Large differences in carbohydrate degradation and transport potential among lichen fungal symbionts

Philipp Resl; Adina R. Bujold; Gulnara Tagirdzhanova; Peter Meidl; Sandra Freire Rallo; Mieko Kono; Samantha Fernández-Brime; Hörður Guðmundsson; Ólafur Sigmar Andrésson; Lucia Muggia; Helmut Mayrhofer; John P. McCutcheon; Mats Wedin; Silke Werth; Lisa M. Willis; Toby Spribille

doi:10.1038/s41467-022-30218-6

Large differences in carbohydrate degradation and transport potential among lichen fungal symbionts

Philipp Resl, Adina R. Bujold, Gulnara Tagirdzhanova, Peter Meidl, Sandra Freire Rallo, Mieko Kono, Samantha Fernández-Brime, Hörður Guðmundsson, Ólafur Sigmar Andrésson, Lucia Muggia, Helmut Mayrhofer, John P. McCutcheon, Mats Wedin, Silke Werth, Lisa M. Willis, Toby Spribille

Life Sciences, School of (SOLS)

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

15 Scopus citations

Abstract

Lichen symbioses are thought to be stabilized by the transfer of fixed carbon from a photosynthesizing symbiont to a fungus. In other fungal symbioses, carbohydrate subsidies correlate with reductions in plant cell wall-degrading enzymes, but whether this is true of lichen fungal symbionts (LFSs) is unknown. Here, we predict genes encoding carbohydrate-active enzymes (CAZymes) and sugar transporters in 46 genomes from the Lecanoromycetes, the largest extant clade of LFSs. All LFSs possess a robust CAZyme arsenal including enzymes acting on cellulose and hemicellulose, confirmed by experimental assays. However, the number of genes and predicted functions of CAZymes vary widely, with some fungal symbionts possessing arsenals on par with well-known saprotrophic fungi. These results suggest that stable fungal association with a phototroph does not in itself result in fungal CAZyme loss, and lends support to long-standing hypotheses that some lichens may augment fixed CO₂ with carbon from external sources.

Original language	English (US)
Article number	2634
Journal	Nature communications
Volume	13
Issue number	1
DOIs	https://doi.org/10.1038/s41467-022-30218-6
State	Published - Dec 2022

ASJC Scopus subject areas

Chemistry(all)
Biochemistry, Genetics and Molecular Biology(all)
General
Physics and Astronomy(all)

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10.1038/s41467-022-30218-6

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Resl, P., Bujold, A. R., Tagirdzhanova, G., Meidl, P., Freire Rallo, S., Kono, M., Fernández-Brime, S., Guðmundsson, H., Andrésson, Ó. S., Muggia, L., Mayrhofer, H., McCutcheon, J. P., Wedin, M., Werth, S., Willis, L. M., & Spribille, T. (2022). Large differences in carbohydrate degradation and transport potential among lichen fungal symbionts. Nature communications, 13(1), Article 2634. https://doi.org/10.1038/s41467-022-30218-6

Resl, P, Bujold, AR, Tagirdzhanova, G, Meidl, P, Freire Rallo, S, Kono, M, Fernández-Brime, S, Guðmundsson, H, Andrésson, ÓS, Muggia, L, Mayrhofer, H, McCutcheon, JP, Wedin, M, Werth, S, Willis, LM & Spribille, T 2022, 'Large differences in carbohydrate degradation and transport potential among lichen fungal symbionts', Nature communications, vol. 13, no. 1, 2634. https://doi.org/10.1038/s41467-022-30218-6

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title = "Large differences in carbohydrate degradation and transport potential among lichen fungal symbionts",

abstract = "Lichen symbioses are thought to be stabilized by the transfer of fixed carbon from a photosynthesizing symbiont to a fungus. In other fungal symbioses, carbohydrate subsidies correlate with reductions in plant cell wall-degrading enzymes, but whether this is true of lichen fungal symbionts (LFSs) is unknown. Here, we predict genes encoding carbohydrate-active enzymes (CAZymes) and sugar transporters in 46 genomes from the Lecanoromycetes, the largest extant clade of LFSs. All LFSs possess a robust CAZyme arsenal including enzymes acting on cellulose and hemicellulose, confirmed by experimental assays. However, the number of genes and predicted functions of CAZymes vary widely, with some fungal symbionts possessing arsenals on par with well-known saprotrophic fungi. These results suggest that stable fungal association with a phototroph does not in itself result in fungal CAZyme loss, and lends support to long-standing hypotheses that some lichens may augment fixed CO2 with carbon from external sources.",

author = "Philipp Resl and Bujold, {Adina R.} and Gulnara Tagirdzhanova and Peter Meidl and {Freire Rallo}, Sandra and Mieko Kono and Samantha Fern{\'a}ndez-Brime and H{\"o}r{\dh}ur Gu{\dh}mundsson and Andr{\'e}sson, {{\'O}lafur Sigmar} and Lucia Muggia and Helmut Mayrhofer and McCutcheon, {John P.} and Mats Wedin and Silke Werth and Willis, {Lisa M.} and Toby Spribille",

