Novel methods to characterise spatial distribution and enantiomeric composition of usnic acids in four Icelandic lichens

Maonian Xu; Ernest Oppong-Danquah; Xiaoyu Wang; Sebastian Oddsson; Asmaa Abdelrahman; Simon Vilms Pedersen; Maria Szomek; Aron Elvar Gylfason; Bergþóra Sigríður Snorradóttir; Eva Arnspang Christensen; Deniz Tasdemir; Cynthia J. Jameson; Sohail Murad; Ólafur Sigmar Andrésson; Kristinn Pétur Magnússon; Hugo J. de Boer; Margrét Þorsteinsdóttir; Sesselja Sigurborg Ómarsdóttir; Starri Heidmarsson; Elín Soffía Ólafsdóttir; Bergthora Sigridur Snorradottir; Margret Thorsteinsdottir

doi:10.1016/j.phytochem.2022.113210

Novel methods to characterise spatial distribution and enantiomeric composition of usnic acids in four Icelandic lichens

Maonian Xu^*, Ernest Oppong-Danquah, Xiaoyu Wang, Sebastian Oddsson, Asmaa Abdelrahman, Simon Vilms Pedersen, Maria Szomek, Aron Elvar Gylfason, Bergþóra Sigríður Snorradóttir, Eva Arnspang Christensen, Deniz Tasdemir, Cynthia J. Jameson, Sohail Murad, Ólafur Sigmar Andrésson, Kristinn Pétur Magnússon, Hugo J. de Boer, Margrét Þorsteinsdóttir, Sesselja Sigurborg Ómarsdóttir, Starri Heidmarsson, Elín Soffía ÓlafsdóttirBergthora Sigridur Snorradottir, Margret Thorsteinsdottir

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

Abstract

Usnic acid is an antibiotic metabolite produced by a wide variety of lichenized fungal lineages. The enantiomers of usnic acid have been shown to display contrasting bioactivities, and hence it is important to determine their spatial distribution, amounts and enantiomeric ratios in lichens to understand their roles in nature and grasp their pharmaceutical potential. The overall aim of the study was to characterise the spatial distribution of the predominant usnic acid enantiomer in lichens by combining spatial imaging and chiral chromatography. Specifically, separation and quantification of usnic acid enantiomers in four common lichens in Iceland was performed using a validated chiral chromatographic method. Molecular dynamics simulation was carried out to rationalize the chiral separation mechanism. Spatial distribution of usnic acid in the lichen thallus cross-sections were analysed using Desorption Electrospray Ionization-Imaging Mass Spectrometry (DESI-IMS) and fluorescence microscopy. DESI-IMS confirmed usnic acid as a cortical compound, and revealed that usnic acid can be more concentrated around the algal vicinity. Fluorescence microscopy complemented DESI-IMS by providing more detailed distribution information. By combining results from spatial imaging and chiral separation, we were able to visualize the distribution of the predominant usnic acid enantiomer in lichen cross-sections: (+)-usnic acid in Cladonia arbuscula and Ramalina siliquosa, and (−)-usnic acid in Alectoria ochroleuca and Flavocetraria nivalis. This study provides an analytical foundation for future environmental and functional studies of usnic acid enantiomers in lichens.

Original language	English
Article number	113210
Number of pages	11
Journal	Phytochemistry
Volume	200
DOIs	https://doi.org/10.1016/j.phytochem.2022.113210
Publication status	Published - Aug 2022

Bibliographical note

Funding Information:
The work was supported by the European Union's Seventh Framework Programme for research, technological development and demonstration to FP7-MCA-ITN MedPlant [grant number 606895 ]; and the Icelandic Research Fund [grant number 185442051 ] and the Bergthora and Thorsteinn Scheving Thorsteinsson Fund . We thank Mr. Arni Kristjansson for technical assistance and instrumental maintenance. The screening support of Dr. Aidan Harrison was of considerable help. We also acknowledge the central microscopy facility of Kiel University for support and access to their cryostat microtome (CM3050 S cryostat, Leica, Wetzlar, Germany) for sectioning lichens used for DESI-IMS analysis. X.W., S.M. and C.J.J. acknowledge support from the Eppley Foundation . We thank Dr. Steffen Madsen (Department of Biology, University of Southern Denmark) for kind access to cryotome facilities. The authors thank the Danish Molecular Biomedical Imaging Center (DaMBIC, University of Southern Denmark) for access to fluorescence microscopy facilities, supported by the Novo Nordisk Foundation (NNF) (grant agreement number NNF18SA0032928 ).

