Genomic characterization of three marine fungi, including Emericellopsis atlantica sp. nov. with signatures of a generalist lifestyle and marine biomass degradation

ABSTRACT Marine fungi remain poorly covered in global genome sequencing campaigns; the 1000 fungal genomes (1KFG) project attempts to shed light on the diversity, ecology and potential industrial use of overlooked and poorly resolved fungal taxa. This study characterizes the genomes of three marine...

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Main Authors: Ole Christian Hagestad, Lingwei Hou, Jeanette H. Andersen, Espen H. Hansen, Bjørn Altermark, Chun Li, Eric Kuhnert, Russell J. Cox, Pedro W. Crous, Joseph W. Spatafora, Kathleen Lail, Mojgan Amirebrahimi, Anna Lipzen, Jasmyn Pangilinan, William Andreopoulos, Richard D. Hayes, Vivian Ng, Igor V. Grigoriev, Stephen A. Jackson, Thomas D. S. Sutton, Alan D. W. Dobson, Teppo Rämä
Format: Article
Language:English
Published: BMC 2021-08-01
Series:IMA Fungus
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Online Access:https://doi.org/10.1186/s43008-021-00072-0
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author Ole Christian Hagestad
Lingwei Hou
Jeanette H. Andersen
Espen H. Hansen
Bjørn Altermark
Chun Li
Eric Kuhnert
Russell J. Cox
Pedro W. Crous
Joseph W. Spatafora
Kathleen Lail
Mojgan Amirebrahimi
Anna Lipzen
Jasmyn Pangilinan
William Andreopoulos
Richard D. Hayes
Vivian Ng
Igor V. Grigoriev
Stephen A. Jackson
Thomas D. S. Sutton
Alan D. W. Dobson
Teppo Rämä
author_facet Ole Christian Hagestad
Lingwei Hou
Jeanette H. Andersen
Espen H. Hansen
Bjørn Altermark
Chun Li
Eric Kuhnert
Russell J. Cox
Pedro W. Crous
Joseph W. Spatafora
Kathleen Lail
Mojgan Amirebrahimi
Anna Lipzen
Jasmyn Pangilinan
William Andreopoulos
Richard D. Hayes
Vivian Ng
Igor V. Grigoriev
Stephen A. Jackson
Thomas D. S. Sutton
Alan D. W. Dobson
Teppo Rämä
author_sort Ole Christian Hagestad
collection DOAJ
description ABSTRACT Marine fungi remain poorly covered in global genome sequencing campaigns; the 1000 fungal genomes (1KFG) project attempts to shed light on the diversity, ecology and potential industrial use of overlooked and poorly resolved fungal taxa. This study characterizes the genomes of three marine fungi: Emericellopsis sp. TS7, wood-associated Amylocarpus encephaloides and algae-associated Calycina marina. These species were genome sequenced to study their genomic features, biosynthetic potential and phylogenetic placement using multilocus data. Amylocarpus encephaloides and C. marina were placed in the Helotiaceae and Pezizellaceae (Helotiales), respectively, based on a 15-gene phylogenetic analysis. These two genomes had fewer biosynthetic gene clusters (BGCs) and carbohydrate active enzymes (CAZymes) than Emericellopsis sp. TS7 isolate. Emericellopsis sp. TS7 (Hypocreales, Ascomycota) was isolated from the sponge Stelletta normani. A six-gene phylogenetic analysis placed the isolate in the marine Emericellopsis clade and morphological examination confirmed that the isolate represents a new species, which is described here as E. atlantica. Analysis of its CAZyme repertoire and a culturing experiment on three marine and one terrestrial substrates indicated that E. atlantica is a psychrotrophic generalist fungus that is able to degrade several types of marine biomass. FungiSMASH analysis revealed the presence of 35 BGCs including, eight non-ribosomal peptide synthases (NRPSs), six NRPS-like, six polyketide synthases, nine terpenes and six hybrid, mixed or other clusters. Of these BGCs, only five were homologous with characterized BGCs. The presence of unknown BGCs sets and large CAZyme repertoire set stage for further investigations of E. atlantica. The Pezizellaceae genome and the genome of the monotypic Amylocarpus genus represent the first published genomes of filamentous fungi that are restricted in their occurrence to the marine habitat and form thus a valuable resource for the community that can be used in studying ecological adaptions of fungi using comparative genomics.
