Neriman Yilmaz

Phylogeny and nomenclature of the genus Talaromyces and taxa accommodated in Penicillium subgenus Biverticillium

The taxonomic history of anamorphic species attributed to Penicillium subgenus Biverticillium is reviewed, along with evidence supporting their relationship with teleomorphic species classified in Talaromyces. To supplement previous conclusions based on ITS, SSU and/or LSU sequencing that Talaromyces and subgenus Biverticillium comprise a monophyletic group that is distinct from Penicillium at the generic level, the phylogenetic relationships of these two groups with other genera of Trichocomaceae was further studied by sequencing a part of the RPB1 (RNA polymerase II largest subunit) gene. Talaromyces species and most species of Penicillium subgenus Biverticillium sensu Pitt reside in a monophyletic clade distant from species of other subgenera of Penicillium. For detailed phylogenetic analysis of species relationships, the ITS region (incl. 5.8S nrDNA) was sequenced for the available type strains and/or representative isolates of Talaromyces and related biverticillate anamorphic species. Extrolite profiles were compiled for all type strains and many supplementary cultures. All evidence supports our conclusions that Penicillium subgenus Biverticillium is distinct from other subgenera in Penicillium and should be taxonomically unified with the Talaromyces species that reside in the same clade. Following the concepts of nomenclatural priority and single name nomenclature, we transfer all accepted species of Penicillium subgenus Biverticillium to Talaromyces. A holomorphic generic diagnosis for the expanded concept of Talaromyces, including teleomorph and anamorph characters, is provided. A list of accepted Talaromyces names and newly combined Penicillium names is given. Species of biotechnological and medical importance, such as P. funiculosum and P. marneffei, are now combined in Talaromyces. Excluded species and taxa that need further taxonomic study are discussed. An appendix lists other generic names, usually considered synonyms of Penicillium sensu lato that were considered prior to our adoption of the name Talaromyces. Taxonomic novelties: Taxonomic novelties: New species – Talaromyces apiculatus Samson, Yilmaz & Frisvad, sp. nov. New combinations and names – Talaromyces aculeatus (Raper & Fennell) Samson, Yilmaz, Frisvad & Seifert, T. albobiverticillius (H.-M. Hsieh, Y.-M. Ju & S.-Y. Hsieh) Samson, Yilmaz, Frisvad & Seifert, T. allahabadensis (B.S. Mehrotra & D. Kumar) Samson, Yilmaz & Frisvad, T. aurantiacus (J.H. Mill., Giddens & A.A. Foster) Samson, Yilmaz, & Frisvad, T. boninensis (Yaguchi & Udagawa) Samson, Yilmaz, & Frisvad, T. brunneus (Udagawa) Samson, Yilmaz & Frisvad, T. calidicanius (J.L. Chen) Samson, Yilmaz & Frisvad, T. cecidicola (Seifert, Hoekstra & Frisvad) Samson, Yilmaz, Frisvad & Seifert, T. coalescens (Quintan.) Samson, Yilmaz & Frisvad, T. dendriticus (Pitt) Samson, Yilmaz, Frisvad & Seifert, T. diversus (Raper & Fennell) Samson, Yilmaz & Frisvad, T. duclauxii (Delacr.) Samson, Yilmaz, Frisvad & Seifert, T. echinosporus (Nehira) Samson, Yilmaz & Frisvad, comb. nov. T. erythromellis (A.D. Hocking) Samson, Yilmaz, Frisvad & Seifert, T. funiculosus (Thom) Samson, Yilmaz, Frisvad & Seifert, T. islandicus (Sopp) Samson, Yilmaz, Frisvad & Seifert, T. loliensis (Pitt) Samson, Yilmaz & Frisvad, T. marneffei (Segretain, Capponi & Sureau) Samson, Yilmaz, Frisvad & Seifert, T. minioluteus (Dierckx) Samson, Yilmaz, Frisvad & Seifert, T. palmae (Samson, Stolk & Frisvad) Samson, Yilmaz, Frisvad & Seifert, T. panamensis (Samson, Stolk & Frisvad) Samson, Yilmaz, Frisvad & Seifert, T. paucisporus (Yaguchi, Someya & Udagawa) Samson & Houbraken T. phialosporus (Udagawa) Samson, Yilmaz & Frisvad, T. piceus (Raper & Fennell) Samson, Yilmaz, Frisvad & Seifert, T. pinophilus (Hedgcock) Samson, Yilmaz, Frisvad & Seifert, T. pittii (Quintan.) Samson, Yilmaz, Frisvad & Seifert, T. primulinus (Pitt) Samson, Yilmaz & Frisvad, T. proteolyticus (Kamyschko) Samson, Yilmaz & Frisvad, T. pseudostromaticus (Hodges, G.M. Warner, Rogerson) Samson, Yilmaz, Frisvad & Seifert, T. purpurogenus (Stoll) Samson, Yilmaz, Frisvad & Seifert, T. rademirici (Quintan.) Samson, Yilmaz & Frisvad, T. radicus (A.D. Hocking & Whitelaw) Samson, Yilmaz, Frisvad & Seifert, T. ramulosus (Visagie & K. Jacobs) Samson, Yilmaz, Frisvad & Seifert, T. rubicundus (J.H. Mill., Giddens & A.A. Foster) Samson, Yilmaz, Frisvad & Seifert, T. rugulosus (Thom) Samson, Yilmaz, Frisvad & Seifert, T. sabulosus (Pitt & A.D. Hocking) Samson, Yilmaz & Frisvad, T. siamensis (Manoch & C. Ramírez) Samson, Yilmaz & Frisvad, T. sublevisporus (Yaguchi & Udagawa) Samson, Yilmaz & Frisvad, T. variabilis (Sopp) Samson, Yilmaz, Frisvad & Seifert, T. varians (G. Sm.) Samson, Yilmaz & Frisvad, T. verruculosus (Peyronel) Samson, Yilmaz, Frisvad & Seifert, T. viridulus Samson, Yilmaz & Frisvad.

