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...

Full description

Bibliographic Details
Main Authors: Małgorzata Orłowska, Drishtee Barua, Sebastian Piłsyk, Anna Muszewska
Format: Article
Language:English
Published: BMC 2023-09-01
Series:IMA Fungus
Subjects:
Online Access:https://doi.org/10.1186/s43008-023-00123-8
_version_ 1797451914249502720
author Małgorzata Orłowska
Drishtee Barua
Sebastian Piłsyk
Anna Muszewska
author_facet Małgorzata Orłowska
Drishtee Barua
Sebastian Piłsyk
Anna Muszewska
author_sort Małgorzata Orłowska
collection DOAJ
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
first_indexed 2024-03-09T15:01:19Z
format Article
id doaj.art-be46bb656e904a9d9f03c16d419a6b84
institution Directory Open Access Journal
issn 2210-6359
language English
last_indexed 2024-03-09T15:01:19Z
publishDate 2023-09-01
publisher BMC
record_format Article
series IMA Fungus
spelling doaj.art-be46bb656e904a9d9f03c16d419a6b842023-11-26T13:53:39ZengBMCIMA Fungus2210-63592023-09-0114111710.1186/s43008-023-00123-8Fucose as a nutrient ligand for Dikarya and a building block of early diverging lineagesMałgorzata Orłowska0Drishtee Barua1Sebastian Piłsyk2Anna Muszewska3Institute of Biochemistry and Biophysics, Polish Academy of SciencesInstitute of Biochemistry and Biophysics, Polish Academy of SciencesInstitute of Biochemistry and Biophysics, Polish Academy of SciencesInstitute of Biochemistry and Biophysics, Polish Academy of SciencesAbstract 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 abstracthttps://doi.org/10.1186/s43008-023-00123-8FucosyltransferasesFucose degradationFungal proteinsFungal enzymesLectinsFucose biosynthesis
spellingShingle Małgorzata Orłowska
Drishtee Barua
Sebastian Piłsyk
Anna Muszewska
Fucose as a nutrient ligand for Dikarya and a building block of early diverging lineages
IMA Fungus
Fucosyltransferases
Fucose degradation
Fungal proteins
Fungal enzymes
Lectins
Fucose biosynthesis
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 Fucosyltransferases
Fucose degradation
Fungal proteins
Fungal enzymes
Lectins
Fucose biosynthesis
url https://doi.org/10.1186/s43008-023-00123-8
work_keys_str_mv AT małgorzataorłowska fucoseasanutrientligandfordikaryaandabuildingblockofearlydiverginglineages
AT drishteebarua fucoseasanutrientligandfordikaryaandabuildingblockofearlydiverginglineages
AT sebastianpiłsyk fucoseasanutrientligandfordikaryaandabuildingblockofearlydiverginglineages
AT annamuszewska fucoseasanutrientligandfordikaryaandabuildingblockofearlydiverginglineages