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Fucose as a nutrient ligand for Dikarya and a building block of early diverging lineages

ABSTRACT: Fucose is a deoxyhexose sugar present and studied in mammals. The process of fucosylation has been the primary focus in studies relating to fucose in animals due to the presence of fucose in Lewis antigens. Very few studies have reported its presence in Fungi, mostly in Mucoromycotina. The...

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Autores principales: Orłowska, Małgorzata, Barua, Drishtee, Piłsyk, Sebastian, Muszewska, Anna
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10481521/
https://www.ncbi.nlm.nih.gov/pubmed/37670396
http://dx.doi.org/10.1186/s43008-023-00123-8
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author Orłowska, Małgorzata
Barua, Drishtee
Piłsyk, Sebastian
Muszewska, Anna
author_facet Orłowska, Małgorzata
Barua, Drishtee
Piłsyk, Sebastian
Muszewska, Anna
author_sort Orłowska, Małgorzata
collection PubMed
description ABSTRACT: Fucose is a deoxyhexose sugar present and studied in mammals. The process of fucosylation has been the primary focus in studies relating to fucose in animals due to the presence of fucose in Lewis antigens. Very few studies have reported its presence in Fungi, mostly in Mucoromycotina. The constitution of 25% and 12% of this sugar in the carbohydrates of cell wall in the respective Umbelopsis and Mucorales strains boosts the need to bridge the gap of knowledge on fucose metabolism across the fungal tree of life. In the absence of a network map involving fucose proteins, we carried out an in-silico approach to construct the fucose metabolic map in Fungi. We analyzed the taxonomic distribution of 85 protein families in Fungi including diverse early diverging fungal lineages. The expression of fucose-related protein-coding genes proteins was validated with the help of transcriptomic data originating from representatives of early diverging fungi. We found proteins involved in several metabolic activities apart from fucosylation such as synthesis, transport and binding. Most of the identified protein families are shared with Metazoa suggesting an ancestral origin in Opisthokonta. However, the overall complexity of fucose metabolism is greater in Metazoa than in Fungi. Massive gene loss has shaped the evolutionary history of these metabolic pathways, leading to a repeated reduction of these pathways in most yeast-forming lineages. Our results point to a distinctive mode of utilization of fucose among fungi belonging to Dikarya and the early diverging lineages. We speculate that, while Dikarya used fucose as a source of nutrients for metabolism, the early diverging group of fungi depended on fucose as a building block and signaling compound. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s43008-023-00123-8.
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spelling pubmed-104815212023-09-07 Fucose as a nutrient ligand for Dikarya and a building block of early diverging lineages Orłowska, Małgorzata Barua, Drishtee Piłsyk, Sebastian Muszewska, Anna IMA Fungus Research ABSTRACT: Fucose is a deoxyhexose sugar present and studied in mammals. The process of fucosylation has been the primary focus in studies relating to fucose in animals due to the presence of fucose in Lewis antigens. Very few studies have reported its presence in Fungi, mostly in Mucoromycotina. The constitution of 25% and 12% of this sugar in the carbohydrates of cell wall in the respective Umbelopsis and Mucorales strains boosts the need to bridge the gap of knowledge on fucose metabolism across the fungal tree of life. In the absence of a network map involving fucose proteins, we carried out an in-silico approach to construct the fucose metabolic map in Fungi. We analyzed the taxonomic distribution of 85 protein families in Fungi including diverse early diverging fungal lineages. The expression of fucose-related protein-coding genes proteins was validated with the help of transcriptomic data originating from representatives of early diverging fungi. We found proteins involved in several metabolic activities apart from fucosylation such as synthesis, transport and binding. Most of the identified protein families are shared with Metazoa suggesting an ancestral origin in Opisthokonta. However, the overall complexity of fucose metabolism is greater in Metazoa than in Fungi. Massive gene loss has shaped the evolutionary history of these metabolic pathways, leading to a repeated reduction of these pathways in most yeast-forming lineages. Our results point to a distinctive mode of utilization of fucose among fungi belonging to Dikarya and the early diverging lineages. We speculate that, while Dikarya used fucose as a source of nutrients for metabolism, the early diverging group of fungi depended on fucose as a building block and signaling compound. GRAPHICAL ABSTRACT: [Image: see text] SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s43008-023-00123-8. BioMed Central 2023-09-05 /pmc/articles/PMC10481521/ /pubmed/37670396 http://dx.doi.org/10.1186/s43008-023-00123-8 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research
Orłowska, Małgorzata
Barua, Drishtee
Piłsyk, Sebastian
Muszewska, Anna
Fucose as a nutrient ligand for Dikarya and a building block of early diverging lineages
title Fucose as a nutrient ligand for Dikarya and a building block of early diverging lineages
title_full Fucose as a nutrient ligand for Dikarya and a building block of early diverging lineages
title_fullStr Fucose as a nutrient ligand for Dikarya and a building block of early diverging lineages
title_full_unstemmed Fucose as a nutrient ligand for Dikarya and a building block of early diverging lineages
title_short Fucose as a nutrient ligand for Dikarya and a building block of early diverging lineages
title_sort fucose as a nutrient ligand for dikarya and a building block of early diverging lineages
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10481521/
https://www.ncbi.nlm.nih.gov/pubmed/37670396
http://dx.doi.org/10.1186/s43008-023-00123-8
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