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. 2021 Aug 9;12(1):21.
doi: 10.1186/s43008-021-00072-0.

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

Ole Christian Hagestad  1 , Lingwei Hou  2 , Jeanette H Andersen  3 , Espen H Hansen  3 , Bjørn Altermark  4 , Chun Li  3 , Eric Kuhnert  5 , Russell J Cox  5 , Pedro W Crous  2 , Joseph W Spatafora  6 , Kathleen Lail  7 , Mojgan Amirebrahimi  7 , Anna Lipzen  7 , Jasmyn Pangilinan  7 , William Andreopoulos  7 , Richard D Hayes  7 , Vivian Ng  7 , Igor V Grigoriev  7   8 , Stephen A Jackson  9   10 , Thomas D S Sutton  9   11 , Alan D W Dobson  9   10 , Teppo Rämä  3
Affiliations

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

Ole Christian Hagestad et al. IMA Fungus. .

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.

Keywords: 1 new taxon; Bioprospecting; Genome mining; Illumina; Lignocellulolytic enzymes; Physiology; Taxonomy.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
Phylogenetic tree from MrBayes of the genus Emericellopsis based on a six gene multilocus alignment of available ex-type and representative sequences. Branch support values are from Bayesian posterior probability (top) and Maximum-likelihood aBayes support test (bottom). Branch length represents substitutions per sequence site. The taxon in bold is the studied fungus. The bold letter T denotes sequences of ex-type cultures. Accession numbers for each isolate are in Supplementary data 2, PhyML tree can be seen in Supplementary data 3
Fig. 2
Fig. 2
Growth characterization of Emericellopsis sp. TS7 using four different substrates and three different salinities incubated at four different temperatures. Maximum growth was 86 mm. Max growth of growth control on distilled water agar is shown in the first panel with encircled symbols. The control for 10 °C and 15 °C is identical
Fig. 3
Fig. 3
Overview of the distribution of CAZymes in Emericellopsis sp. TS7 Amylocarpus encephaloides and Calycina marina and three other fungi. The lines indicate the number of genes and number of genes with putative secretion signal and uses the secondary Y-axis
Fig. 4
Fig. 4
Examples of putatively secreted modular CAZymes from Emericellopsis sp. TS7, Amylocarpus encephaloides and Calycina marina. The illustration is not to scale. SP – Secretion signal peptide, GH – Glycoside hydrolase, CBM – Carbohydrate binding module, AA – Auxiliary activity, CE – Carboxyl esterase. Number indicates enzyme class. Number in brackets is protein identifier
Fig. 5
Fig. 5
Overview of BGC structure of the predicted clusters in Emericellopsis sp. TS7 colored after function. Clusters marked in red were on the end of scaffolds and may be incomplete. The leucinostatin-like cluster was split in two, but is presented as one cluster with a gap. Helvolic acid, produced by the cluster in bold, were detected in MS analyses of fermentation broths
Fig. 6
Fig. 6
Phylogeny of Helotiales based on a 15-gene dataset for the analysis. The support values are from the ultrafast bootstrap in IQ-TREE. The bold letter T denotes ex-type sequences. Xylaria hypoxylon was used as an outgroup
Fig. 7
Fig. 7
Emericellopsis atlantica (ex-type CBS 147198). Colonies on OA (a), MEA (b) and PDA (c) after 21 d at 25 C. d–f, i Phialides. g–h. Branched conidiophores. j Conidia. Scale bars = 10 μm
See this image and copyright information in PMC

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