 91(10):fiv106
pubmed: 26324854
pmcid: 4629873
doi: 10.1093/femsec/fiv106
Pasulka AL, Thamatrakoln K, Kopf SH, Guan Y, Poulos B, Moradian A, Sweredoski MJ, Hess S, Sullivan MB, Bidle KD (2018) Interrogating marine virus-host interactions and elemental transfer with BONCAT and nanoSIMS-based methods. Environ Microbiol 20(2):671–692
pubmed: 29159966
doi: 10.1111/1462-2920.13996
Greenwood DJ, Dos Santos MS, Huang S, Russell MR, Collinson LM, MacRae JI, West A, Jiang H, Gutierrez MG (2019) Subcellular antibiotic visualization reveals a dynamic drug reservoir in infected macrophages. Science 364(6447):1279–1282
pubmed: 31249058
pmcid: 7012645
doi: 10.1126/science.aat9689
Gates SD, Condit RC, Moussatche N, Stewart BJ, Malkin AJ, Weber PK (2018) High initial sputter rate found for vaccinia virions using isotopic labeling, nanoSIMS, and AFM. Anal Chem 90(3):1613–1620
pubmed: 29295620
doi: 10.1021/acs.analchem.7b02786
Stuart RK, Mayali X, Boaro AA, Zemla A, Everroad RC, Nilson D, Weber PK, Lipton M, Bebout BM, Pett-Ridge J (2016) Light regimes shape utilization of extracellular organic C and N in a cyanobacterial biofilm. mBio 7(3):e00650–e00616
pubmed: 27353754
pmcid: 4937211
doi: 10.1128/mBio.00650-16
Stuart RK, Mayali X, Lee JZ, Everroad RC, Hwang M, Bebout BM, Weber PK, Pett-Ridge J, Thelen MP (2016) Cyanobacterial reuse of extracellular organic carbon in microbial mats. ISME J 10(5):1240–1251
pubmed: 26495994
doi: 10.1038/ismej.2015.180
Stuart RK, Mayali X, Thelen MP, Pett-Ridge J, Weber PK (2017) Measuring cyanobacterial metabolism in biofilms with NanoSIMS isotope imaging and scanning electron microscopy (SEM). Bioprotocol 7:e2263
Probst AJ, Weinmaier T, Raymann K, Perras A, Emerson JB, Rattei T, Wanner G, Klingl A, Berg IA, Yoshinaga M, Viehweger B, Hinrichs K-U, Thomas BC, Meck S, Auerbach AK, Heise M, Schintlmeister A, Schmid M, Wagner M, Gribaldo S, Banfield JF, Moissl-Eichinger C (2014) Biology of a widespread uncultivated archaeon that contributes to carbon fixation in the subsurface. Nat Commun 5:5497
pubmed: 25425419
doi: 10.1038/ncomms6497
Tveit AT, Hestnes AG, Robinson SL, Schintlmeister A, Dedysh SN, Jehmlich N, von Bergen M, Herbold C, Wagner M, Richter A (2019) Widespread soil bacterium that oxidizes atmospheric methane. Proc Natl Acad Sci 116(17):8515–8524
pubmed: 30962365
pmcid: 6486757
doi: 10.1073/pnas.1817812116
Sheik AR, Muller EE, Audinot J-N, Lebrun LA, Grysan P, Guignard C, Wilmes P (2016) In situ phenotypic heterogeneity among single cells of the filamentous bacterium Candidatus Microthrix parvicella. ISME J 10(5):1274–1279
pubmed: 26505828
doi: 10.1038/ismej.2015.181
Nikolic N, Schreiber F, Kiviet DJ, Bergmiller T, Littmann S, Kuypers MM, Ackermann M (2017) Cell-to-cell variation and specialization in sugar metabolism in clonal bacterial populations. PLoS Genet 13(12):e1007122
pubmed: 29253903
pmcid: 5773225
doi: 10.1371/journal.pgen.1007122
Gangwe Nana GY, Ripoll C, Cabin-Flaman A, Gibouin D, Delaune A, Jannière L, Grancher G, Chagny G, Loutelier-Bourhis C, Lentzen E (2018) Division-based, growth rate diversity in bacteria. Front Microbiol 9:849
pubmed: 29867792
pmcid: 5958220
doi: 10.3389/fmicb.2018.00849
Zimmermann M, Escrig S, Hübschmann T, Kirf MK, Brand A, Inglis RF, Musat N, Müller S, Meibom A, Ackermann M (2015) Phenotypic heterogeneity in metabolic traits among single cells of a rare bacterial species in its natural environment quantified with a combination of flow cell sorting and NanoSIMS. Front Microbiol 6:243
