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Fungal secretome profile categorization of CAZymes by function and family corresponds to fungal phylogeny and taxonomy: Example Aspergillus and Penicillium.

ABSTRACT: Fungi secrete an array of carbohydrate-active enzymes (CAZymes), reflecting their specialized habitat-related substrate utilization. Despite its importance for fitness, enzyme secretome composition is not used in fungal classification, since an overarching relationship between CAZyme profiles and fungal phylogeny/taxonomy has not been established. For 465 Ascomycota and Basidiomycota genomes, we predicted CAZyme-secretomes, using a new peptide-based annotation method, Conserved-Unique-Peptide-Patterns, enabling functional prediction directly from sequence. We categorized each enzyme according to CAZy-family and predicted molecular function, hereby obtaining a list of "EC-Function;CAZy-Family" observations. These "Function;Family"-based secretome profiles were compared, using a Yule-dissimilarity scoring algorithm, giving equal consideration to the presence and absence of individual observations. Assessment of "Function;Family" enzyme profile relatedness (EPR) across 465 genomes partitioned Ascomycota from Basidiomycota placing Aspergillus and Penicillium among the Ascomycota. Analogously, we calculated CAZyme "Function;Family" profile-similarities among 95 Aspergillus and Penicillium species to form an alignment-free, EPR-based dendrogram. This revealed a stunning congruence between EPR categorization and phylogenetic/taxonomic grouping of the Aspergilli and Penicillia. Our analysis suggests EPR grouping of fungi to be defined both by "shared presence" and "shared absence" of CAZyme "Function;Family" observations. This finding indicates that CAZymes-secretome evolution is an integral part of fungal speciation, supporting integration of cladogenesis and anagenesis.

SUBMITTER: Barrett K

PROVIDER: S-EPMC7083838 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Aspergillus, Penicillium and Talaromyces are diverse, phenotypically polythetic genera encompassing species important to the environment, economy, biotechnology and medicine, causing significant social impacts. Taxonomic studies on these fungi are essential since they could provide invaluable information on their evolutionary relationships and define criteria for species recognition. With the advancement of various biological, biochemical and computational technologies, different approaches have been adopted for the taxonomy of Aspergillus, Penicillium and Talaromyces; for example, from traditional morphotyping, phenotyping to chemotyping (e.g. lipotyping, proteotypingand metabolotyping) and then mitogenotyping and/or phylotyping. Since different taxonomic approaches focus on different sets of characters of the organisms, various classification and identification schemes would result. In view of this, the consolidated species concept, which takes into account different types of characters, is recently accepted for taxonomic purposes and, together with the lately implemented 'One Fungus - One Name' policy, is expected to bring a more stable taxonomy for Aspergillus, Penicillium and Talaromyces, which could facilitate their evolutionary studies. The most significant taxonomic change for the three genera was the transfer of Penicillium subgenus Biverticillium to Talaromyces (e.g. the medically important thermally dimorphic 'P. marneffei' endemic in Southeast Asia is now named T. marneffei), leaving both Penicillium and Talaromyces as monophyletic genera. Several distantly related Aspergillus-like fungi were also segregated from Aspergillus, making this genus, containing members of both sexual and asexual morphs, monophyletic as well. In the current omics era, application of various state-of-the-art omics technologies is likely to provide comprehensive information on the evolution of Aspergillus, Penicillium and Talaromyces and a stable taxonomy will hopefully be achieved.

Project description:Species of Penicillium section Citrina have a worldwide distribution and occur commonly in soils. The section is here delimited using a combination of phenotypic characters and sequences of the nuclear ribosomal RNA gene operon, including the internal transcribed spacer regions ITS1 and ITS2, the 5.8S nrDNA (ITS) and partial RPB2 sequences. Species assigned to section Citrina share the production of symmetrically biverticillate conidiophores, flask shaped phialides (7.0-9.0 μm long) and relatively small conidia (2.0-3.0 μm diam). Some species can produce greyish-brown coloured cleistothecia containing flanged ascospores. In the present study, more than 250 isolates presumably belonging to section Citrina were examined using a combined analysis of phenotypic and physiological characters, extrolite profiles and ITS, β-tubulin and/or calmodulin sequences. Section Citrina includes 39 species, and 17 of those are described here as new. The most important phenotypic characters for distinguishing species are growth rates and colony reverse colours on the agar media CYA, MEA and YES; shape, size and ornamentation of conidia and the production of sclerotia or cleistothecia. Temperature-growth profiles were made for all examined species and are a valuable character characters for species identification. Species centered around P. citrinum generally have a higher maximum growth temperature (33-36 °C) than species related to P. westlingii (27-33 °C). Extrolite patterns and partial calmodulin and β-tubulin sequences can be used for sequence based identification and resolved all species. In contrast, ITS sequences were less variable and only 55 % of the species could be unambiguously identified with this locus.Taxonomic noveltiesPenicillium argentinense Houbraken, Frisvad & Samson, P. atrofulvum Houbraken, Frisvad & Samson, P. aurantiacobrunneum Houbraken, Frisvad & Samson, P. cairnsense Houbraken, Frisvad & Samson, P. christenseniae Houbraken, Frisvad & Samson, P. copticola Houbraken, Frisvad & Samson, P. cosmopolitanum Houbraken, Frisvad & Samson, P. neomiczynskii Cole, Houbraken, Frisvad & Samson, P. nothofagi Houbraken, Frisvad & Samson, P. pancosmium Houbraken, Frisvad & Samson, P. pasqualense Houbraken, Frisvad & Samson, P. quebecense Seifert, Houbraken, Frisvad & Samson, P. raphiae Houbraken, Frisvad & Samson, P. terrigenum Seifert, Houbraken, Frisvad & Samson, P. ubiquetum Houbraken, Frisvad & Samson, P. vancouverense Houbraken, Frisvad & Samson, P. wellingtonense Cole, Houbraken, Frisvad & Samson.

Dataset Information

Fungal secretome profile categorization of CAZymes by function and family corresponds to fungal phylogeny and taxonomy: Example Aspergillus and Penicillium.

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