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: 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.

Genomic and Metabolomic Analyses of the Marine Fungus Emericellopsis cladophorae: Insights into Saltwater Adaptability Mechanisms and Its Biosynthetic Potential

“…A. sclerotigenum), previously known as the phytopathogenic fungus Ascochyta viciae [48]. Ascochlorin or related compounds have been reported to show antiviral and antitumor activities [49] and was found in some ascomycetes, including Acremonium-like or Emericellopsis species [22]. The ascochlorin cluster is constituted by eight genes: ascA (prenyltransferase), ascB (NRPS-like oxidoreductase), ascC (polyketide synthase), ascD (halogenase), ascE (P450 monooxygenase/P450 reductase), ascF (terpene cyclase), ascG (cytochrome P450) and ascR (transcription regulator).…”

“…The genus Emericellopsis harbors 23 species described so far. Recently, Hagestad et al [22] sequenced the first genome of an Emericellopsis species: E. atlantica strain TS7. The genome assembly and gene statistics for E. cladophorae and E. atlantica are summarized in Table 4.…”

“…The number of predicted genes encoding putative CAZymes of E. cladophorae is higher (2.7%) than that of E. atlantica. These differences might define the kind of carbon sources/substrates these species can use, possibly reflecting an adaption to their hosts: as mentioned above E. cladophorae was isolated from the alga Cladophora sp., and E. atlantica from the sponge Stelletta normani [22]. Such carbon sources include typically marine polysaccharides, such as agarose, alginate, carrageenan, chitin, fucoidan, laminarin, ulvan, among others [67].…”

“…Kuvarina et al [8] used an alkaline medium (pH 10.5) containing malt and yeast extract with ethyl acetate as solvent to obtain the crude extracts, while Gonçalves et al [18] used PDB and methanol. Additionally, Hagestad et al [22] used 11 different fermentation culture media and observed different bioactivities profiles, indicating the likelihood of expression of different compounds.…”

“…At present, studies on Emericellopsis mostly focus on the phylogenetic identification of species, but information about the entire genome and metabolome of this fungal genus is lacking. Recently, Hagestad et al [22] provided a detailed taxonomic and genomic description of the first sequenced Emericellopsis species: E. atlantica, isolated from the sponge Stelletta normani in the Atlantic Ocean.…”