pubmed: 25932020
pmcid: 4399338
doi: 10.3389/fmicb.2015.00243
Tsednee M, Castruita M, Salomé PA, Sharma A, Lewis BE, Schmollinger SR, Strenkert D, Holbrook K, Otegui MS, Khatua K (2019) Manganese co-localizes with calcium and phosphorus in Chlamydomonas acidocalcisomes and is mobilized in manganese-deficient conditions. J Biol Chem 294(46):17626–17641
pubmed: 31527081
pmcid: 6873200
doi: 10.1074/jbc.RA119.009130
Kessler N, Armoza-Zvuloni R, Wang S, Basu S, Weber PK, Stuart RK, Shaked Y (2020) Selective collection of iron-rich dust particles by natural Trichodesmium colonies. ISME J 14(1):91–103
pubmed: 31551530
doi: 10.1038/s41396-019-0505-x
Newsome L, Lopez Adams R, Downie HF, Moore KL, Lloyd JR (2018) NanoSIMS imaging of extracellular electron transport processes during microbial iron (III) reduction. FEMS Microbiol Ecol 94(8):fiy104
pmcid: 6041951
doi: 10.1093/femsec/fiy104
pubmed: 6041951
Fleming E, Woyke T, Donatello R, Kuypers MM, Sczyrba A, Littmann S, Emerson D (2018) Insights into the fundamental physiology of the uncultured Fe-oxidizing bacterium Leptothrix ochracea. Appl Environ Microbiol 84(9). https://doi.org/10.1128/AEM.02239-17
Stryhanyuk H, Calabrese F, Kümmel S, Musat F, Richnow HH, Musat N (2018) Calculation of single cell assimilation rates from SIP-NanoSIMS-derived isotope ratios: a comprehensive approach. Front Microbiol 9:2342
pubmed: 30337916
pmcid: 6178922
doi: 10.3389/fmicb.2018.02342
Arandia-Gorostidi N, Weber PK, Alonso-Saez L, Moran XAG, Mayali X (2017) Elevated temperature increases carbon and nitrogen fluxes between phytoplankton and heterotrophic bacteria through physical attachment. ISME J 11(3):641–650
pubmed: 27922602
doi: 10.1038/ismej.2016.156
Frisz JF, Lou K, Klitzing HA, Hanafin WP, Lizunov V, Wilson RL, Carpenter KJ, Kim R, Hutcheon ID, Zimmerberg J (2013) Direct chemical evidence for sphingolipid domains in the plasma membranes of fibroblasts. Proc Natl Acad Sci 110(8):E613–E622
pubmed: 23359681
pmcid: 3581929
doi: 10.1073/pnas.1216585110
Smith NS, Boswell RW, Tesch PP, Martin NP (2017) Rf system, magnetic filter, and high voltage isolation for an inductively coupled plasma ion source, Google Patents
Smith N, Tesch P, Martin N, Kinion D (2008) A high brightness source for nano-probe secondary ion mass spectrometry. Appl Surf Sci 255(4):1606–1609
doi: 10.1016/j.apsusc.2008.05.141
Malherbe J, Penen F, Isaure M-P, Frank J, Hause G, Dobritzsch D, Gontier E, Horréard FO, Hillion FO, Schaumlöffel D (2016) A new radio frequency plasma oxygen primary ion source on nano secondary ion mass spectrometry for improved lateral resolution and detection of electropositive elements at single cell level. Anal Chem 88(14):7130–7136
pubmed: 27291826
doi: 10.1021/acs.analchem.6b01153
Cabin-Flaman A, Monnier AFO, Coffinier Y, Audinot J-N, Gibouin D, Wirtz T, Boukherroub R, Migeon H-N, Bensimon A, Jannière L (2011) Combed single DNA molecules imaged by secondary ion mass spectrometry. Anal Chem 83(18):6940–6947
pubmed: 21851091
doi: 10.1021/ac201685t
Cabin-Flaman A, Monnier A-F, Coffinier Y, Audinot J-N, Gibouin D, Wirtz T, Boukherroub R, Migeon H-N, Bensimon A, Jannière L (2016) Combining combing and secondary ion mass spectrometry to study DNA on chips using 13C and 15N labeling. F1000Res 5:27429742
