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Title: Synchrotron-based X-ray fluorescence microscopy enables multiscale spatial visualization of ions involved in fungal lignocellulose deconstruction

Ions play an important role in the growth and development of filamentous fungi, particularly in the fungal decay process of lignocellulose materials. The role of ions in wood degradation, and more broadly fungal metabolism, have implications for diverse research disciplines ranging from plant pathology and forest ecology, to wood protection. Despite the importance of ions in both enzymatic and non-enzymatic fungal decay mechanisms, the spatial distribution of ions in wood and fungal hyphae during decay is not known. Here we employ synchrotron based X-ray fluorescence microscopy (XFM) to map physiologically relevant ions, such as K, Ca, Mn, Fe, and Zn, in wood being decayed by the model brown rot fungus Serpula lacrymans. Two-dimensional XFM maps were obtained to study the ion spatial distributions from mm to submicron length scales in wood and hyphae. Three-dimensional ion volume reconstructions with submicron spatial resolution were also acquired of wood cell walls and fungal hyphae, and an estimation of oxalate concentration at the microscale was made. Results show that the fungus actively transports some ions, such as Fe, into the wood and controls the distribution of ions at both the bulk wood and cellular length scales. Within the fungal hyphae, ion volume reconstructions showmore » inhomogeneous ion distributions at the micron length scale and this localization may be indicative of both physiological status and requirements or in some cases, potentially sites associated with the initiation of metal-catalyzed wood degradation. Finally, these measurements illustrate how synchrotron based XFM is uniquely qualified for probing the role of ions in the growth and metabolic processes of filamentous fungi.« less
Authors:
 [1] ;  [1] ;  [2] ;  [2] ;  [2] ;  [2] ;  [3] ;  [4] ;  [2] ;  [5] ;  [5] ;  [1]
  1. USDA Forest Service, Madison, WI (United States)
  2. Argonne National Lab. (ANL), Argonne, IL (United States)
  3. Northwestern Univ., Evanston, IL (United States)
  4. Univ. de Sao Paulo (Brazil)
  5. Univ. of Massachusetts, Amherst, MA (United States)
Publication Date:
Grant/Contract Number:
AC02-06CH11357
Type:
Accepted Manuscript
Journal Name:
Scientific Reports
Additional Journal Information:
Journal Volume: 7; Journal ID: ISSN 2045-2322
Publisher:
Nature Publishing Group
Research Org:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); U.S. Department of Agriculture (USDA); FAPESP Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Brown rot fungi; X-ray fluorescence microscopy; tomography; wood decay
OSTI Identifier:
1343413

Kirker, Grant, Zelinka, Sam, Gleber, Sophie -Charlotte, Vine, David, Finney, Lydia, Chen, Si, Hong, Young Pyo, Uyarte, Omar, Vogt, Stefan, Jellison, Jody, Goodell, Barry, and Jakes, Joseph E. Synchrotron-based X-ray fluorescence microscopy enables multiscale spatial visualization of ions involved in fungal lignocellulose deconstruction. United States: N. p., Web. doi:10.1038/srep41798.
Kirker, Grant, Zelinka, Sam, Gleber, Sophie -Charlotte, Vine, David, Finney, Lydia, Chen, Si, Hong, Young Pyo, Uyarte, Omar, Vogt, Stefan, Jellison, Jody, Goodell, Barry, & Jakes, Joseph E. Synchrotron-based X-ray fluorescence microscopy enables multiscale spatial visualization of ions involved in fungal lignocellulose deconstruction. United States. doi:10.1038/srep41798.
Kirker, Grant, Zelinka, Sam, Gleber, Sophie -Charlotte, Vine, David, Finney, Lydia, Chen, Si, Hong, Young Pyo, Uyarte, Omar, Vogt, Stefan, Jellison, Jody, Goodell, Barry, and Jakes, Joseph E. 2017. "Synchrotron-based X-ray fluorescence microscopy enables multiscale spatial visualization of ions involved in fungal lignocellulose deconstruction". United States. doi:10.1038/srep41798. https://www.osti.gov/servlets/purl/1343413.
@article{osti_1343413,
title = {Synchrotron-based X-ray fluorescence microscopy enables multiscale spatial visualization of ions involved in fungal lignocellulose deconstruction},
author = {Kirker, Grant and Zelinka, Sam and Gleber, Sophie -Charlotte and Vine, David and Finney, Lydia and Chen, Si and Hong, Young Pyo and Uyarte, Omar and Vogt, Stefan and Jellison, Jody and Goodell, Barry and Jakes, Joseph E.},
abstractNote = {Ions play an important role in the growth and development of filamentous fungi, particularly in the fungal decay process of lignocellulose materials. The role of ions in wood degradation, and more broadly fungal metabolism, have implications for diverse research disciplines ranging from plant pathology and forest ecology, to wood protection. Despite the importance of ions in both enzymatic and non-enzymatic fungal decay mechanisms, the spatial distribution of ions in wood and fungal hyphae during decay is not known. Here we employ synchrotron based X-ray fluorescence microscopy (XFM) to map physiologically relevant ions, such as K, Ca, Mn, Fe, and Zn, in wood being decayed by the model brown rot fungus Serpula lacrymans. Two-dimensional XFM maps were obtained to study the ion spatial distributions from mm to submicron length scales in wood and hyphae. Three-dimensional ion volume reconstructions with submicron spatial resolution were also acquired of wood cell walls and fungal hyphae, and an estimation of oxalate concentration at the microscale was made. Results show that the fungus actively transports some ions, such as Fe, into the wood and controls the distribution of ions at both the bulk wood and cellular length scales. Within the fungal hyphae, ion volume reconstructions show inhomogeneous ion distributions at the micron length scale and this localization may be indicative of both physiological status and requirements or in some cases, potentially sites associated with the initiation of metal-catalyzed wood degradation. Finally, these measurements illustrate how synchrotron based XFM is uniquely qualified for probing the role of ions in the growth and metabolic processes of filamentous fungi.},
doi = {10.1038/srep41798},
journal = {Scientific Reports},
number = ,
volume = 7,
place = {United States},
year = {2017},
month = {1}
}