note = "Funding Information: The early phases of this project were funded by the Austrian Science Fund (FWF grant P25237, “Evolution of Substrate Specificity in Lichens”) and carried out at the Institute of Plant Sciences (Uni Graz). PR would like to acknowledge the Theodor K{\"o}rner Funds (Vienna, Austria) and Network of Biological Systematics Austria (NOBIS; Vienna, Austria) for funding that enabled genome sequencing of several species. PR would also like to thank Christoph Hahn and Fernando Fern{\'a}ndez-Mendoza for many methodological discussions. SW received funding from the Icelandic Research Fund IRF (174307-051), from Deutsche Forschungsgemeinschaft DFG (WE 6443/1-1) and from LMU Munich (startup funds). MW received funding from the Swedish Research Council, grant VR 2016-03589. MW and MK would like to acknowledge support from the NRM Department of Bioinformatics and Genetics, the National Genomics Infrastructure in Stockholm, the SNIC/Uppsala Multidisciplinary Center for Advanced Computational Science and the UPPMAX computational infrastructure, and Linda Phillips for assistance with material. TS would like to acknowledge an NSERC Discovery Grant, a Canada Research Chair in Symbiosis, and the generosity of Susan Dalby and Eskild Petersen, who provided a place to work on this manuscript. Special thanks go to Sophie Dang at the Molecular Biology Service Unit, University of Alberta Department of Biological Sciences, for help in data acquisition, and members of the U of A Lichen Evolution Lab for reading and commenting on the manuscript. We are also grateful to Sigrun Kraker, Theodora Kopun, Tanja Ernst and Andrea Brandl for laboratory assistance. Funding Information: The early phases of this project were funded by the Austrian Science Fund (FWF grant P25237, “Evolution of Substrate Specificity in Lichens”) and carried out at the Institute of Plant Sciences (Uni Graz). PR would like to acknowledge the Theodor K{\"o}rner Funds (Vienna, Austria) and Network of Biological Systematics Austria (NOBIS; Vienna, Austria) for funding that enabled genome sequencing of several species. PR would also like to thank Christoph Hahn and Fernando Fern{\'a}ndez-Mendoza for many methodological discussions. SW received funding from the Icelandic Research Fund IRF (174307-051), from Deutsche Forschungsgemeinschaft DFG (WE 6443/1-1) and from LMU Munich (startup funds). MW received funding from the Swedish Research Council, grant VR 2016-03589. MW and MK would like to acknowledge support from the NRM Department of Bioinformatics and Genetics, the National Genomics Infrastructure in Stockholm, the SNIC/Uppsala Multidisciplinary Center for Advanced Computational Science and the UPPMAX computational infrastructure, and Linda Phillips for assistance with material. TS would like to acknowledge an NSERC Discovery Grant, a Canada Research Chair in Symbiosis, and the generosity of Susan Dalby and Eskild Petersen, who provided a place to work on this manuscript. Special thanks go to Sophie Dang at the Molecular Biology Service Unit, University of Alberta Department of Biological Sciences, for help in data acquisition, and members of the U of A Lichen Evolution Lab for reading and commenting on the manuscript. We are also grateful to Sigrun Kraker, Theodora Kopun, Tanja Ernst and Andrea Brandl for laboratory assistance. Publisher Copyright: {\textcopyright} 2022, The Author(s).",

year = "2022",

month = dec,

doi = "10.1038/s41467-022-30218-6",

language = "English (US)",

volume = "13",

journal = "Nature communications",

issn = "2041-1723",

publisher = "Nature Publishing Group",

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TY - JOUR

T1 - Large differences in carbohydrate degradation and transport potential among lichen fungal symbionts

AU - Resl, Philipp

AU - Bujold, Adina R.

AU - Tagirdzhanova, Gulnara

AU - Meidl, Peter

AU - Freire Rallo, Sandra

AU - Kono, Mieko

AU - Fernández-Brime, Samantha

AU - Guðmundsson, Hörður

AU - Andrésson, Ólafur Sigmar

AU - Muggia, Lucia

AU - Mayrhofer, Helmut

AU - McCutcheon, John P.

AU - Wedin, Mats

AU - Werth, Silke

AU - Willis, Lisa M.