doi: 10.12688/f1000research.8361.1
Weber PK, Graham GA, Teslich NE, MoberlyChan W, Ghosal S, Leighton TJ, Wheeler KE (2010) NanoSIMS imaging of Bacillus spores sectioned by focused ion beam. J Microsc 238:189–199
pubmed: 20579257
doi: 10.1111/j.1365-2818.2009.03336.x
Wilson RG, Stevie FA, Magee CW (1989) Secondary ion mass spectrometry: a practical handbook for depth profiling and bulk impurity analysis. Wiley, New York, NY
Polerecky L, Adam B, Milucka J, Musat N, Vagner T, Kuypers MM (2012) Look@ NanoSIMS–a tool for the analysis of nanoSIMS data in environmental microbiology. Environ Microbiol 14(4):1009–1023
pubmed: 22221878
doi: 10.1111/j.1462-2920.2011.02681.x
Huang W, Hammel KE, Hao J, Thompson A, Timokhin VI, Hall SJ (2019) Enrichment of lignin-derived carbon in mineral-associated soil organic matter. Environ Sci Technol 53(13):7522–7531
pubmed: 31177774
doi: 10.1021/acs.est.9b01834
Whitman T, Zhu Z, Lehmann J (2014) Carbon mineralizability determines interactive effects on mineralization of pyrogenic organic matter and soil organic carbon. Environ Sci Technol 48(23):13727–13734
pubmed: 25361379
doi: 10.1021/es503331y
Hatton P-J, Remusat L, Zeller B, Brewer EA, Derrien D (2015) NanoSIMS investigation of glycine-derived C and N retention with soil organo-mineral associations. Biogeochemistry 125(3):303–313
doi: 10.1007/s10533-015-0138-8
Li T, Wu TD, Mazeas L, Toffin L, Guerquin-Kern JL, Leblon G, Bouchez T (2008) Simultaneous analysis of microbial identity and function using NanoSIMS. Environ Microbiol 10(3):580–588
pubmed: 18028417
pmcid: 2253709
doi: 10.1111/j.1462-2920.2007.01478.x
Benn PA, Perle MA (1992) Chromosome staining and banding techniques. In: Rooney DE, Czepulkowski BH (eds) Human cytogenetics: volume I, constitutional analysis: a practical approach. Oxford University Press, New York, NY
Latt SA (1973) Microfluorometric detection of deoxyribonucleic acid replication in human metaphase chromosomes. Proc Natl Acad Sci U S A 49:3395–3399
doi: 10.1073/pnas.70.12.3395
Manefield M, Whiteley AS, Griffiths RI, Bailey MJ (2002) RNA stable isotope probing, a novel means of linking microbial community function to phylogeny. Appl Environ Microbiol 68:5367–5373
pubmed: 12406726
pmcid: 129944
doi: 10.1128/AEM.68.11.5367-5373.2002
Radajewski S, Ineson P, Parekh NR, Murrell J (2000) Stable-isotope probing as a tool in microbial ecology. Nature 403(10):646–649
pubmed: 10688198
doi: 10.1038/35001054
Jensen LHS, Cheng T, Plane FOV, Escrig S, Comment A, van den Brandt B, Humbel BM, Meibom A (2016) En route to ion microprobe analysis of soluble compounds at the single cell level: the CryoNanoSIMS. In: European microscopy congress 2016: proceedings. Wiley, New York, NY
Lovrić J, Malmberg P, Johansson BR, Fletcher JS, Ewing AG (2016) Multimodal imaging of chemically fixed cells in preparation for NanoSIMS. Anal Chem 88(17):8841–8848
pubmed: 27462909
doi: 10.1021/acs.analchem.6b02408
Gibbin E, Gavish A, Domart-Coulon I, Kramarsky-Winter E, Shapiro O, Meibom A, Vardi A (2018) Using NanoSIMS coupled with microfluidics to visualize the early stages of coral infection by Vibrio coralliilyticus. BMC Microbiol 18(1):1–10
doi: 10.1186/s12866-018-1173-0
Nunan N, Ritz K, Crabb D, Harris K, Wu K, Crawford JW, Young IM (2001) Quantification of the in situ distribution of soil bacteria by large-scale imaging of thin sections of undisturbed soil. FEMS Microbiol Ecol 37(1):67–77
