Vibrational spectroscopy for imaging single microbial cells in complex biological samples

Harrison, Jesse P.; Berry, David

doi:10.3389/fmicb.2017.00675

Title: Vibrational spectroscopy for imaging single microbial cells in complex biological samples

Journal Article · Thu Apr 13 00:00:00 EDT 2017 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2017.00675· OSTI ID:1367190

Harrison, Jesse P. ^[1]; Berry, David ^[1]

Univ. of Vienna, Vienna (Austria)

Here, vibrational spectroscopy is increasingly used for the rapid and non-destructive imaging of environmental and medical samples. Both Raman and Fourier-transform infrared (FT-IR) imaging have been applied to obtain detailed information on the chemical composition of biological materials, ranging from single microbial cells to tissues. Due to its compatibility with methods such as stable isotope labeling for the monitoring of cellular activities, vibrational spectroscopy also holds considerable power as a tool in microbial ecology. Chemical imaging of undisturbed biological systems (such as live cells in their native habitats) presents unique challenges due to the physical and chemical complexity of the samples, potential for spectral interference, and frequent need for real-time measurements. This Mini Review provides a critical synthesis of recent applications of Raman and FT-IR spectroscopy for characterizing complex biological samples, with a focus on developments in single-cell imaging. We also discuss how new spectroscopic methods could be used to overcome current limitations of singlecell analyses. Given the inherent complementarity of Raman and FT-IR spectroscopic methods, we discuss how combining these approaches could enable us to obtain new insights into biological activities either in situ or under conditions that simulate selected properties of the natural environment.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: University of North Carolina, Chapel Hill, NC (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: SC0013887

OSTI ID:: 1367190

Journal Information:: Frontiers in Microbiology, Vol. 8; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 39 works

Citation information provided by
Web of Science

References (70)

