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...
Saved in:
Main Authors: | , , , , , , , , , , , , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
BMC
2021-08-01
|
Series: | IMA Fungus |
Subjects: | |
Online Access: | https://doi.org/10.1186/s43008-021-00072-0 |
Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
_version_ | 1832573885502980096 |
---|---|
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. |
format | Article |
id | doaj-art-2d4678d8f908489583a2e1a111df6ec7 |
institution | Kabale University |
issn | 2210-6359 |
language | English |
publishDate | 2021-08-01 |
publisher | BMC |
record_format | Article |
series | IMA Fungus |
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 |
work_keys_str_mv | AT olechristianhagestad genomiccharacterizationofthreemarinefungiincludingemericellopsisatlanticaspnovwithsignaturesofageneralistlifestyleandmarinebiomassdegradation AT lingweihou genomiccharacterizationofthreemarinefungiincludingemericellopsisatlanticaspnovwithsignaturesofageneralistlifestyleandmarinebiomassdegradation AT jeanettehandersen genomiccharacterizationofthreemarinefungiincludingemericellopsisatlanticaspnovwithsignaturesofageneralistlifestyleandmarinebiomassdegradation AT espenhhansen genomiccharacterizationofthreemarinefungiincludingemericellopsisatlanticaspnovwithsignaturesofageneralistlifestyleandmarinebiomassdegradation AT bjørnaltermark genomiccharacterizationofthreemarinefungiincludingemericellopsisatlanticaspnovwithsignaturesofageneralistlifestyleandmarinebiomassdegradation AT chunli genomiccharacterizationofthreemarinefungiincludingemericellopsisatlanticaspnovwithsignaturesofageneralistlifestyleandmarinebiomassdegradation AT erickuhnert genomiccharacterizationofthreemarinefungiincludingemericellopsisatlanticaspnovwithsignaturesofageneralistlifestyleandmarinebiomassdegradation AT russelljcox genomiccharacterizationofthreemarinefungiincludingemericellopsisatlanticaspnovwithsignaturesofageneralistlifestyleandmarinebiomassdegradation AT pedrowcrous genomiccharacterizationofthreemarinefungiincludingemericellopsisatlanticaspnovwithsignaturesofageneralistlifestyleandmarinebiomassdegradation AT josephwspatafora genomiccharacterizationofthreemarinefungiincludingemericellopsisatlanticaspnovwithsignaturesofageneralistlifestyleandmarinebiomassdegradation AT kathleenlail genomiccharacterizationofthreemarinefungiincludingemericellopsisatlanticaspnovwithsignaturesofageneralistlifestyleandmarinebiomassdegradation AT mojganamirebrahimi genomiccharacterizationofthreemarinefungiincludingemericellopsisatlanticaspnovwithsignaturesofageneralistlifestyleandmarinebiomassdegradation AT annalipzen genomiccharacterizationofthreemarinefungiincludingemericellopsisatlanticaspnovwithsignaturesofageneralistlifestyleandmarinebiomassdegradation AT jasmynpangilinan genomiccharacterizationofthreemarinefungiincludingemericellopsisatlanticaspnovwithsignaturesofageneralistlifestyleandmarinebiomassdegradation AT williamandreopoulos genomiccharacterizationofthreemarinefungiincludingemericellopsisatlanticaspnovwithsignaturesofageneralistlifestyleandmarinebiomassdegradation AT richarddhayes genomiccharacterizationofthreemarinefungiincludingemericellopsisatlanticaspnovwithsignaturesofageneralistlifestyleandmarinebiomassdegradation AT vivianng genomiccharacterizationofthreemarinefungiincludingemericellopsisatlanticaspnovwithsignaturesofageneralistlifestyleandmarinebiomassdegradation AT igorvgrigoriev genomiccharacterizationofthreemarinefungiincludingemericellopsisatlanticaspnovwithsignaturesofageneralistlifestyleandmarinebiomassdegradation AT stephenajackson genomiccharacterizationofthreemarinefungiincludingemericellopsisatlanticaspnovwithsignaturesofageneralistlifestyleandmarinebiomassdegradation AT thomasdssutton genomiccharacterizationofthreemarinefungiincludingemericellopsisatlanticaspnovwithsignaturesofageneralistlifestyleandmarinebiomassdegradation AT alandwdobson genomiccharacterizationofthreemarinefungiincludingemericellopsisatlanticaspnovwithsignaturesofageneralistlifestyleandmarinebiomassdegradation AT tepporama genomiccharacterizationofthreemarinefungiincludingemericellopsisatlanticaspnovwithsignaturesofageneralistlifestyleandmarinebiomassdegradation |