DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

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

Journal Article · · 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.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
Research Council of Norway; USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1812405
Journal Information:
IMA Fungus, Journal Name: IMA Fungus Journal Issue: 1 Vol. 12; ISSN 2210-6359
Publisher:
Pensoft PublishersCopyright Statement
Country of Publication:
Netherlands
Language:
English

References (138)

Determination of the uronic acid composition of seaweed dietaryfibre by HPLC journal March 2004
Extreme biophysics: Enzymes under pressure journal January 2017
Predicting transmembrane protein topology with a hidden markov model: application to complete genomes11Edited by F. Cohen journal January 2001
Polymorphic karyotypes in related Acremonium strains journal February 1991
Sopra un interessante plectomicete umicolo nuovo per la scienza:Peyronellula mirabilis n.g. et n.sp. journal June 1952
Beschreibung einiger neuer Pilzarten aus dem Centraalbureau voor Schimmelcultures, Baarn (Nederland): VI. Mitteilung journal December 1939
The chemical composition of the diatom frustule journal April 1961
Diversity and Characterization of Culturable Fungi from Marine Sediment Collected from St. Helena Bay, South Africa journal March 2012
Bioconversion of red seaweed galactans: a focus on bacterial agarases and carrageenases journal June 2006
Diverse Deep-Sea Fungi from the South China Sea and Their Antimicrobial Activity journal June 2013
Fungal community associated with marine macroalgae from Antarctica journal November 2009
Fungal Infection of Mantis Shrimp (Oratosquilla oratoria) Caused by Two Anamorphic Fungi Found in Japan journal January 2009
Psychrophilic and psychrotrophic fungi: a comprehensive review journal April 2016
Diversity and potential antifungal properties of fungi associated with a Mediterranean sponge journal January 2010
Fungal diversity notes 367–490: taxonomic and phylogenetic contributions to fungal taxa journal September 2016
Fungal diversity notes 929–1035: taxonomic and phylogenetic contributions on genera and species of fungi journal March 2019
High quality genome sequences of thirteen Hypoxylaceae (Ascomycota) strengthen the phylogenetic family backbone and enable the discovery of new taxa journal May 2020
Biosynthesis of gallotannins: β-Glucogallin-dependent formation of 1,2,3,4,6-pentagalloylglucose by enzymatic galloylation of 1,2,3,6-tetragalloylglucose journal August 1989
Emericellopsis minima sp.nov. and Westerdykella ornata gen.nov., sp.nov. journal December 1955
Emericellopsis stolkiae sp.nov. from saline soils in Wyoming journal December 1971
Cephalosporium-like hyphomycetes journal June 1975
The pectic substances of zosteraceae journal March 1968
Fucoidans from the brown seaweed Adenocystis utricularis: extraction methods, antiviral activity and structural studies journal January 2003
Drugs from the deep: marine natural products as drug candidates journal June 2003
Innovations in CAZyme gene diversity and its modification for biorefinery applications journal December 2020
Missing data and the design of phylogenetic analyses journal February 2006
Genomic and proteomic biases inform metabolic engineering strategies for anaerobic fungi journal June 2020
Bacterial genomic G+C composition-eliciting environmental adaptation journal January 2010
Sesquiterpene Synthase from the Botrydial Biosynthetic Gene Cluster of the Phytopathogen Botrytis cinerea journal November 2008
Biosynthesis of Steroidal Antibiotic Fusidanes: Functional Analysis of Oxidosqualene Cyclase and Subsequent Tailoring Enzymes from Aspergillus fumigatus journal April 2009
Induction of phlorotannin production in a brown alga: defense or resource dynamics? journal October 2003
Intense hydrolytic enzyme activity on marine aggregates and implications for rapid particle dissolution journal September 1992
Full-length transcriptome assembly from RNA-Seq data without a reference genome journal May 2011
Genomic adaptations of the halophilic Dead Sea filamentous fungus Eurotium rubrum journal May 2014
SignalP 4.0: discriminating signal peptides from transmembrane regions journal September 2011
Fast and sensitive protein alignment using DIAMOND journal November 2014
ModelFinder: fast model selection for accurate phylogenetic estimates journal May 2017
Polysaccharide utilization loci of North Sea Flavobacteriia as basis for using SusC/D-protein expression for predicting major phytoplankton glycans journal August 2018
Extreme sensitivity to ultraviolet light in the fungal pathogen causing white-nose syndrome of bats journal January 2018
Three previously unrecognised classes of biosynthetic enzymes revealed during the production of xenovulene A journal May 2018
The birth, evolution and death of metabolic gene clusters in fungi journal September 2018
A marine bacterial enzymatic cascade degrades the algal polysaccharide ulvan journal July 2019
Diversity and distribution of fungal communities in the marine sediments of Kongsfjorden, Svalbard (High Arctic) journal October 2015
