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

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: Em...

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Autores principales: Hagestad, Ole Christian, Hou, Lingwei, Andersen, Jeanette H., Hansen, Espen H., Altermark, Bjørn, Li, Chun, Kuhnert, Eric, Cox, Russell J., Crous, Pedro W., Spatafora, Joseph W., Lail, Kathleen, Amirebrahimi, Mojgan, Lipzen, Anna, Pangilinan, Jasmyn, Andreopoulos, William, Hayes, Richard D., Ng, Vivian, Grigoriev, Igor V., Jackson, Stephen A., Sutton, Thomas D. S., Dobson, Alan D. W., Rämä, Teppo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8351168/
https://www.ncbi.nlm.nih.gov/pubmed/34372938
http://dx.doi.org/10.1186/s43008-021-00072-0
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author Hagestad, Ole Christian
Hou, Lingwei
Andersen, Jeanette H.
Hansen, Espen H.
Altermark, Bjørn
Li, Chun
Kuhnert, Eric
Cox, Russell J.
Crous, Pedro W.
Spatafora, Joseph W.
Lail, Kathleen
Amirebrahimi, Mojgan
Lipzen, Anna
Pangilinan, Jasmyn
Andreopoulos, William
Hayes, Richard D.
Ng, Vivian
Grigoriev, Igor V.
Jackson, Stephen A.
Sutton, Thomas D. S.
Dobson, Alan D. W.
Rämä, Teppo
author_facet Hagestad, Ole Christian
Hou, Lingwei
Andersen, Jeanette H.
Hansen, Espen H.
Altermark, Bjørn
Li, Chun
Kuhnert, Eric
Cox, Russell J.
Crous, Pedro W.
Spatafora, Joseph W.
Lail, Kathleen
Amirebrahimi, Mojgan
Lipzen, Anna
Pangilinan, Jasmyn
Andreopoulos, William
Hayes, Richard D.
Ng, Vivian
Grigoriev, Igor V.
Jackson, Stephen A.
Sutton, Thomas D. S.
Dobson, Alan D. W.
Rämä, Teppo
author_sort Hagestad, Ole Christian
collection PubMed
description 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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s43008-021-00072-0.
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spelling pubmed-83511682021-08-23 Genomic characterization of three marine fungi, including Emericellopsis atlantica sp. nov. with signatures of a generalist lifestyle and marine biomass degradation Hagestad, Ole Christian Hou, Lingwei Andersen, Jeanette H. Hansen, Espen H. Altermark, Bjørn Li, Chun Kuhnert, Eric Cox, Russell J. Crous, Pedro W. Spatafora, Joseph W. Lail, Kathleen Amirebrahimi, Mojgan Lipzen, Anna Pangilinan, Jasmyn Andreopoulos, William Hayes, Richard D. Ng, Vivian Grigoriev, Igor V. Jackson, Stephen A. Sutton, Thomas D. S. Dobson, Alan D. W. Rämä, Teppo IMA Fungus Research 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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s43008-021-00072-0. BioMed Central 2021-08-09 /pmc/articles/PMC8351168/ /pubmed/34372938 http://dx.doi.org/10.1186/s43008-021-00072-0 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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
Hagestad, Ole Christian
Hou, Lingwei
Andersen, Jeanette H.
Hansen, Espen H.
Altermark, Bjørn
Li, Chun
Kuhnert, Eric
Cox, Russell J.
Crous, Pedro W.
Spatafora, Joseph W.
Lail, Kathleen
Amirebrahimi, Mojgan
Lipzen, Anna
Pangilinan, Jasmyn
Andreopoulos, William
Hayes, Richard D.
Ng, Vivian
Grigoriev, Igor V.
Jackson, Stephen A.
Sutton, Thomas D. S.
Dobson, Alan D. W.
Rämä, Teppo
Genomic characterization of three marine fungi, including Emericellopsis atlantica sp. nov. with signatures of a generalist lifestyle and marine biomass degradation
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 Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8351168/
https://www.ncbi.nlm.nih.gov/pubmed/34372938
http://dx.doi.org/10.1186/s43008-021-00072-0
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