Funding Information:
The work was supported by the European Union's Seventh Framework Programme for research, technological development and demonstration to FP7-MCA-ITN MedPlant [grant number 606895]; and the Icelandic Research Fund [grant number 185442051] and the Bergthora and Thorsteinn Scheving Thorsteinsson Fund. We thank Mr. Arni Kristjansson for technical assistance and instrumental maintenance. The screening support of Dr. Aidan Harrison was of considerable help. We also acknowledge the central microscopy facility of Kiel University for support and access to their cryostat microtome (CM3050 S cryostat, Leica, Wetzlar, Germany) for sectioning lichens used for DESI-IMS analysis. X.W. S.M. and C.J.J. acknowledge support from the Eppley Foundation. We thank Dr. Steffen Madsen (Department of Biology, University of Southern Denmark) for kind access to cryotome facilities. The authors thank the Danish Molecular Biomedical Imaging Center (DaMBIC, University of Southern Denmark) for access to fluorescence microscopy facilities, supported by the Novo Nordisk Foundation (NNF) (grant agreement number NNF18SA0032928).

Publisher Copyright:
© 2022 Elsevier Ltd

Other keywords

Alectoria ochroleuca
Cladonia arbuscula
Enantioseparation
Flavocetraria nivalis
Fluorescence microscopy
Imaging mass spectrometry
Molecular dynamics simulation
Parmeliaceae
Ramalina siliquosa
Usnic acid

Access to Document

10.1016/j.phytochem.2022.113210

Cite this

Xu, M., Oppong-Danquah, E., Wang, X., Oddsson, S., Abdelrahman, A., Pedersen, S. V., Szomek, M., Gylfason, A. E., Snorradóttir, B. S., Christensen, E. A., Tasdemir, D., Jameson, C. J., Murad, S., Andrésson, Ó. S., Magnússon, K. P., de Boer, H. J., Þorsteinsdóttir, M., Ómarsdóttir, S. S., Heidmarsson, S., ... Thorsteinsdottir, M. (2022). Novel methods to characterise spatial distribution and enantiomeric composition of usnic acids in four Icelandic lichens. Phytochemistry, 200, Article 113210. https://doi.org/10.1016/j.phytochem.2022.113210

@article{c3ea9484319f4f078459e072c960f698,

title = "Novel methods to characterise spatial distribution and enantiomeric composition of usnic acids in four Icelandic lichens",

abstract = "Usnic acid is an antibiotic metabolite produced by a wide variety of lichenized fungal lineages. The enantiomers of usnic acid have been shown to display contrasting bioactivities, and hence it is important to determine their spatial distribution, amounts and enantiomeric ratios in lichens to understand their roles in nature and grasp their pharmaceutical potential. The overall aim of the study was to characterise the spatial distribution of the predominant usnic acid enantiomer in lichens by combining spatial imaging and chiral chromatography. Specifically, separation and quantification of usnic acid enantiomers in four common lichens in Iceland was performed using a validated chiral chromatographic method. Molecular dynamics simulation was carried out to rationalize the chiral separation mechanism. Spatial distribution of usnic acid in the lichen thallus cross-sections were analysed using Desorption Electrospray Ionization-Imaging Mass Spectrometry (DESI-IMS) and fluorescence microscopy. DESI-IMS confirmed usnic acid as a cortical compound, and revealed that usnic acid can be more concentrated around the algal vicinity. Fluorescence microscopy complemented DESI-IMS by providing more detailed distribution information. By combining results from spatial imaging and chiral separation, we were able to visualize the distribution of the predominant usnic acid enantiomer in lichen cross-sections: (+)-usnic acid in Cladonia arbuscula and Ramalina siliquosa, and (−)-usnic acid in Alectoria ochroleuca and Flavocetraria nivalis. This study provides an analytical foundation for future environmental and functional studies of usnic acid enantiomers in lichens.",