Microfluidic approaches to synchrotron radiation-based Fourier transform infrared (SR-FTIR) spectral microscopy of living biosystems Loutherback, Kevin; Birarda, Giovanni; Chen, Liang Protein & Peptide Letters, Vol. 23, Issue 3 https://doi.org/10.2174/0929866523666160106154035	journal	February 2016
FTIR spectroscopic imaging of protein aggregation in living cells Miller, Lisa M.; Bourassa, Megan W.; Smith, Randy J. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1828, Issue 10 https://doi.org/10.1016/j.bbamem.2013.01.014	journal	October 2013
Biochemical label-free tissue imaging with subcellular-resolution synchrotron FTIR with focal plane array detector Kastyak-Ibrahim, M. Z.; Nasse, M. J.; Rak, M. NeuroImage, Vol. 60, Issue 1 https://doi.org/10.1016/j.neuroimage.2011.11.069	journal	March 2012
Micron-scale mapping of sulfur cycling across the oxycline of a cyanobacterial mat: a paired nanoSIMS and CARD-FISH approach Fike, David Andrew; Gammon, Crystal Lynn; Ziebis, Wiebke The ISME Journal, Vol. 2, Issue 7 https://doi.org/10.1038/ismej.2008.39	journal	June 2008
High-speed Raman imaging of cellular processes Ando, Jun; Palonpon, Almar F.; Sodeoka, Mikiko Current Opinion in Chemical Biology, Vol. 33 https://doi.org/10.1016/j.cbpa.2016.04.005	journal	August 2016
Application of Mid-infrared and Raman Spectroscopy to the Study of Bacteria Lu, Xiaonan; Al-Qadiri, Hamzah M.; Lin, Mengshi Food and Bioprocess Technology, Vol. 4, Issue 6 https://doi.org/10.1007/s11947-011-0516-8	journal	January 2011
Single cell stable isotope probing in microbiology using Raman microspectroscopy Wang, Yun; Huang, Wei E.; Cui, Li Current Opinion in Biotechnology, Vol. 41 https://doi.org/10.1016/j.copbio.2016.04.018	journal	October 2016
Real-Time Chemical Imaging of Bacterial Activity in Biofilms Using Open-Channel Microfluidics and Synchrotron FTIR Spectromicroscopy Holman, Hoi-Ying N.; Miles, Robin; Hao, Zhao Analytical Chemistry, Vol. 81, Issue 20 https://doi.org/10.1021/ac9015424	journal	October 2009
High-resolution Fourier-transform infrared chemical imaging with multiple synchrotron beams Nasse, Michael J.; Walsh, Michael J.; Mattson, Eric C. Nature Methods, Vol. 8, Issue 5 https://doi.org/10.1038/nmeth.1585	journal	March 2011
Rapid, accurate, and comparative differentiation of clinically and industrially relevant microorganisms via multiple vibrational spectroscopic fingerprinting Muhamadali, Howbeer; Subaihi, Abdu; Mohammadtaheri, Mahsa The Analyst, Vol. 141, Issue 17 https://doi.org/10.1039/c6an00883f	journal	January 2016
Self-organized patchiness facilitates survival in a cooperatively growing Bacillus subtilis population Ratzke, Christoph; Gore, Jeff Nature Microbiology, Vol. 1, Issue 5 https://doi.org/10.1038/nmicrobiol.2016.22	journal	March 2016
Rapid FTIR chemical imaging: highlighting FPA detectors Dorling, Konrad M.; Baker, Matthew J. Trends in Biotechnology, Vol. 31, Issue 8 https://doi.org/10.1016/j.tibtech.2013.05.008	journal	August 2013
Combining Raman and FT-IR Spectroscopy with Quantitative Isotopic Labeling for Differentiation of E. coli Cells at Community and Single Cell Levels Muhamadali, Howbeer; Chisanga, Malama; Subaihi, Abdu Analytical Chemistry, Vol. 87, Issue 8 https://doi.org/10.1021/acs.analchem.5b00892	journal	April 2015
Comparative Evaluation Of Raman Spectroscopy At Different Wavelengths For Extremophile Exemplars Villar, S. E. Jorge; Edwards, H. G. M.; Worland, M. R. Origins of Life and Evolution of Biospheres, Vol. 35, Issue 5 https://doi.org/10.1007/s11084-005-3528-4	journal	October 2005
Laser wavelength selection for Raman spectroscopy of microbial pigments in situ in Antarctic desert ecosystem analogues of former habitats on Mars Edwards, Howell G. M.; Newton, Emma M.; Wynn-Williams, David D. International Journal of Astrobiology, Vol. 1, Issue 4 https://doi.org/10.1017/S147355040300123X	journal	October 2002
Synchrotron FTIR microspectroscopy of Escherichia coli at single-cell scale under silver-induced stress conditions Saulou, Claire; Jamme, Frédéric; Girbal, Laurence Analytical and Bioanalytical Chemistry, Vol. 405, Issue 8 https://doi.org/10.1007/s00216-013-6725-4	journal	January 2013
Hyperspectral coherent Raman imaging - principle, theory, instrumentation, and applications to life sciences: Hyperspectral coherent Raman imaging Kano, Hideaki; Segawa, Hiroki; Okuno, Masanari Journal of Raman Spectroscopy, Vol. 47, Issue 1 https://doi.org/10.1002/jrs.4853	journal	December 2015
