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Elucidating fungal decomposition of organic matter at sub-micrometer spatial scales using optical photothermal infrared (O-PTIR) microspectroscopy

De Beeck, Michiel Op LU orcid ; Troein, Carl LU orcid ; Peterson, Carsten LU ; Tunlid, Anders LU and Persson, Per LU (2024) In Applied and Environmental Microbiology 90(2).
Abstract

In microbiological studies, a common goal is to link environmental factors to microbial activities. Both environmental factors and microbial activities are typically derived from bulk samples. It is becoming increasingly clear that such bulk environmental parameters poorly represent the microscale environments microorganisms experience. Using infrared (IR) microspectroscopy, the spatial distribution of chemical compound classes can be visualized, making it a useful tool for studying the interactions between microbial cells and their microenvironments. The spatial resolution of conventional IR microspectroscopy has been limited by the diffractionlimit of IR light. The recent development of optical photothermal infrared (O-PTIR)... (More)

In microbiological studies, a common goal is to link environmental factors to microbial activities. Both environmental factors and microbial activities are typically derived from bulk samples. It is becoming increasingly clear that such bulk environmental parameters poorly represent the microscale environments microorganisms experience. Using infrared (IR) microspectroscopy, the spatial distribution of chemical compound classes can be visualized, making it a useful tool for studying the interactions between microbial cells and their microenvironments. The spatial resolution of conventional IR microspectroscopy has been limited by the diffractionlimit of IR light. The recent development of optical photothermal infrared (O-PTIR) microspectroscopy has pushed the spatial resolution of IR microspectroscopy beyond this diffractionlimit, allowing the distribution of chemical compound classes to be visualized at sub-micrometer spatial scales. To examine the potential and limitations of O-PTIR microspectroscopy to probe the interactions between fungal cells and their immediate environments, we imaged the decomposition of cellulose filmsby cells of the ectomycorrhizal fungus Paxillus involutus and compared O-PTIR results using conventional IR microspectroscopy. Whereas the data collected with conventional IR microspectroscopy indicated that P. involutus has only a very limited ability to decompose cellulose films,O-PTIR data suggested that the ability of P. involutus to decompose cellulose was substantial. Moreover, the O-PTIR method enabled the identificationof a zone located outside the fungal hyphae where the cellulose was decomposed by oxidation. We conclude that O-PTIR can provide valuable new insights into the abilities and mechanisms by which microorganisms interact with their surrounding environments.

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author
; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
cellulose, decomposition, infrared microspectroscopy, microenvironment, microorganism, organic matter
in
Applied and Environmental Microbiology
volume
90
issue
2
article number
e01489-23.
publisher
American Society for Microbiology
external identifiers
  • pmid:38289133
  • scopus:85185705956
ISSN
0099-2240
DOI
10.1128/aem.01489-23
language
English
LU publication?
yes
id
bfa53ffd-c6d9-4efa-a6b6-efdb1df6583f
date added to LUP
2024-03-26 16:03:49
date last changed
2024-04-23 19:59:09
@article{bfa53ffd-c6d9-4efa-a6b6-efdb1df6583f,
  abstract     = {{<p>In microbiological studies, a common goal is to link environmental factors to microbial activities. Both environmental factors and microbial activities are typically derived from bulk samples. It is becoming increasingly clear that such bulk environmental parameters poorly represent the microscale environments microorganisms experience. Using infrared (IR) microspectroscopy, the spatial distribution of chemical compound classes can be visualized, making it a useful tool for studying the interactions between microbial cells and their microenvironments. The spatial resolution of conventional IR microspectroscopy has been limited by the diffractionlimit of IR light. The recent development of optical photothermal infrared (O-PTIR) microspectroscopy has pushed the spatial resolution of IR microspectroscopy beyond this diffractionlimit, allowing the distribution of chemical compound classes to be visualized at sub-micrometer spatial scales. To examine the potential and limitations of O-PTIR microspectroscopy to probe the interactions between fungal cells and their immediate environments, we imaged the decomposition of cellulose filmsby cells of the ectomycorrhizal fungus Paxillus involutus and compared O-PTIR results using conventional IR microspectroscopy. Whereas the data collected with conventional IR microspectroscopy indicated that P. involutus has only a very limited ability to decompose cellulose films,O-PTIR data suggested that the ability of P. involutus to decompose cellulose was substantial. Moreover, the O-PTIR method enabled the identificationof a zone located outside the fungal hyphae where the cellulose was decomposed by oxidation. We conclude that O-PTIR can provide valuable new insights into the abilities and mechanisms by which microorganisms interact with their surrounding environments.</p>}},
  author       = {{De Beeck, Michiel Op and Troein, Carl and Peterson, Carsten and Tunlid, Anders and Persson, Per}},
  issn         = {{0099-2240}},
  keywords     = {{cellulose; decomposition; infrared microspectroscopy; microenvironment; microorganism; organic matter}},
  language     = {{eng}},
  number       = {{2}},
  publisher    = {{American Society for Microbiology}},
  series       = {{Applied and Environmental Microbiology}},
  title        = {{Elucidating fungal decomposition of organic matter at sub-micrometer spatial scales using optical photothermal infrared (O-PTIR) microspectroscopy}},
  url          = {{http://dx.doi.org/10.1128/aem.01489-23}},
  doi          = {{10.1128/aem.01489-23}},
  volume       = {{90}},
  year         = {{2024}},
}