skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

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

Journal Article · · Scientific Reports
DOI:https://doi.org/10.1038/srep41798· OSTI ID:1343413
 [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)

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.

Research Organization:
Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES); U.S. Department of Agriculture (USDA); FAPESP Foundation
Grant/Contract Number:
AC02-06CH11357
OSTI ID:
1343413
Journal Information:
Scientific Reports, Vol. 7; ISSN 2045-2322
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 28 works
Citation information provided by
Web of Science

References (39)

White rot and manganese deposition in TnBTO-AAC preservative treated pine stakes from field tests journal March 1997
X-ray fluorescence microprobe imaging in biology and medicine journal January 2006
Changes in cation concentrations in red spruce wood decayed by brown rot and white rot fungi journal January 1997
Trends in environmental science using microscopic X-ray fluorescence journal August 2011
TomoPy: A framework for the analysis of synchrotron tomographic data conference September 2014
Protection of Wood-Based Materials book January 2012
Carbon sequestration in forest ecosystems journal August 2010
Oxalate regulation by two brown rot fungi decaying oxalate-amended and non-amended wood journal November 2005
Wood Decay Fungi Restore Essential Calcium to Acidic Soils in Northern New England journal July 2015
The role of cations in the biodegradation of wood by the brown rot fungi journal January 1997
Quantifying Trace Elements in Individual Aquatic Protist Cells with a Synchrotron X-ray Fluorescence Microprobe journal August 2003
De Novo Synthesis of 4,5-Dimethoxycatechol and 2,5-Dimethoxyhydroquinone by the Brown Rot FungusGloeophyllum trabeum journal February 1999
Fungal sporocarp mediated losses of Ca, Fe, K, Mg, Mn, N, P, and Zn from conifer logs in the early stages of decomposition journal September 1994
Synchrotron-based X-ray Fluorescence Microscopy in Conjunction with Nanoindentation to Study Molecular-Scale Interactions of Phenol–Formaldehyde in Wood Cell Walls journal March 2015
Iron and fungal pathogenesis: a case study with Cryptococcus neoformans: Iron and cryptococcosi journal October 2007
The Plant Cell Wall-Decomposing Machinery Underlies the Functional Diversity of Forest Fungi journal July 2011
Manganese Accumulation in Wood Decayed by White Rot Fungi journal January 1984
Mechanisms of iron acquisition from siderophores by microorganisms and plants journal January 1991
Low molecular weight chelators and phenolic compounds isolated from wood decay fungi and their role in the fungal biodegradation of wood1This is paper 2084 of the Maine Agricultural and Forest Experiment Station.1 journal March 1997
Carbon Sequestration in Forest Ecosystems book January 2010
Protection of Wood-Based Materials book January 2018
Peculiarities of brown-rot fungi and biochemical Fenton reaction with regard to their potential as a model for bioprocessing biomass journal March 2012
Fungal accumulation of metals from building materials during brown rot wood decay journal May 2014
TomoPy: a framework for the analysis of synchrotron tomographic data journal August 2014
Nondestructive elemental analysis of wood biodeterioration using electron paramagnetic resonance and synchrotron X-ray fluorescence journal January 1997
A new workflow for x-ray fluorescence tomography: MAPStoTomoPy conference September 2015
Changes in cation concentrations in red spruce wood decayed by brown rot and white rot fungi journal April 1997
Lignocellulose degradation mechanisms across the Tree of Life journal December 2015
Quantitative, chemically specific imaging of selenium transformation in plants journal September 2000
Brown rot fungal early stage decay mechanism as a biological pretreatment for softwood biomass in biofuel production journal August 2010
Extraction and translocation of calcium from gypsum during wood biodegradation by oxalate-producing fungi journal July 2007
Mechanisms of iron acquisition from siderophores by microorganisms and plants book January 1991
Iron Nutrition in Plants and Rhizospheric Microorganisms book January 2006
Variation in iron, aluminum and dissolved organic carbon mass transfer coefficients in lakes journal April 2003
Effects of minor elements on the physiology of fungi journal March 1949
Threshold for ion movements in wood cell walls below fiber saturation observed by X-ray fluorescence microscopy (XFM) journal May 2015
X-ray Imaging and Microspectroscopy of Plants and Fungi journal November 1998
Wood decomposition, higher fungi, and their role in nutrient redistribution journal December 1995
Spatial Distribution of Lignin- and Manganese II Peroxidase(S) During Degradation of Wood and Wood Fragments by Phanerochaete Chrysosporium as Revealed by T.E.M. Immunogold Labelling book January 1990

Cited By (5)

Changes in sorption and electrical properties of wood caused by fungal decay journal May 2019
Surface properties and crystallinity of Pinus taeda and Hymenaea stilbocarpa treated at low temperatures in different grain directions journal January 2020
Resistance of in natura and torrefied wood chips to xylophage fungi journal July 2019
Emerging chemical tools and techniques for tracking biological manganese journal January 2019
The Importance of Moisture for Brown Rot Degradation of Modified Wood: A Critical Discussion journal June 2019