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Download Hi-Res ImageDownload to MS-PowerPointCite This:Anal. Chem. 2019, 91, 19, 12501-12508
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Inhomogeneous Molecular Distributions and Cytochrome Types and Redox States in Fungal Cells Revealed by Raman Hyperspectral Imaging Using Multivariate Curve Resolution–Alternating Least Squares

  • Mitsuru Yasuda
    Mitsuru Yasuda
    Department of Chemistry, School of Science and Technology, Kwansei Gakuin University, Sanda, Hyogo 669-1337, Japan
    More by Mitsuru Yasuda
    • , 
  • Norio Takeshita
    Norio Takeshita
    Microbiology Research Center for Sustainability (MiCS), Faculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8572, Japan
    More by Norio Takeshita
    • , and 
  • Shinsuke Shigeto*
    Shinsuke Shigeto
    Department of Chemistry, School of Science and Technology, Kwansei Gakuin University, Sanda, Hyogo 669-1337, Japan
    *E-mail: [email protected]
    More by Shinsuke Shigeto
    Orcidhttp://orcid.org/0000-0002-2035-2068
Cite this: Anal. Chem. 2019, 91, 19, 12501–12508
Publication Date (Web):September 4, 2019
https://doi.org/10.1021/acs.analchem.9b03261
Copyright © 2019 American Chemical Society
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Abstract

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Hyphae of filamentous fungi consist of compartments that are distinct both spatially and functionally, thereby forming a unique multicellular system. Much work has been done mainly using fluorescence imaging to reveal what biomolecules are present in those different hyphal sections and what physiological roles they play. Nevertheless, a holistic understanding of hyphal functions including the polarized growth of hyphae is still lacking because of the difficulty in simultaneous acquisition of spatial and chemical information on various molecular components in living hyphae. Here, we used a multivariate curve resolution–alternating least-squares (MCR–ALS) analysis of Raman hyperspectral imaging data to study in vivo the spatial distributions and chemical properties of major cellular components in the tip, basal, and branching regions of the model fungus Aspergillus nidulans. The MCR–ALS Raman imaging method visualized, without any labeling, the characteristic distributions of cytochromes as well as other components including polysaccharides, noncytochrome proteins, nucleic acids, lipids, and ergosterol in the hyphal regions studied. Furthermore, the intrinsic Raman spectra derived for the first time from the MCR–ALS analysis enabled us to gain otherwise unobtainable chemical insights into those visualized components. We show variations in the relative abundance of cytochromes b and c and in their redox states (reduced vs oxidized form) among the three different representative compartments of A. nidulans hyphae, which could potentially be associated with specific physiological activities and functions of hyphae. The present results demonstrate that our MCR–ALS Raman imaging can serve as a useful tool complementary to the conventional approaches, for elucidating the diverse roles of filamentous fungi at the molecular level.

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The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.analchem.9b03261.

  • Description and result of SVD-ADC (Figure S1); optical micrograph and space-resolved Raman spectra of a damaged hypha (Figure S2); medium spectra (Figure S3); fluorescence image of A. nidulans hyphae with GFP-labeled nuclei (Figure S4); cytochrome spectrum with the combination-band range being enlarged (Figure S5); fluorescence image of an A. nidulans hypha with mitochondria labeled with GFP and nuclei labeled with mRFP (Figure S6); Raman images of the C–H stretching band and the 748 cm–1 band of cytochromes, and that of their ratio (Figure S7); assignments of representative Raman bands (Table S1); and band areas and their ratios obtained from the fitting analysis (Table S2) (PDF)

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Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

Cited By

This article is cited by 5 publications.

  1. Mitsuru Yasuda, Norio Takeshita, Shinsuke Shigeto. Deuterium-labeled Raman tracking of glucose accumulation and protein metabolic dynamics in Aspergillus nidulans hyphal tips. Scientific Reports 2021, 11 (1) https://doi.org/10.1038/s41598-020-80270-9
  2. Mirko Maturi, Paolo Armanetti, Luca Menichetti, Mauro Comes Franchini. An Application of Multivariate Data Analysis to Photoacoustic Imaging for the Spectral Unmixing of Gold Nanorods in Biological Tissues. Nanomaterials 2021, 11 (1) , 142. https://doi.org/10.3390/nano11010142
  3. Hiroto Horiue, Mai Sasaki, Yuki Yoshikawa, Masanori Toyofuku, Shinsuke Shigeto. Raman spectroscopic signatures of carotenoids and polyenes enable label-free visualization of microbial distributions within pink biofilms. Scientific Reports 2020, 10 (1) https://doi.org/10.1038/s41598-020-64737-3
  4. Takayuki Hiraoka, Shinsuke Shigeto. Interactions of water confined in a metal–organic framework as studied by a combined approach of Raman, FTIR, and IR electroabsorption spectroscopies and multivariate curve resolution analysis. Physical Chemistry Chemical Physics 2020, 22 (32) , 17798-17806. https://doi.org/10.1039/D0CP02958K
  5. Alexey V. Vlasov, Nina L. Maliar, Sergey V. Bazhenov, Evelina I. Nikelshparg, Nadezda A. Brazhe, Anastasiia D. Vlasova, Stepan D. Osipov, Vsevolod V. Sudarev, Yury L. Ryzhykau, Andrey O. Bogorodskiy, Egor V. Zinovev, Andrey V. Rogachev, Ilya V. Manukhov, Valentin I. Borshchevskiy, Alexander I. Kuklin, Jan Pokorný, Olga Sosnovtseva, Georgy V. Maksimov, Valentin I. Gordeliy. Raman Scattering: From Structural Biology to Medical Applications. Crystals 2020, 10 (1) , 38. https://doi.org/10.3390/cryst10010038

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