keywords = "Alectoria ochroleuca, Cladonia arbuscula, Enantioseparation, Flavocetraria nivalis, Fluorescence microscopy, Imaging mass spectrometry, Molecular dynamics simulation, Parmeliaceae, Ramalina siliquosa, Usnic acid",

author = "Maonian Xu and Ernest Oppong-Danquah and Xiaoyu Wang and Sebastian Oddsson and Asmaa Abdelrahman and Pedersen, {Simon Vilms} and Maria Szomek and Gylfason, {Aron Elvar} and Snorrad{\'o}ttir, {Berg{\th}{\'o}ra Sigr{\'i}{\dh}ur} and Christensen, {Eva Arnspang} and Deniz Tasdemir and Jameson, {Cynthia J.} and Sohail Murad and Andr{\'e}sson, {{\'O}lafur Sigmar} and Magn{\'u}sson, {Kristinn P{\'e}tur} and {de Boer}, {Hugo J.} and Margr{\'e}t {\TH}orsteinsd{\'o}ttir and {\'O}marsd{\'o}ttir, {Sesselja Sigurborg} and Starri Heidmarsson and {\'O}lafsd{\'o}ttir, {El{\'i}n Soff{\'i}a} and Snorradottir, {Bergthora Sigridur} and Margret Thorsteinsdottir",

note = "Funding Information: The work was supported by the European Union's Seventh Framework Programme for research, technological development and demonstration to FP7-MCA-ITN MedPlant [grant number 606895 ]; and the Icelandic Research Fund [grant number 185442051 ] and the Bergthora and Thorsteinn Scheving Thorsteinsson Fund . We thank Mr. Arni Kristjansson for technical assistance and instrumental maintenance. The screening support of Dr. Aidan Harrison was of considerable help. We also acknowledge the central microscopy facility of Kiel University for support and access to their cryostat microtome (CM3050 S cryostat, Leica, Wetzlar, Germany) for sectioning lichens used for DESI-IMS analysis. X.W., S.M. and C.J.J. acknowledge support from the Eppley Foundation . We thank Dr. Steffen Madsen (Department of Biology, University of Southern Denmark) for kind access to cryotome facilities. The authors thank the Danish Molecular Biomedical Imaging Center (DaMBIC, University of Southern Denmark) for access to fluorescence microscopy facilities, supported by the Novo Nordisk Foundation (NNF) (grant agreement number NNF18SA0032928 ). Funding Information: The work was supported by the European Union's Seventh Framework Programme for research, technological development and demonstration to FP7-MCA-ITN MedPlant [grant number 606895]; and the Icelandic Research Fund [grant number 185442051] and the Bergthora and Thorsteinn Scheving Thorsteinsson Fund. We thank Mr. Arni Kristjansson for technical assistance and instrumental maintenance. The screening support of Dr. Aidan Harrison was of considerable help. We also acknowledge the central microscopy facility of Kiel University for support and access to their cryostat microtome (CM3050 S cryostat, Leica, Wetzlar, Germany) for sectioning lichens used for DESI-IMS analysis. X.W. S.M. and C.J.J. acknowledge support from the Eppley Foundation. We thank Dr. Steffen Madsen (Department of Biology, University of Southern Denmark) for kind access to cryotome facilities. The authors thank the Danish Molecular Biomedical Imaging Center (DaMBIC, University of Southern Denmark) for access to fluorescence microscopy facilities, supported by the Novo Nordisk Foundation (NNF) (grant agreement number NNF18SA0032928). Publisher Copyright: {\textcopyright} 2022 Elsevier Ltd",