doi: 10.1111/j.1574-6941.2001.tb00854.x
Kuo J (2007) Electron microscopy: methods and protocols. In: Methods in molecular biology, 2nd edn. Humana, Totowa, NJ
Tippkötter R, Ritz K (1996) Evaluation of polyester, epoxy and acrylic resins for suitability in preparation of soil thin sections for in situ biological studies. Geoderma 69(1–2):31–57
doi: 10.1016/0016-7061(95)00041-0
Chandra S, Morrison GH (1992) Sample preparation of animal tissues and cell cultures for secondary ion mass spectrometry (SIMS) microscopy. Biol Cell 74:31–42
pubmed: 1511245
doi: 10.1016/0248-4900(92)90006-M
Dykstra MJ, Reuss LE (eds) (2003) Biological electron microscopy: theory, techniques and troubleshooting, 2nd edn. Kluwer Academic/Plenum Publishers, New York, NY
Echlin P (1992) Low-temperature microscopy and analysis. Springer, New York, NY
doi: 10.1007/978-1-4899-2302-8
Musat N, Stryhanyuk H, Bombach P, Adrian L, Audinot J-N, Richnow HH (2014) The effect of FISH and CARD-FISH on the isotopic composition of 13C- and 15N-labeled Pseudomonas putida cells measured by nanoSIMS. Syst Appl Microbiol 37(4):267–276
pubmed: 24702905
doi: 10.1016/j.syapm.2014.02.002
Woebken D, Burow LC, Behnam F, Mayali X, Schintlmeister A, Fleming ED, Prufert-Bebout L, Singer SW, Lopez Cortes A, Hoehler TM, Pett-Ridge J, Spormann AM, Wagner M, Weber PK, Bebout BM (2015) Revisiting N-2 fixation in Guerrero Negro intertidal microbial mats with a functional single-cell approach. ISME J 9(2):485–496
pubmed: 25303712
doi: 10.1038/ismej.2014.144
Herrmann AM, Clode PL, Fletcher IR, Nunan N, Stockdale EA, O'Donnel AG, Murphy DV (2007) A novel method for the study of the biophysical interface in soils using nano-scale secondary ion mass spectrometry. Rapid Commun Mass Spectrom 21(1):29–34
pubmed: 17131465
doi: 10.1002/rcm.2811
Weng N, Jiang H, Wang W-X (2017) In situ subcellular imaging of copper and zinc in contaminated oysters revealed by nanoscale secondary ion mass spectrometry. Environ Sci Technol 51(24):14426–14435
pubmed: 29172472
doi: 10.1021/acs.est.7b05090
Rogge A, Flintrop CM, Iversen MH, Salter I, Fong AA, Vogts A, Waite AM (2018) Hard and soft plastic resin embedding for single-cell element uptake investigations of marine-snow-associated microorganisms using nano-scale secondary ion mass spectrometry. Limnol Oceanogr Methods 16(8):484–503
doi: 10.1002/lom3.10261
Fike DA, Gammon CL, Ziebis W, Orphan VJ (2008) Micron-scale mapping of sulfur cycling across the oxycline of a cyanobacterial mat: a paired nanoSIMS and CARD-FISH approach. ISME J 2(7):749–759
pubmed: 18528418
doi: 10.1038/ismej.2008.39
De Gregorio BT, Stroud RM, Nittler LR, Alexander CMOD, Kilcoyne ALD, Zega TJ (2010) Isotopic anomalies in organic nanoglobules from Comet 81P/Wild 2: comparison to Murchison nanoglobules and isotopic anomalies induced in terrestrial organics by electron irradiation. Geochim Cosmochim Acta 74(15):4454–4470
doi: 10.1016/j.gca.2010.05.010
Lehmann J, Liang BQ, Solomon D, Lerotic M, Luizao F, Kinyangi J, Schafer T, Wirick S, Jacobsen C (2005) Near-edge X-ray absorption fine structure (NEXAFS) spectroscopy for mapping nano-scale distribution of organic carbon forms in soil: application to black carbon particles. Global Biogeochem Cycles 29:Art. No. GB1013
Flynn GJ, Keller LP, Jacobsen C, Wirick S (2004) An assessment of the amount and types of organic matter contributed to the Earth by interplanetary dust. Adv Space Res 33:57–66