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spelling doaj-art-2d4678d8f908489583a2e1a111df6ec72025-02-02T02:21:51ZengBMCIMA Fungus2210-63592021-08-0112112310.1186/s43008-021-00072-0Genomic characterization of three marine fungi, including Emericellopsis atlantica sp. nov. with signatures of a generalist lifestyle and marine biomass degradationOle Christian Hagestad0Lingwei Hou1Jeanette H. Andersen2Espen H. Hansen3Bjørn Altermark4Chun Li5Eric Kuhnert6Russell J. Cox7Pedro W. Crous8Joseph W. Spatafora9Kathleen Lail10Mojgan Amirebrahimi11Anna Lipzen12Jasmyn Pangilinan13William Andreopoulos14Richard D. Hayes15Vivian Ng16Igor V. Grigoriev17Stephen A. Jackson18Thomas D. S. Sutton19Alan D. W. Dobson20Teppo Rämä21Marbio, The Norwegian College of Fishery Science, Department at Faculty of Biosciences, Fisheries and Economics, UiT The Arctic University of NorwayWesterdijk Fungal Biodiversity InstituteMarbio, The Norwegian College of Fishery Science, Department at Faculty of Biosciences, Fisheries and Economics, UiT The Arctic University of NorwayMarbio, The Norwegian College of Fishery Science, Department at Faculty of Biosciences, Fisheries and Economics, UiT The Arctic University of NorwayThe Norwegian Structural Biology Centre (NorStruct), Department of Chemistry, Faculty of Science and Technology, UiT the Arctic University of NorwayMarbio, The Norwegian College of Fishery Science, Department at Faculty of Biosciences, Fisheries and Economics, UiT The Arctic University of NorwayInstitute of Organic Chemistry and BMWZ, Leibniz Universität HannoverInstitute of Organic Chemistry and BMWZ, Leibniz Universität HannoverWesterdijk Fungal Biodiversity InstituteDepartment of Botany and Plant Pathology, Oregon State UniversityUS Department of Energy Joint Genome Institute, Lawrence Berkeley National LaboratoryUS Department of Energy Joint Genome Institute, Lawrence Berkeley National LaboratoryUS Department of Energy Joint Genome Institute, Lawrence Berkeley National LaboratoryUS Department of Energy Joint Genome Institute, Lawrence Berkeley National LaboratoryUS Department of Energy Joint Genome Institute, Lawrence Berkeley National LaboratoryUS Department of Energy Joint Genome Institute, Lawrence Berkeley National LaboratoryUS Department of Energy Joint Genome Institute, Lawrence Berkeley National LaboratoryUS Department of Energy Joint Genome Institute, Lawrence Berkeley National LaboratorySchool of Microbiology, University College CorkSchool of Microbiology, University College CorkSchool of Microbiology, University College CorkMarbio, The Norwegian College of Fishery Science, Department at Faculty of Biosciences, Fisheries and Economics, UiT The Arctic University of NorwayABSTRACT Marine fungi remain poorly covered in global genome sequencing campaigns; the 1000 fungal genomes (1KFG) project attempts to shed light on the diversity, ecology and potential industrial use of overlooked and poorly resolved fungal taxa. This study characterizes the genomes of three marine fungi: Emericellopsis sp. TS7, wood-associated Amylocarpus encephaloides and algae-associated Calycina marina. These species were genome sequenced to study their genomic features, biosynthetic potential and phylogenetic placement using multilocus data. Amylocarpus encephaloides and C. marina were placed in the Helotiaceae and Pezizellaceae (Helotiales), respectively, based on a 15-gene phylogenetic analysis. These two genomes had fewer biosynthetic gene clusters (BGCs) and carbohydrate active enzymes (CAZymes) than Emericellopsis sp. TS7 isolate. Emericellopsis sp. TS7 (Hypocreales, Ascomycota) was isolated from the sponge Stelletta normani. A six-gene phylogenetic analysis placed the isolate in the marine Emericellopsis clade and morphological examination confirmed that the isolate represents a new species, which is described here as E. atlantica. Analysis of its CAZyme repertoire and a culturing experiment on three marine and one terrestrial substrates indicated that E. atlantica is a psychrotrophic generalist fungus that is able to degrade several types of marine biomass. FungiSMASH analysis revealed the presence of 35 BGCs including, eight non-ribosomal peptide synthases (NRPSs), six NRPS-like, six polyketide synthases, nine terpenes and six hybrid, mixed or other clusters. Of these BGCs, only five were homologous with characterized BGCs. The presence of unknown BGCs sets and large CAZyme repertoire set stage for further investigations of E. atlantica. The Pezizellaceae genome and the genome of the monotypic Amylocarpus genus represent the first published genomes of filamentous fungi that are restricted in their occurrence to the marine habitat and form thus a valuable resource for the community that can be used in studying ecological adaptions of fungi using comparative genomics.https://doi.org/10.1186/s43008-021-00072-0BioprospectingGenome miningIlluminaLignocellulolytic enzymesPhysiologyTaxonomy
spellingShingle Ole Christian Hagestad
Lingwei Hou
Jeanette H. Andersen
Espen H. Hansen
Bjørn Altermark
Chun Li
Eric Kuhnert
Russell J. Cox
Pedro W. Crous
Joseph W. Spatafora
Kathleen Lail
Mojgan Amirebrahimi
Anna Lipzen
Jasmyn Pangilinan
William Andreopoulos
Richard D. Hayes
Vivian Ng
Igor V. Grigoriev
Stephen A. Jackson
Thomas D. S. Sutton
Alan D. W. Dobson
Teppo Rämä
Genomic characterization of three marine fungi, including Emericellopsis atlantica sp. nov. with signatures of a generalist lifestyle and marine biomass degradation
IMA Fungus
Bioprospecting
Genome mining
Illumina
Lignocellulolytic enzymes
Physiology
Taxonomy
title Genomic characterization of three marine fungi, including Emericellopsis atlantica sp. nov. with signatures of a generalist lifestyle and marine biomass degradation
title_full Genomic characterization of three marine fungi, including Emericellopsis atlantica sp. nov. with signatures of a generalist lifestyle and marine biomass degradation
title_fullStr Genomic characterization of three marine fungi, including Emericellopsis atlantica sp. nov. with signatures of a generalist lifestyle and marine biomass degradation
title_full_unstemmed Genomic characterization of three marine fungi, including Emericellopsis atlantica sp. nov. with signatures of a generalist lifestyle and marine biomass degradation
title_short Genomic characterization of three marine fungi, including Emericellopsis atlantica sp. nov. with signatures of a generalist lifestyle and marine biomass degradation
title_sort genomic characterization of three marine fungi including emericellopsis atlantica sp nov with signatures of a generalist lifestyle and marine biomass degradation
topic Bioprospecting
Genome mining
Illumina
Lignocellulolytic enzymes
Physiology
Taxonomy
url https://doi.org/10.1186/s43008-021-00072-0
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