year = "2022",

month = aug,

doi = "10.1016/j.phytochem.2022.113210",

language = "English",

volume = "200",

journal = "Phytochemistry",

issn = "0031-9422",

publisher = "Elsevier Ltd.",

}

Xu, M, Oppong-Danquah, E, Wang, X, Oddsson, S, Abdelrahman, A, Pedersen, SV, Szomek, M, Gylfason, AE, Snorradóttir, BS, Christensen, EA, Tasdemir, D, Jameson, CJ, Murad, S, Andrésson, ÓS , Magnússon, KP, de Boer, HJ, Þorsteinsdóttir, M , Ómarsdóttir, SS, Heidmarsson, S, Ólafsdóttir, ES, Snorradottir, BS & Thorsteinsdottir, M 2022, 'Novel methods to characterise spatial distribution and enantiomeric composition of usnic acids in four Icelandic lichens', Phytochemistry, vol. 200, 113210. https://doi.org/10.1016/j.phytochem.2022.113210

TY - JOUR

T1 - Novel methods to characterise spatial distribution and enantiomeric composition of usnic acids in four Icelandic lichens

AU - Xu, Maonian

AU - Oppong-Danquah, Ernest

AU - Wang, Xiaoyu

AU - Oddsson, Sebastian

AU - Abdelrahman, Asmaa

AU - Pedersen, Simon Vilms

AU - Szomek, Maria

AU - Gylfason, Aron Elvar

AU - Snorradóttir, Bergþóra Sigríður

AU - Christensen, Eva Arnspang

AU - Tasdemir, Deniz

AU - Jameson, Cynthia J.

AU - Murad, Sohail

AU - Andrésson, Ólafur Sigmar

AU - Magnússon, Kristinn Pétur

AU - de Boer, Hugo J.

AU - Þorsteinsdóttir, Margrét

AU - Ómarsdóttir, Sesselja Sigurborg

AU - Heidmarsson, Starri

AU - Ólafsdóttir, Elín Soffía

AU - Snorradottir, Bergthora Sigridur

AU - Thorsteinsdottir, Margret

N1 - Funding Information: The work was supported by the European Union's Seventh Framework Programme for research, technological development and demonstration to FP7-MCA-ITN MedPlant [grant number 606895 ]; and the Icelandic Research Fund [grant number 185442051 ] and the Bergthora and Thorsteinn Scheving Thorsteinsson Fund . We thank Mr. Arni Kristjansson for technical assistance and instrumental maintenance. The screening support of Dr. Aidan Harrison was of considerable help. We also acknowledge the central microscopy facility of Kiel University for support and access to their cryostat microtome (CM3050 S cryostat, Leica, Wetzlar, Germany) for sectioning lichens used for DESI-IMS analysis. X.W., S.M. and C.J.J. acknowledge support from the Eppley Foundation . We thank Dr. Steffen Madsen (Department of Biology, University of Southern Denmark) for kind access to cryotome facilities. The authors thank the Danish Molecular Biomedical Imaging Center (DaMBIC, University of Southern Denmark) for access to fluorescence microscopy facilities, supported by the Novo Nordisk Foundation (NNF) (grant agreement number NNF18SA0032928 ). Funding Information: The work was supported by the European Union's Seventh Framework Programme for research, technological development and demonstration to FP7-MCA-ITN MedPlant [grant number 606895]; and the Icelandic Research Fund [grant number 185442051] and the Bergthora and Thorsteinn Scheving Thorsteinsson Fund. We thank Mr. Arni Kristjansson for technical assistance and instrumental maintenance. The screening support of Dr. Aidan Harrison was of considerable help. We also acknowledge the central microscopy facility of Kiel University for support and access to their cryostat microtome (CM3050 S cryostat, Leica, Wetzlar, Germany) for sectioning lichens used for DESI-IMS analysis. X.W. S.M. and C.J.J. acknowledge support from the Eppley Foundation. We thank Dr. Steffen Madsen (Department of Biology, University of Southern Denmark) for kind access to cryotome facilities. The authors thank the Danish Molecular Biomedical Imaging Center (DaMBIC, University of Southern Denmark) for access to fluorescence microscopy facilities, supported by the Novo Nordisk Foundation (NNF) (grant agreement number NNF18SA0032928). Publisher Copyright: © 2022 Elsevier Ltd