doi: 10.1016/j.asr.2003.09.036
Gnaser H (1997) Formation of metastable N2- and CO-anions in sputtering. Phys Rev A 56(4):R2518
doi: 10.1103/PhysRevA.56.R2518
McMahon G, Saint-Cyr HF, Lechene C, Unkefer CJ (2006) CN− secondary ions form by recombination as demonstrated using multi-isotope mass spectrometry of 13C- and 15N-labeled polyglycine. J Am Soc Mass Spectrom 17(8):1181–1187
pubmed: 16750387
doi: 10.1016/j.jasms.2006.04.031
Mayali X, Weber PK, Nuccio E, Lietard J, Somoza M, Blazewicz SJ, Pett-Ridge J (2019) Chip-SIP: stable isotope probing analyzed with rRNA-targeted microarrays and NanoSIMS. In: Stable isotope probing. Springer, New York, NY, pp 71–87
doi: 10.1007/978-1-4939-9721-3_6
Gnaser H (1999) Singly-and doubly-negative carbon clusters in sputtering: energy spectra, abundance distributions and unimolecular fragmentation. Nucl Instrum Methods Phys Res, Sect B 149(1–2):38–52
doi: 10.1016/S0168-583X(98)00756-3
Weber PK, Bacon CR, Hutcheon ID, Ingram BL, Wooden JL (2005) Ion microprobe measurement of strontium isotopes in calcium carbonate with application to salmon otoliths. Geochim Cosmochim Acta 69(5):1225–1239
doi: 10.1016/j.gca.2004.05.051
Ghosal S, Fallon SJ, Leighton T, Wheeler K, Hutcheon ID, Weber PK (2006) Analysis of bacterial spore permeability to water and ions using NanoSecondary Ion Mass Spectrometry (NanoSIMS). Abstr Pap Am Chem Soc 231:3
Wolfe-Simon F, Blum JS, Kulp TR, Gordon GW, Hoeft SE, Pett-Ridge J, Stolz JF, Webb SM, Weber PK, Davies PCW, Anbar AD, Oremland RS (2011) A bacterium that can grow by using arsenic instead of phosphorus. Science 332(6034):1163–1166
pubmed: 21127214
doi: 10.1126/science.1197258
Hauri EH, Papineau D, Wang J, Hillion F (2016) High-precision analysis of multiple sulfur isotopes using NanoSIMS. Chem Geol 420:148–161
doi: 10.1016/j.chemgeo.2015.11.013
Chandra S, Smith DR, Morrison GH (2000) Subcellular imaging by dynamic SIMS ion microscopy. Anal Chem 72:104A–114A
pubmed: 10695124
doi: 10.1021/ac002716i
Guerquin-Kern JL, Wu TD, Quintana C, Croisy A (2005) Progress in analytical imaging of the cell by dynamic secondary ion mass spectrometry (SIMS microscopy). BBA-Gen Subjects 1724(3):228–238
doi: 10.1016/j.bbagen.2005.05.013
Burns MS, File DM, Deline V, Galle P (1986) Matrix effects in secondary ion mass spectrometric analysis of biological tissue. Scan Electron Microscopy 1986(4):1277–1290
Harris WC, Chandra S, Morrison GH (1983) Ion implantation for quantitative ion microscopy of biological soft tissue. Anal Chem 55(12):1959–1963
pubmed: 6638519
doi: 10.1021/ac00262a029
Phinney D (2006) Quantitative analysis of microstructures by secondary ion mass spectrometry. Microsc Microanal 12(4):352
pubmed: 16842652
doi: 10.1017/S1431927606060399
Decelle J, Veronesi G, Gallet B, Stryhanyuk H, Benettoni P, Schmidt M, Tucoulou R, Passarelli M, Bohic S, Clode P (2020) Subcellular chemical imaging: new avenues in cell biology. Trends Cell Biol 30(3):173–188
pubmed: 31987730
doi: 10.1016/j.tcb.2019.12.007
Penen F, Malherbe J, Isaure M-P, Dobritzsch D, Bertalan I, Gontier E, Le Coustumer P, Schaumlöffel D (2016) Chemical bioimaging for the subcellular localization of trace elements by high contrast TEM, TEM/X-EDS, and NanoSIMS. J Trace Elem Med Biol 37:62–68
pubmed: 27288221
doi: 10.1016/j.jtemb.2016.04.014
