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 fungi: <i>Emericellopsis</i> sp. TS7, wood-associated <i>Amylocarpus encephaloides</i> and algae-associated <i>Calycina marina</i>. These species were genome sequenced to study their genomic features, biosynthetic potential and phylogenetic placement using multilocus data. <i>Amylocarpus encephaloides</i> and <i>C. marina</i> were placed in the <i>Helotiaceae</i> and <i>Pezizellaceae (Helotiales)</i>, respectively, based on a 15-gene phylogenetic analysis. These two genomes had fewer biosynthetic gene clusters (BGCs) and carbohydrate active enzymes (CAZymes) than <i>Emericellopsis</i> sp. TS7 isolate. <i>Emericellopsis</i> sp. TS7 (<i>Hypocreales, Ascomycota</i>) was isolated from the sponge <i>Stelletta normani</i>. A six-gene phylogenetic analysis placed the isolate in the marine <i>Emericellopsis</i> clade and morphological examination confirmed that the isolate represents a new species, which is described here as <i>E. atlantica</i>. Analysis of its CAZyme repertoire and a culturing experiment on three marine and one terrestrial substrates indicated that <i>E. atlantica</i> 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 <i>E. atlantica</i>. The <i>Pezizellaceae</i> genome and the genome of the monotypic <i>Amylocarpus</i> 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.