Evaluation of tip-enhanced Raman spectroscopy for characterizing different virus strains Hermann, Peter; Hermelink, Antje; Lausch, Veronika The Analyst, Vol. 136, Issue 6 https://doi.org/10.1039/c0an00531b	journal	January 2011
Deciphering single cell metabolism by coherent Raman scattering microscopy Yue, Shuhua; Cheng, Ji-Xin Current Opinion in Chemical Biology, Vol. 33 https://doi.org/10.1016/j.cbpa.2016.05.016	journal	August 2016
Open-Channel Microfluidic Membrane Device for Long-Term FT-IR Spectromicroscopy of Live Adherent Cells Loutherback, Kevin; Chen, Liang; Holman, Hoi-Ying N. Analytical Chemistry, Vol. 87, Issue 9 https://doi.org/10.1021/acs.analchem.5b00524	journal	April 2015
Quantitative CARS Molecular Fingerprinting of Single Living Cells with the Use of the Maximum Entropy Method Okuno, Masanari; Kano, Hideaki; Leproux, Philippe Angewandte Chemie International Edition, Vol. 49, Issue 38 https://doi.org/10.1002/anie.201001560	journal	August 2010
Modeling Microbial Dynamics in Heterogeneous Environments: Growth on Soil Carbon Sources Resat, Haluk; Bailey, Vanessa; McCue, Lee Ann Microbial Ecology, Vol. 63, Issue 4 https://doi.org/10.1007/s00248-011-9965-x	journal	December 2011
Characterization and analysis of mycobacteria and Gram-negative bacteria and co-culture mixtures by Raman microspectroscopy, FTIR, and atomic force microscopy Tang, Mingjie; McEwen, Gerald D.; Wu, Yangzhe Analytical and Bioanalytical Chemistry, Vol. 405, Issue 5 https://doi.org/10.1007/s00216-012-6556-8	journal	November 2012
Molecular imaging with CARS micro-spectroscopy Cicerone, Marcus Current Opinion in Chemical Biology, Vol. 33 https://doi.org/10.1016/j.cbpa.2016.05.010	journal	August 2016
Rapid biodiagnostic ex vivo imaging at 1 μm pixel resolution with thermal source FTIR FPA Findlay, C. R.; Wiens, R.; Rak, M. The Analyst, Vol. 140, Issue 7 https://doi.org/10.1039/c4an01982b	journal	January 2015
Development of Visible-Wavelength MALDI Cell Mass Spectrometry for High-Efficiency Single-Cell Analysis Xiong, Caiqiao; Zhou, Xiaoyu; He, Qing Analytical Chemistry, Vol. 88, Issue 23 https://doi.org/10.1021/acs.analchem.6b03789	journal	November 2016
Shining Light on the Microbial World Huang, Wei E.; Li, Mengqiu; Jarvis, Roger M. Advances in Applied Microbiology https://doi.org/10.1016/S0065-2164(10)70005-8	book	January 2010
Reagentless Identification of Single Bacterial Spores in Aqueous Solution by Confocal Laser Tweezers Raman Spectroscopy Chan, J. W.; Esposito, A. P.; Talley, C. E. Analytical Chemistry, Vol. 76, Issue 3 https://doi.org/10.1021/ac0350155	journal	February 2004
Challenges in imaging and predictive modeling of rhizosphere processes Roose, T.; Keyes, S. D.; Daly, K. R. Plant and Soil, Vol. 407, Issue 1-2 https://doi.org/10.1007/s11104-016-2872-7	journal	April 2016
Hyperspectral infrared nanoimaging of organic samples based on Fourier transform infrared nanospectroscopy Amenabar, Iban; Poly, Simon; Goikoetxea, Monika Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms14402	journal	February 2017
Analysis of Bacteria on Steel Surfaces Using Reflectance Micro-Fourier Transform Infrared Spectroscopy Ojeda, Jesús J.; Romero-González, María E.; Banwart, Steven A. Analytical Chemistry, Vol. 81, Issue 15 https://doi.org/10.1021/ac900841c	journal	August 2009
Deeper Understanding of Biological Tissue: Quantitative Correlation of MALDI-TOF and Raman Imaging Bocklitz, T. W.; Crecelius, A. C.; Matthäus, C. Analytical Chemistry, Vol. 85, Issue 22 https://doi.org/10.1021/ac402175c	journal	October 2013
Advancements in quantum cascade laser-based infrared microscopy of aqueous media Haase, K.; Kröger-Lui, N.; Pucci, A. Faraday Discussions, Vol. 187 https://doi.org/10.1039/c5fd00177c	journal	January 2016
Rapid analysis of two food-borne microbial communities at the species level by Fourier-transform infrared microspectroscopy Wenning, Mareike; Theilmann, Vera; Scherer, Siegfried Environmental Microbiology, Vol. 8, Issue 5 https://doi.org/10.1111/j.1462-2920.2005.00971.x	journal	May 2006
Studying Bacterial Metabolic States Using Raman Spectroscopy Escoriza, Maria Fernanda; Vanbriesen, Jeanne M.; Stewart, Shona Applied Spectroscopy, Vol. 60, Issue 9 https://doi.org/10.1366/000370206778397290	journal	September 2006