Nomaki H, LeKieffre C, Escrig S, Meibom A, Yagyu S, Richardson EA, Matsuzaki T, Murayama M, Geslin E, Bernhard JM (2018) Innovative TEM-coupled approaches to study foraminiferal cells. Mar Micropaleontol 138:90–104
doi: 10.1016/j.marmicro.2017.10.002
Kraft ML, Weber PK, Longo ML, Hutcheon ID, Boxer SG (2006) Phase separation of lipid membranes analyzed with high-resolution secondary ion mass spectrometry. Science 313:1948–1951
pubmed: 17008528
doi: 10.1126/science.1130279
Wirtz T, Fleming Y, Gysin U, Glatzel T, Wegmann U, Meyer E, Maier U, Rychen J (2013) Combined SIMS-SPM instrument for high sensitivity and high-resolution elemental 3D analysis. Surf Interface Anal 45(1):513–516
doi: 10.1002/sia.5010
Orphan VJ, House CH, Hinrichs K-U, McKeegan KD, DeLong EF (2001) Methane-consuming Archaea revealed by directly coupled isotopic and phylogenetic analysis. Science 293:484–487
pubmed: 11463914
doi: 10.1126/science.1061338
Amann RI, Krumholz L, Stahl DA (1990) Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. J Bacteriol 172(2):762–770
pubmed: 1688842
pmcid: 208504
doi: 10.1128/jb.172.2.762-770.1990
Pernthaler A, Pernthaler J, Amann R (2002) Fluorescence in situ hybridization and catalyzed reporter deposition for the identification of marine bacteria. Appl Environ Microbiol 68(6):3094–3101
pubmed: 12039771
pmcid: 123953
doi: 10.1128/AEM.68.6.3094-3101.2002
Woebken D, Burow LC, Prufert-Bebout L, Bebout BM, Hoehler TM, Pett-Ridge J, Spormann AM, Weber PK, Singer SW (2012) Identification of a novel cyanobacterial group as active diazotrophs in a coastal microbial mat using NanoSIMS analysis. ISME J 6(7):1427–1439
pubmed: 22237543
pmcid: 3379636
doi: 10.1038/ismej.2011.200
Lemaire R, Webb RI, Yuan Z (2008) Micro-scale observations of the structure of aerobic microbial granules used for the treatment of nutrient-rich industrial wastewater. ISME J 2(5):528–541
pubmed: 18256703
doi: 10.1038/ismej.2008.12
Hatzenpichler R, Scheller S, Tavormina PL, Babin BM, Tirrell DA, Orphan VJ (2014) In situ visualization of newly synthesized proteins in environmental microbes using amino acid tagging and click chemistry. Environ Microbiol 16(8):2568–2590
pubmed: 24571640
pmcid: 4122687
doi: 10.1111/1462-2920.12436
Bradley JP, Dai ZR, Erni R, Browning ND, Graham GA, Weber PK, Smith JB, Hutcheon ID, Ishii H, Bajt S, Floss C, Stadermann FJ, Sandford S (2005) An astronomical 2175 Å feature in interplanetary dust particles. Science 307:244–247
pubmed: 15653501
doi: 10.1126/science.1106717
Remusat L, Hatton P-J, Nico PS, Zeller B, Kleber M, Derrien D (2012) NanoSIMS study of organic matter associated with soil aggregates: advantages, limitations, and combination with STXM. Environ Sci Technol 46(7):3943–3949
pubmed: 22360342
doi: 10.1021/es203745k
pmcid: 22360342
De Samber B, De Rycke R, De Bruyne M, Kienhuis M, Sandblad L, Bohic S, Cloetens P, Urban C, Polerecky L, Vincze L (2020) Effect of sample preparation techniques upon single cell chemical imaging: a practical comparison between synchrotron radiation based X-ray fluorescence (SR-XRF) and nanoscopic secondary ion mass spectrometry (nano-SIMS). Anal Chim Acta 1106:22–32
pubmed: 32145852
doi: 10.1016/j.aca.2020.01.054
Lehmann J, Kinyangi J, Solomon D (2007) Organic matter stabilization in soil microaggregates: implications from spatial heterogeneity of organic carbon contents and carbon forms. Biogeochemistry 85(1):45–57
doi: 10.1007/s10533-007-9105-3