The cycloaspeptides: uncovering a new model for methylated nonribosomal peptide biosynthesis journal January 2018
Marine natural products journal January 2020
Carbohydrate-binding modules: fine-tuning polysaccharide recognition journal September 2004
Complete biosynthetic pathways of ascofuranone and ascochlorin in Acremonium egyptiacum journal April 2019
A Novel Unsaturated β-Glucuronyl Hydrolase Involved in Ulvan Degradation Unveils the Versatility of Stereochemistry Requirements in Family GH105 journal February 2014
Endo-fucoidan hydrolases from glycoside hydrolase family 107 (GH107) display structural and mechanistic similarities to α-l-fucosidases from GH29 journal November 2018
The Perfect Stage of an Antibiotic—Producing Cephalosporium journal May 1957
A New Emericellopsis Species with Stilbella-Type of Conidia journal September 1960
A New Emericellopsis from Wisconsin, With Notes on Other Species journal January 1961
Novel halotolerant species of Emericellopsis and Parasarocladium associated with macroalgae in an estuarine environment journal December 2019
Approximate Likelihood-Ratio Test for Branches: A Fast, Accurate, and Powerful Alternative journal August 2006
Fungal Diversity and Enzyme Activity Associated with the Macroalgae, Agarum clathratum journal January 2019
Deep-sea sponge grounds of the Flemish Cap, Flemish Pass and the Grand Banks of Newfoundland (Northwest Atlantic Ocean): Distribution and species composition journal November 2012
Fueling the future with fungal genomics journal July 2011
Living strategy of cold-adapted fungi with the reference to several representative species journal July 2017
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing journal May 2012
PROSITE: A documented database using patterns and profiles as motif descriptors journal January 2002
clinker & clustermap.js: automatic generation of gene cluster comparison figures journal January 2021
CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes journal March 2007
Prediction of missing sequences and branch lengths in phylogenomic data journal January 2016
Evolution and Diversity of Transposable Elements in Vertebrate Genomes journal January 2017
Cut-and-Paste Transposons in Fungi with Diverse Lifestyles journal December 2017
Characterization of a new  -L-fucosidase isolated from the marine mollusk Pecten maximus that catalyzes the hydrolysis of  -L-fucose from algal fucoidan (Ascophyllum nodosum) journal April 2002
PartitionFinder: Combined Selection of Partitioning Schemes and Substitution Models for Phylogenetic Analyses journal January 2012
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability journal January 2013
Ultrafast Approximation for Phylogenetic Bootstrap journal February 2013
IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies journal November 2014
PartitionFinder 2: New Methods for Selecting Partitioned Models of Evolution for Molecular and Morphological Phylogenetic Analyses journal December 2016
SMS: Smart Model Selection in PhyML journal May 2017
MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform journal July 2002
Base-stacking and base-pairing contributions into thermal stability of the DNA double helix journal January 2006
ScanProsite: detection of PROSITE signature matches and ProRule-associated functional and structural residues in proteins journal July 2006
InterPro: the integrative protein signature database journal January 2009
Assessing the gene space in draft genomes journal November 2008
KEGG for integration and interpretation of large-scale molecular data sets journal November 2011
MycoCosm portal: gearing up for 1000 fungal genomes journal December 2013
Database resources of the National Center for Biotechnology Information journal November 2017
dbCAN2: a meta server for automated carbohydrate-active enzyme annotation journal May 2018
antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline journal April 2019
Tandem repeats lead to sequence assembly errors and impose multi-level challenges for genome and protein databases journal October 2019
New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0 journal March 2010
Survey of Branch Support Methods Demonstrates Accuracy, Power, and Robustness of Fast Likelihood-based Approximation Schemes journal May 2011
MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space journal February 2012
Comparative genomics of citric-acid-producing Aspergillus niger ATCC 1015 versus enzyme-producing CBS 513.88 journal May 2011
Aquatic adaptation of a laterally acquired pectin degradation pathway in marine gammaproteobacteria: Aquatic adaptation of a pectinolytic pathway journal April 2017
Fungal evolution: major ecological adaptations and evolutionary transitions journal April 2019
Bacteria in the cold deep-sea benthic boundary layer and sediment–water interface of the NE Atlantic journal August 2000
Towards a unified paradigm for sequence-based identification of fungi journal September 2013
Life with 6000 Genes journal October 1996
Biochemical Reconstruction of a Metabolic Pathway from a Marine Bacterium Reveals Its Mechanism of Pectin Depolymerization journal October 2018
Functional Characterization of MAT1-1-Specific Mating-Type Genes in the Homothallic Ascomycete Sordaria macrospora Provides New Insights into Essential and Nonessential Sexual Regulators journal April 2010