Single-Cell Ecophysiology of Microbes as Revealed by Raman Microspectroscopy or Secondary Ion Mass Spectrometry Imaging Wagner, Michael Annual Review of Microbiology, Vol. 63, Issue 1 https://doi.org/10.1146/annurev.micro.091208.073233	journal	October 2009
Modern Raman Imaging: Vibrational Spectroscopy on the Micrometer and Nanometer Scales Opilik, Lothar; Schmid, Thomas; Zenobi, Renato Annual Review of Analytical Chemistry, Vol. 6, Issue 1 https://doi.org/10.1146/annurev-anchem-062012-092646	journal	June 2013
A manual and an automatic TERS based virus discrimination Olschewski, Konstanze; Kämmer, Evelyn; Stöckel, Stephan Nanoscale, Vol. 7, Issue 10 https://doi.org/10.1039/c4nr07033j	journal	January 2015
Infrared Imaging and Spectroscopy Beyond the Diffraction Limit Centrone, Andrea Annual Review of Analytical Chemistry, Vol. 8, Issue 1 https://doi.org/10.1146/annurev-anchem-071114-040435	journal	July 2015
Direct analysis of clinical relevant single bacterial cells from cerebrospinal fluid during bacterial meningitis by means of micro-Raman spectroscopy Harz, Michaela; Kiehntopf, Michael; Stöckel, Stephan Journal of Biophotonics, Vol. 2, Issue 1-2 https://doi.org/10.1002/jbio.200810068	journal	February 2009
Microfluidics and Raman microscopy: current applications and future challenges Chrimes, Adam F.; Khoshmanesh, Khashayar; Stoddart, Paul R. Chemical Society Reviews, Vol. 42, Issue 13 https://doi.org/10.1039/c3cs35515b	journal	January 2013
Chemically sensitive bioimaging with coherent Raman scattering Camp Jr, Charles H.; Cicerone, Marcus T. Nature Photonics, Vol. 9, Issue 5 https://doi.org/10.1038/nphoton.2015.60	journal	April 2015
Fourier Transform Infrared Spectroscopy for Molecular Analysis of Microbial Cells Ojeda, Jesús J.; Dittrich, Maria Microbial Systems Biology https://doi.org/10.1007/978-1-61779-827-6_8	book	January 2012
Domain-level identification and quantification of relative prokaryotic cell abundance in microbial communities by Micro-FTIR spectroscopy: Domain-level diagnosis of prokaryotes by micro-FTIR Igisu, Motoko; Takai, Ken; Ueno, Yuichiro Environmental Microbiology Reports, Vol. 4, Issue 1 https://doi.org/10.1111/j.1758-2229.2011.00277.x	journal	August 2011
Nanoscale Chemical Imaging of Bacillus subtilis Spores by Combining Tip-Enhanced Raman Scattering and Advanced Statistical Tools Rusciano, Giulia; Zito, Gianluigi; Isticato, Rachele ACS Nano, Vol. 8, Issue 12 https://doi.org/10.1021/nn504595k	journal	November 2014
Investigating microbial micro-habitat structure using X-ray computed tomography Nunan, Naoise; Ritz, Karl; Rivers, Mark Geoderma, Vol. 133, Issue 3-4 https://doi.org/10.1016/j.geoderma.2005.08.004	journal	August 2006
Live-Cell Bioorthogonal Chemical Imaging: Stimulated Raman Scattering Microscopy of Vibrational Probes Wei, Lu; Hu, Fanghao; Chen, Zhixing Accounts of Chemical Research, Vol. 49, Issue 8 https://doi.org/10.1021/acs.accounts.6b00210	journal	August 2016
Rapid resonance Raman microspectroscopy to probe carbon dioxide fixation by single cells in microbial communities Li, Mengqiu; Canniffe, Daniel P.; Jackson, Philip J. The ISME Journal, Vol. 6, Issue 4 https://doi.org/10.1038/ismej.2011.150	journal	November 2011
Tracking heavy water (D ₂ O) incorporation for identifying and sorting active microbial cells Berry, David; Mader, Esther; Lee, Tae Kwon Proceedings of the National Academy of Sciences, Vol. 112, Issue 2 https://doi.org/10.1073/pnas.1420406112	journal	December 2014
Label-Free Imaging and Spectroscopic Analysis of Intracellular Bacterial Infections Große, Christina; Bergner, Norbert; Dellith, Jan Analytical Chemistry, Vol. 87, Issue 4 https://doi.org/10.1021/ac503316s	journal	January 2015
Applications of modern micro-Raman spectroscopy for cell analyses Mariani, Melissa M.; Day, Philip J. R.; Deckert, Volker Integrative Biology, Vol. 2, Issue 2-3 https://doi.org/10.1039/b920572a	journal	January 2010
Privatization of cooperative benefits stabilizes mutualistic cross-feeding interactions in spatially structured environments Pande, Samay; Kaftan, Filip; Lang, Stefan The ISME Journal, Vol. 10, Issue 6 https://doi.org/10.1038/ismej.2015.212	journal	December 2015
Single-cell genomics based on Raman sorting reveals novel carotenoid-containing bacteria in the Red Sea Song, Yizhi; Kaster, Anne-Kristin; Vollmers, John Microbial Biotechnology, Vol. 10, Issue 1 https://doi.org/10.1111/1751-7915.12420	journal	October 2016