AU - Spribille, Toby

N1 - Funding Information: The early phases of this project were funded by the Austrian Science Fund (FWF grant P25237, “Evolution of Substrate Specificity in Lichens”) and carried out at the Institute of Plant Sciences (Uni Graz). PR would like to acknowledge the Theodor Körner Funds (Vienna, Austria) and Network of Biological Systematics Austria (NOBIS; Vienna, Austria) for funding that enabled genome sequencing of several species. PR would also like to thank Christoph Hahn and Fernando Fernández-Mendoza for many methodological discussions. SW received funding from the Icelandic Research Fund IRF (174307-051), from Deutsche Forschungsgemeinschaft DFG (WE 6443/1-1) and from LMU Munich (startup funds). MW received funding from the Swedish Research Council, grant VR 2016-03589. MW and MK would like to acknowledge support from the NRM Department of Bioinformatics and Genetics, the National Genomics Infrastructure in Stockholm, the SNIC/Uppsala Multidisciplinary Center for Advanced Computational Science and the UPPMAX computational infrastructure, and Linda Phillips for assistance with material. TS would like to acknowledge an NSERC Discovery Grant, a Canada Research Chair in Symbiosis, and the generosity of Susan Dalby and Eskild Petersen, who provided a place to work on this manuscript. Special thanks go to Sophie Dang at the Molecular Biology Service Unit, University of Alberta Department of Biological Sciences, for help in data acquisition, and members of the U of A Lichen Evolution Lab for reading and commenting on the manuscript. We are also grateful to Sigrun Kraker, Theodora Kopun, Tanja Ernst and Andrea Brandl for laboratory assistance. Funding Information: The early phases of this project were funded by the Austrian Science Fund (FWF grant P25237, “Evolution of Substrate Specificity in Lichens”) and carried out at the Institute of Plant Sciences (Uni Graz). PR would like to acknowledge the Theodor Körner Funds (Vienna, Austria) and Network of Biological Systematics Austria (NOBIS; Vienna, Austria) for funding that enabled genome sequencing of several species. PR would also like to thank Christoph Hahn and Fernando Fernández-Mendoza for many methodological discussions. SW received funding from the Icelandic Research Fund IRF (174307-051), from Deutsche Forschungsgemeinschaft DFG (WE 6443/1-1) and from LMU Munich (startup funds). MW received funding from the Swedish Research Council, grant VR 2016-03589. MW and MK would like to acknowledge support from the NRM Department of Bioinformatics and Genetics, the National Genomics Infrastructure in Stockholm, the SNIC/Uppsala Multidisciplinary Center for Advanced Computational Science and the UPPMAX computational infrastructure, and Linda Phillips for assistance with material. TS would like to acknowledge an NSERC Discovery Grant, a Canada Research Chair in Symbiosis, and the generosity of Susan Dalby and Eskild Petersen, who provided a place to work on this manuscript. Special thanks go to Sophie Dang at the Molecular Biology Service Unit, University of Alberta Department of Biological Sciences, for help in data acquisition, and members of the U of A Lichen Evolution Lab for reading and commenting on the manuscript. We are also grateful to Sigrun Kraker, Theodora Kopun, Tanja Ernst and Andrea Brandl for laboratory assistance. Publisher Copyright: © 2022, The Author(s).

PY - 2022/12

Y1 - 2022/12

N2 - Lichen symbioses are thought to be stabilized by the transfer of fixed carbon from a photosynthesizing symbiont to a fungus. In other fungal symbioses, carbohydrate subsidies correlate with reductions in plant cell wall-degrading enzymes, but whether this is true of lichen fungal symbionts (LFSs) is unknown. Here, we predict genes encoding carbohydrate-active enzymes (CAZymes) and sugar transporters in 46 genomes from the Lecanoromycetes, the largest extant clade of LFSs. All LFSs possess a robust CAZyme arsenal including enzymes acting on cellulose and hemicellulose, confirmed by experimental assays. However, the number of genes and predicted functions of CAZymes vary widely, with some fungal symbionts possessing arsenals on par with well-known saprotrophic fungi. These results suggest that stable fungal association with a phototroph does not in itself result in fungal CAZyme loss, and lends support to long-standing hypotheses that some lichens may augment fixed CO2 with carbon from external sources.

AB - Lichen symbioses are thought to be stabilized by the transfer of fixed carbon from a photosynthesizing symbiont to a fungus. In other fungal symbioses, carbohydrate subsidies correlate with reductions in plant cell wall-degrading enzymes, but whether this is true of lichen fungal symbionts (LFSs) is unknown. Here, we predict genes encoding carbohydrate-active enzymes (CAZymes) and sugar transporters in 46 genomes from the Lecanoromycetes, the largest extant clade of LFSs. All LFSs possess a robust CAZyme arsenal including enzymes acting on cellulose and hemicellulose, confirmed by experimental assays. However, the number of genes and predicted functions of CAZymes vary widely, with some fungal symbionts possessing arsenals on par with well-known saprotrophic fungi. These results suggest that stable fungal association with a phototroph does not in itself result in fungal CAZyme loss, and lends support to long-standing hypotheses that some lichens may augment fixed CO2 with carbon from external sources.

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JO - Nature communications

JF - Nature communications

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ER -

Large differences in carbohydrate degradation and transport potential among lichen fungal symbionts

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