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

TY - JOUR

T1 - Genomic characterization of three marine fungi, including Emericellopsis atlantica sp. nov. with signatures of a generalist lifestyle and marine biomass degradation

AU - Hagestad, Ole Christian

AU - Hou, Lingwei

AU - Andersen, Jeanette H.

AU - Hansen, Espen H.

AU - Altermark, Bjørn

AU - Li, Chun

AU - Kuhnert, Eric

AU - Cox, Russell J.

AU - Crous, Pedro W.

AU - Spatafora, Joseph W.

AU - Lail, Kathleen

AU - Amirebrahimi, Mojgan

AU - Lipzen, Anna

AU - Pangilinan, Jasmyn

AU - Andreopoulos, William

AU - Hayes, Richard D.

AU - Ng, Vivian

AU - Grigoriev, Igor V.

AU - Jackson, Stephen A.

AU - Sutton, Thomas D.S.

AU - Dobson, Alan D.W.

AU - Rämä, Teppo

N1 - Funding Information: Digibiotics (Digital Life Norway) and Centre for New Antibacterial Strategies at UiT The Arctic University of Norway, through the Research Council of Norway (Project 269425) provided funding for Teppo Rämä. This research was performed within the Community Sequence Program “1KFG” conducted by the U.S. Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, which was supported by the Office of Science of the U.S. Department of Energy under contract DE-AC02-05CH11231. This work benefitted from the sharing of expertise within the DFG priority program “Taxon-Omics: New Approaches for Discovering and Naming Biodiversity” (SPP 1991) to RJC and EK. Funding Information: Bernard Picton (Ulster Museum) and Christine Morrow (Queens University Belfast) performed the identification of the host sponge. Ronald de Vries and Ad Wiebenga (Westerdijk Institute) provided extraction protocols. Marte Jenssen (Marbio) cultured Emericellopsis atlantica for DNA and RNA extraction. The Norwegian marine biobank (Marbank) provided the sponge extract used in the culturing study. Marte Albrigtsen and Kirsti Helland (Marbio) ran the bioassays. Genetic resources used in this study adhere to national and international regulations (Nagoya Protocol of the Convention on Biological Diversity), as the UK materials used were accessed in accordance with applicable legislation of the providing country (sampled before 12 October 2015). Publisher Copyright: © 2021, The Author(s).

PY - 2021/12

Y1 - 2021/12

N2 - 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.

AB - 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.

KW - 1 new taxon

KW - Bioprospecting

KW - Genome mining

KW - Illumina

KW - Lignocellulolytic enzymes

KW - Physiology

KW - Taxonomy

U2 - 10.1186/s43008-021-00072-0

DO - 10.1186/s43008-021-00072-0

M3 - Article

AN - SCOPUS:85112365826

SN - 2210-6340

VL - 12

JO - IMA Fungus

JF - IMA Fungus

M1 - 21

ER -