Micro-scale determinants of bacterial diversity in soil Vos, Michiel; Wolf, Alexandra B.; Jennings, Sarah J. FEMS Microbiology Reviews, Vol. 37, Issue 6 https://doi.org/10.1111/1574-6976.12023	journal	November 2013
Raman and CARS microspectroscopy of cells and tissues Krafft, Christoph; Dietzek, Benjamin; Popp, Jürgen The Analyst, Vol. 134, Issue 6 https://doi.org/10.1039/b822354h	journal	January 2009
High-Definition Infrared Spectroscopic Imaging Reddy, Rohith K.; Walsh, Michael J.; Schulmerich, Matthew V. Applied Spectroscopy, Vol. 67, Issue 1 https://doi.org/10.1366/11-06568	journal	January 2013
Chemical Imaging of Live Cancer Cells in the Natural Aqueous Environment Kuimova, Marina K.; Chan, K. L. Andrew; Kazarian, Sergei G. Applied Spectroscopy, Vol. 63, Issue 2 https://doi.org/10.1366/000370209787391969	journal	February 2009
Multimodal Spectroscopy Combining Time-of-Flight-Secondary Ion Mass Spectrometry, Synchrotron-FT-IR, and Synchrotron-UV Microspectroscopies on the Same Tissue Section Petit, Vanessa W.; Réfrégiers, Matthieu; Guettier, Catherine Analytical Chemistry, Vol. 82, Issue 9 https://doi.org/10.1021/ac100581y	journal	May 2010
Single Cell Synchrotron FT-IR Microspectroscopy Reveals a Link between Neutral Lipid and Storage Carbohydrate Fluxes in S. cerevisiae Jamme, Frédéric; Vindigni, Jean-David; Méchin, Valérie PLoS ONE, Vol. 8, Issue 9 https://doi.org/10.1371/journal.pone.0074421	journal	September 2013
MALDI-TOF mass spectrometry: an emerging technology for microbial identification and diagnosis Singhal, Neelja; Kumar, Manish; Kanaujia, Pawan K. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00791	journal	August 2015
Developing X-ray Computed Tomography to non-invasively image 3-D root systems architecture in soil Mooney, S. J.; Pridmore, T. P.; Helliwell, J. Plant and Soil, Vol. 352, Issue 1-2 https://doi.org/10.1007/s11104-011-1039-9	journal	November 2011
Profiling the metabolic signals involved in chemical communication between microbes using imaging mass spectrometry Stasulli, Nikolas M.; Shank, Elizabeth A. FEMS Microbiology Reviews, Vol. 40, Issue 6 https://doi.org/10.1093/femsre/fuw032	journal	September 2016
In situ Detection of a Single Bacterium in Complex Environment by Hyperspectral CARS Imaging Hong, Weili; Liao, Chien-Sheng; Zhao, Hansen ChemistrySelect, Vol. 1, Issue 3 https://doi.org/10.1002/slct.201600166	journal	March 2016
Shedding light on host niches: label-free in situ detection of M ycobacterium gordonae via carotenoids in macrophages by Raman microspectroscopy: Label-free in situ detection of intracellular M. gordonae Silge, Anja; Abdou, Elias; Schneider, Kilian Cellular Microbiology, Vol. 17, Issue 6 https://doi.org/10.1111/cmi.12404	journal	January 2015
Raman Chemical Imaging Spectroscopy Reagentless Detection and Identification of Pathogens: Signature Development and Evaluation Kalasinsky, Kathryn S.; Hadfield, Ted; Shea, April A. Analytical Chemistry, Vol. 79, Issue 7 https://doi.org/10.1021/ac0700575	journal	April 2007
Profiling the metabolic signals involved in chemical communication between microbes using imaging mass spectrometry M., Stasulli, Nikolas; A., Shank, Elizabeth The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/2qbd-g722	text	January 2016
Single-cell bacterial transcription measurements reveal the importance of dimethylsulfoniopropionate (DMSP) hotspots in ocean sulfur cycling Gao, Cherry; Fernandez, Vicente I.; Lee, Kang S. ETH Zurich https://doi.org/10.3929/ethz-b-000412734	text	January 2020
Quantitative CARS Molecular Fingerprinting of Single Living Cells with the Use of the Maximum Entropy Method Okuno, Masanari; Kano, Hideaki; Leproux, Philippe Angewandte Chemie, Vol. 122, Issue 38 https://doi.org/10.1002/ange.201001560	journal	August 2010
Disseminated coccidioidomycosis in immunocompetent patients in non-endemic areas: a case series and literature review Guo, Xiaoxiao; Ruan, Qiaoling; Jin, Jialin European Journal of Clinical Microbiology & Infectious Diseases, Vol. 41, Issue 6 https://doi.org/10.1007/s10096-022-04447-y	journal	May 2022
Rapid discrimination of Enterococcus faecium strains using phenotypic analytical techniques AlMasoud, Najla; Xu, Yun; Ellis, David I. Analytical Methods, Vol. 8, Issue 42 https://doi.org/10.1039/c6ay02326f	journal	January 2016