PY - 2022/8

Y1 - 2022/8

N2 - Usnic acid is an antibiotic metabolite produced by a wide variety of lichenized fungal lineages. The enantiomers of usnic acid have been shown to display contrasting bioactivities, and hence it is important to determine their spatial distribution, amounts and enantiomeric ratios in lichens to understand their roles in nature and grasp their pharmaceutical potential. The overall aim of the study was to characterise the spatial distribution of the predominant usnic acid enantiomer in lichens by combining spatial imaging and chiral chromatography. Specifically, separation and quantification of usnic acid enantiomers in four common lichens in Iceland was performed using a validated chiral chromatographic method. Molecular dynamics simulation was carried out to rationalize the chiral separation mechanism. Spatial distribution of usnic acid in the lichen thallus cross-sections were analysed using Desorption Electrospray Ionization-Imaging Mass Spectrometry (DESI-IMS) and fluorescence microscopy. DESI-IMS confirmed usnic acid as a cortical compound, and revealed that usnic acid can be more concentrated around the algal vicinity. Fluorescence microscopy complemented DESI-IMS by providing more detailed distribution information. By combining results from spatial imaging and chiral separation, we were able to visualize the distribution of the predominant usnic acid enantiomer in lichen cross-sections: (+)-usnic acid in Cladonia arbuscula and Ramalina siliquosa, and (−)-usnic acid in Alectoria ochroleuca and Flavocetraria nivalis. This study provides an analytical foundation for future environmental and functional studies of usnic acid enantiomers in lichens.

AB - Usnic acid is an antibiotic metabolite produced by a wide variety of lichenized fungal lineages. The enantiomers of usnic acid have been shown to display contrasting bioactivities, and hence it is important to determine their spatial distribution, amounts and enantiomeric ratios in lichens to understand their roles in nature and grasp their pharmaceutical potential. The overall aim of the study was to characterise the spatial distribution of the predominant usnic acid enantiomer in lichens by combining spatial imaging and chiral chromatography. Specifically, separation and quantification of usnic acid enantiomers in four common lichens in Iceland was performed using a validated chiral chromatographic method. Molecular dynamics simulation was carried out to rationalize the chiral separation mechanism. Spatial distribution of usnic acid in the lichen thallus cross-sections were analysed using Desorption Electrospray Ionization-Imaging Mass Spectrometry (DESI-IMS) and fluorescence microscopy. DESI-IMS confirmed usnic acid as a cortical compound, and revealed that usnic acid can be more concentrated around the algal vicinity. Fluorescence microscopy complemented DESI-IMS by providing more detailed distribution information. By combining results from spatial imaging and chiral separation, we were able to visualize the distribution of the predominant usnic acid enantiomer in lichen cross-sections: (+)-usnic acid in Cladonia arbuscula and Ramalina siliquosa, and (−)-usnic acid in Alectoria ochroleuca and Flavocetraria nivalis. This study provides an analytical foundation for future environmental and functional studies of usnic acid enantiomers in lichens.

KW - Alectoria ochroleuca

KW - Cladonia arbuscula

KW - Enantioseparation

KW - Flavocetraria nivalis

KW - Fluorescence microscopy

KW - Imaging mass spectrometry

KW - Molecular dynamics simulation

KW - Parmeliaceae

KW - Ramalina siliquosa

KW - Usnic acid

UR - http://www.scopus.com/inward/record.url?scp=85128460167&partnerID=8YFLogxK

UR - https://doi.org/10.1016/j.phytochem.2022.113210

U2 - 10.1016/j.phytochem.2022.113210

DO - 10.1016/j.phytochem.2022.113210

M3 - Article

AN - SCOPUS:85128460167

SN - 0031-9422

VL - 200

JO - Phytochemistry

JF - Phytochemistry

M1 - 113210

ER -

Novel methods to characterise spatial distribution and enantiomeric composition of usnic acids in four Icelandic lichens

Abstract

Bibliographical note

Other keywords

Access to Document

Fingerprint

Cite this