Wan J, Tyliszczak T, Tokunaga TK (2007) Organic carbon distribution, speciation, and elemental correlations within soil microaggregates: applications of STXM and NEXAFS spectroscopy. Geochim Cosmochim Acta 71(22):5439–5449
doi: 10.1016/j.gca.2007.07.030
Kopp C, Wisztorski M, Revel J, Mehiri M, Dani V, Capron L, Carette D, Fournier I, Massi L, Mouajjah D (2015) MALDI-MS and NanoSIMS imaging techniques to study cnidarian–dinoflagellate symbioses. Zoology 118(2):125–131
pubmed: 25447219
doi: 10.1016/j.zool.2014.06.006
Schlüter S, Eickhorst T, Mueller CW (2018) Correlative imaging reveals holistic view of soil microenvironments. Environ Sci Technol 53(2):829–837
pubmed: 30525511
doi: 10.1021/acs.est.8b05245
Lin S, Henze S, Lundgren P, Bergman B, Carpenter EJ (1998) Whole-cell immunolocalization of nitrogenase in marine diazotrophic cyanobacteria, Trichodesmium spp. Appl Environ Microbiol 64(8):3052–3058
pubmed: 9687472
pmcid: 106814
doi: 10.1128/AEM.64.8.3052-3058.1998
Levenson RM, Borowsky AD, Angelo M (2015) Immunohistochemistry and mass spectrometry for highly multiplexed cellular molecular imaging. Lab Investig 95(4):397–405
pubmed: 25730370
doi: 10.1038/labinvest.2015.2
Singer SW, Chan CS, Hwang MH, Zemla A, VerBerkmoes NC, Hettich RL, Banfield JF, Thelen MP (2008) Characterization of cytochrome579, an unusual cytochrome isolated from an iron-oxidizing microbial community. Appl Environ Microbiol 74:4454–4462
pubmed: 18469132
pmcid: 2493166
doi: 10.1128/AEM.02799-07
Gerard E, Guyot F, Philippot P, Lopez-Garcia P (2005) Fluorescence in situ hybridization coupled to ultra small immunogold detection to identify prokaryotic cells using transmission and scanning electron microscopy. J Microbiol Methods 63:20–28
pubmed: 15893390
doi: 10.1016/j.mimet.2005.02.018
Mayali X, Weber PK, Mabery S, Pett-Ridge J (2014) Phylogenetic patterns in the microbial response to resource availability: amino acid incorporation in San Francisco Bay. PLoS One 9(4):e95842
pubmed: 24752604
pmcid: 3994146
doi: 10.1371/journal.pone.0095842
Mayali X, Weber PK, Pett-Ridge J (2013) Taxon-specific C:N relative use efficiency for amino acids in an estuarine community. FEMS Microbiol Ecol 83(2):402–412
pubmed: 22994392
doi: 10.1111/j.1574-6941.12000.x
Bryson S, Li Z, Chavez F, Weber PK, Pett-Ridge J, Hettich RL, Pan C, Mayali X, Mueller RS (2017) Phylogenetically conserved resource partitioning in the coastal microbial loop. ISME J 11(12):2781–2792
pubmed: 28800138
pmcid: 5702734
doi: 10.1038/ismej.2017.128
Smith DF, Kiss A, Leach FE, Robinson EW, Paša-Tolić L, Heeren RM (2013) High mass accuracy and high mass resolving power FT-ICR secondary ion mass spectrometry for biological tissue imaging. Anal Bioanal Chem 405(18):6069–6076
pubmed: 23685962
doi: 10.1007/s00216-013-7048-1
Steele AV, Schwarzkopf A, McClelland JJ, Knuffman B (2017) High-brightness Cs focused ion beam from a cold-atomic-beam ion source. Nano Fut 1(1):015005
doi: 10.1088/2399-1984/aa6a48
Hayes JM (2004) An introduction to isotopic calculations. Woods Hole Oceanographic Institution, Woods Hole, MA, USA. https://www.whoi.edu/cms/files/jhayes/2005/9/IsoCalcs30Sept04_5183.pdf
Legin AA, Schintlmeister A, Jakupec MA, Galanski M, Lichtscheidl I, Wagner M, Keppler BK (2014) NanoSIMS combined with fluorescence microscopy as a tool for subcellular imaging of isotopically labeled platinum-based anticancer drugs. Chem Sci 5(8):3135-3143