Cited By (6)

Analysis of basidiomycete pigments in situ by Raman spectroscopy Tauber, James P.; Matthäus, Christian; Lenz, Claudius Journal of Biophotonics, Vol. 11, Issue 6 https://doi.org/10.1002/jbio.201700369	journal	March 2018
Isolation of intact bacteria from blood by selective cell lysis in a microfluidic porous silica monolith Han, Jung Y.; Wiederoder, Michael; DeVoe, Don L. Microsystems & Nanoengineering, Vol. 5, Issue 1 https://doi.org/10.1038/s41378-019-0063-4	journal	June 2019
Next-generation physiology approaches to study microbiome function at single cell level Hatzenpichler, Roland; Krukenberg, Viola; Spietz, Rachel L. Nature Reviews Microbiology, Vol. 18, Issue 4 https://doi.org/10.1038/s41579-020-0323-1	journal	February 2020
Surface-Enhanced Raman Scattering (SERS) in Microbiology: Illumination and Enhancement of the Microbial World Chisanga, Malama; Muhamadali, Howbeer; Ellis, David I. Applied Spectroscopy, Vol. 72, Issue 7 https://doi.org/10.1177/0003702818764672	journal	March 2018
Fourier-Transform Infrared Imaging Spectroscopy and Laser Ablation -ICPMS New Vistas for Biochemical Analyses of Ischemic Stroke in Rat Brain Ali, Mohamed H. M.; Rakib, Fazle; Abdelalim, Essam M. Frontiers in Neuroscience, Vol. 12 https://doi.org/10.3389/fnins.2018.00647	journal	September 2018
Stable-Isotope Probing of Human and Animal Microbiome Function Berry, David; Loy, Alexander Trends in Microbiology, Vol. 26, Issue 12 https://doi.org/10.1016/j.tim.2018.06.004	journal	December 2018

Similar Records

Proteogenomic Approaches for the Molecular Characterization of Natural Microbial Communities

Journal Article · Sat Jan 01 00:00:00 EST 2005 · OMICS: A Journal of Integrative Biology · OSTI ID:1367190

Banfield, Jillian F.; Verberkmoes, Nathan C; Thelen, Michael P.

Inhomogeneity of Cellulose Microfibril Assembly in Plant Cell Walls Revealed with Sum Frequency Generation Microscopy

Journal Article · Thu Apr 26 00:00:00 EDT 2018 · Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry · OSTI ID:1367190

Huang, Shixin; Makarem, Mohamadamin; Kiemle, Sarah N.; +4 more

Nonlinear vibrational microscopy

Patent · Sat Jan 01 00:00:00 EST 2000 · OSTI ID:1367190

Holtom, Gary R; Xie, Xiaoliang Sunney; Zumbusch, Andreas

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
imaging
isotope labeling
single-cell analysis
vibrational spectroscopy

Title: Vibrational spectroscopy for imaging single microbial cells in complex biological samples

Citation Formats

References (70)

Cited By (6)

Similar Records

Related Subjects