Nucleotide Composition of Nucleic Acids of Fungi II. Deoxyribonucleic Acids journal January 1966
Detection and Identification of Fungi Intimately Associated with the Brown Seaweed Fucus serratus journal February 2008
Species Richness and Adaptation of Marine Fungi from Deep-Subseafloor Sediments journal May 2015
Genome Sequence and Annotation of Acremonium chrysogenum , Producer of the β-Lactam Antibiotic Cephalosporin C journal October 2014
Antimicrobial Peptides Produced by Alkaliphilic Fungi Emericellopsis alkalina: Biosynthesis and Biological Activity Against Pathogenic Multidrug-Resistant Fungi journal March 2019
Studies of soil Fungi. Saturnomyces a new Genus of the Aspergillaceae journal January 1956
Combined influence of salinity and temperature ( Phoma -pattern) on growth of marine fungi journal October 1992
Phytase, a New Life for an “Old” Enzyme journal January 2013
Characterization of a Halotolerant Fungus from a Marine Sponge journal November 2019
Consistent mutational paths predict eukaryotic thermostability journal January 2013
Correction: Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi journal January 2014
A comprehensive evolutionary classification of proteins encoded in complete eukaryotic genomes journal January 2004
Homology to peptide pattern for annotation of carbohydrate-active enzymes and prediction of function journal April 2017
A multigene phylogeny toward a new phylogenetic classification of Leotiomycetes journal June 2019
Unambiguous identification of fungi: where do we stand and how accurate and precise is fungal DNA barcoding? journal July 2020
Setting scientific names at all taxonomic ranks in italics facilitates their quick recognition in scientific papers journal November 2020
Comparative Genome Analysis of Filamentous Fungi Reveals Gene Family Expansions Associated with Fungal Pathogenesis journal June 2008
Variation, Evolution, and Correlation Analysis of C+G Content and Genome or Chromosome Size in Different Kingdoms and Phyla journal February 2014
Evidence of a Putative Deep Sea Specific Microbiome in Marine Sponges journal March 2014
Matching the Diversity of Sulfated Biomolecules: Creation of a Classification Database for Sulfatases Reflecting Their Substrate Specificity journal October 2016
Characterization of lignocellulolytic activities from fungi isolated from the deep-sea sponge Stelletta normani journal March 2017
Biosynthesis of Antibiotic Leucinostatins in Bio-control Fungus Purpureocillium lilacinum and Their Inhibition on Phytophthora Revealed by Genome Mining journal July 2016
Morphological update on Calycina marina (Pezizellaceae, Helotiales, Leotiomycetes), a new combination for Laetinaevia marina journal January 2015
Distribution Of Hydrolysable Tannins In The Foliage Of Finnish Birch Species journal April 2002
Epigenetic Control of Phenotypic Plasticity in the Filamentous Fungus Neurospora crassa journal December 2016
The Effect of Temperature, pH, Light and Dark on the Growth of Fungi from Irish Coastal Waters journal March 1980
Relationship between chromosomal GC content and isoelectric points of histones in fungi journal January 2015
Fungal genome sequencing: basic biology to biotechnology journal February 2015
Acremonium phylogenetic overview and revision of Gliomastix, Sarocladium, and Trichothecium journal March 2011
Marine Polysaccharide Sulfatases journal January 2017
A Novel Enzyme Portfolio for Red Algal Polysaccharide Degradation in the Marine Bacterium Paraglaciecola hydrolytica S66T Encoded in a Sizeable Polysaccharide Utilization Locus journal May 2018
Biodiversity of Pigmented Fungi Isolated from Marine Environment in La Réunion Island, Indian Ocean: New Resources for Colored Metabolites journal July 2017
UV-Protective Compounds in Marine Organisms from the Southern Ocean journal September 2018
Marine Polysaccharides in Pharmaceutical Applications: Fucoidan and Chitosan as Key Players in the Drug Delivery Match Field journal November 2019
Advanced Technologies for the Extraction of Marine Brown Algal Polysaccharides journal March 2020
The Protean Acremonium. A. sclerotigenum/egyptiacum: Revision, Food Contaminant, and Human Disease journal August 2018
Update on Marine Carbohydrate Hydrolyzing Enzymes: Biotechnological Applications journal April 2018
A Novel Lipopeptaibol Emericellipsin A with Antimicrobial and Antitumor Activity Produced by the Extremophilic Fungus Emericellopsis alkalina journal October 2018
Diversity and physiology of marine lignicolous fungi in Arctic waters: a preliminary account journal December 2010
Anti-inflammatory effects of peptides from a marine algicolous fungus Acremonium sp. NTU492 in BV-2 microglial cells journal June 2020
Classification of Halophilic Heterotrophic Bacteria Thriving in the Jordanian Dead Sea Littoral Zone journal May 2012
Are alkalitolerant fungi of the Emericellopsis lineage (Bionectriaceae) of marine origin? journal November 2013
Zervamicins i and ii, Polypeptide Antibiotics Produced by Emericellopsis Salmosynnemata journal January 1974
Heptaibin, a Novel Antifungal Peptaibol Antibiotic from Emericellopsis sp. BAUA8289. journal January 2000