Genomic characterization of three marine fungi, including Emericellopsis atlantica sp. nov. with signatures of a generalist lifestyle and marine biomass degradation
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
Affiliations
Ole Christian Hagestad
Marbio, The Norwegian College of Fishery Science, Department at Faculty of Biosciences, Fisheries and Economics, UiT The Arctic University of Norway
Lingwei Hou
Westerdijk Fungal Biodiversity Institute
Jeanette H. Andersen
Marbio, The Norwegian College of Fishery Science, Department at Faculty of Biosciences, Fisheries and Economics, UiT The Arctic University of Norway
Espen H. Hansen
Marbio, The Norwegian College of Fishery Science, Department at Faculty of Biosciences, Fisheries and Economics, UiT The Arctic University of Norway
Bjørn Altermark
The Norwegian Structural Biology Centre (NorStruct), Department of Chemistry, Faculty of Science and Technology, UiT the Arctic University of Norway
Chun Li
Marbio, The Norwegian College of Fishery Science, Department at Faculty of Biosciences, Fisheries and Economics, UiT The Arctic University of Norway
Eric Kuhnert
Institute of Organic Chemistry and BMWZ, Leibniz Universität Hannover
Russell J. Cox
Institute of Organic Chemistry and BMWZ, Leibniz Universität Hannover
Pedro W. Crous
Westerdijk Fungal Biodiversity Institute
Joseph W. Spatafora
Department of Botany and Plant Pathology, Oregon State University
Kathleen Lail
US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory
Mojgan Amirebrahimi
US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory
Anna Lipzen
US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory
Jasmyn Pangilinan
US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory
William Andreopoulos
US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory
Richard D. Hayes
US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory
Vivian Ng
US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory
Igor V. Grigoriev
US Department of Energy Joint Genome Institute, Lawrence Berkeley National Laboratory
Stephen A. Jackson
School of Microbiology, University College Cork
Thomas D. S. Sutton
School of Microbiology, University College Cork
Alan D. W. Dobson
School of Microbiology, University College Cork
Teppo Rämä
Marbio, The Norwegian College of Fishery Science, Department at Faculty of Biosciences, Fisheries and Economics, UiT The Arctic University of Norway
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.