Polyphasic taxonomy of the genus Talaromyces

The genus Talaromyces was described by Benjamin in 1955 as a sexual state of Penicillium that produces soft walled ascomata covered with interwoven hyphae. Phylogenetic information revealed that Penicillium subgenus Biverticillium and Talaromyces form a monophyletic clade distinct from the other Penicillium subgenera. Subsequently, in combination with the recent adoption of the one fungus one name concept, Penicillium subgenus Biverticillium was transferred to Talaromyces. At the time, the new combinations were made based only on phylogenetic information. As such, the aim of this study was to provide a monograph on Talaromyces applying a polyphasic species concept, including morphological, molecular and physiological characters. Based on an ITS, BenA and RPB2 multigene phylogeny, we propose a new sectional classification for the genus, placing the 88 accepted species into seven sections, named sections Bacillispori, Helici, Islandici, Purpurei, Subinflati, Talaromyces and Trachyspermi. We provide morphological descriptions for each of these species, as well as notes on their identification using morphology and DNA sequences. For molecular identification, BenA is proposed as a secondary molecular marker to the accepted ITS barcode for fungi.

Ochratoxin production and taxonomy of the yellow aspergilli (Aspergillus section Circumdati)

Aspergillus section Circumdati or the Aspergillus ochraceus group, includes species with rough walled stipes, biseriate conidial heads, yellow to ochre conidia and sclerotia that do not turn black. Several species are able to produce mycotoxins including ochratoxins, penicillic acids, and xanthomegnins. Some species also produce drug lead candidates such as the notoamides. A polyphasic approach was applied using morphological characters, extrolite data and partial calmodulin, β-tubulin and ITS sequences to examine the evolutionary relationships within this section. Based on this approach the section Circumdati is revised and 27 species are accepted, introducing seven new species: A. occultus, A. pallidofulvus, A. pulvericola, A. salwaensis, A. sesamicola, A. subramanianii and A. westlandensis. In addition we correctly apply the name A. fresenii (≡ A. sulphureus (nom. illeg.)). A guide for the identification of these 27 species is provided. These new species can be distinguished from others based on morphological characters, sequence data and extrolite profiles. The previously described A. onikii and A. petrakii were found to be conspecific with A. ochraceus, whilst A. flocculosus is tentatively synonymised with A. ochraceopetaliformis, despite extrolite differences between the two species. Based on the extrolite data, 13 species of section Circumdati produce large amounts of ochratoxin A: A. affinis, A. cretensis, A. fresenii, A. muricatus, A. occultus, A. ochraceopetaliformis (A. flocculosus), A. ochraceus, A. pseudoelegans, A. pulvericola, A. roseoglobulosus, A. sclerotiorum, A. steynii and A. westerdijkiae. Seven additional species produce ochratoxin A inconsistently and/or in trace amounts: A. melleus, A. ostianus, A. persii, A. salwaensis, A. sesamicola, A. subramanianii and A. westlandensis. The most important species regarding potential ochratoxin A contamination in agricultural products are A. ochraceus, A. steynii and A. westerdijkiae.

Talaromyces atroroseus, a new species efficiently producing industrially relevant red pigments

Some species of Talaromyces secrete large amounts of red pigments. Literature has linked this character to species such as Talaromyces purpurogenus, T. albobiverticillius, T. marneffei, and T. minioluteus often under earlier Penicillium names. Isolates identified as T. purpurogenus have been reported to be interesting industrially and they can produce extracellular enzymes and red pigments, but they can also produce mycotoxins such as rubratoxin A and B and luteoskyrin. Production of mycotoxins limits the use of isolates of a particular species in biotechnology. Talaromyces atroroseus sp. nov., described in this study, produces the azaphilone biosynthetic families mitorubrins and Monascus pigments without any production of mycotoxins. Within the red pigment producing clade, T. atroroseus resolved in a distinct clade separate from all the other species in multigene phylogenies (ITS, β-tubulin and RPB1), which confirm its unique nature. Talaromyces atroroseus resembles T. purpurogenus and T. albobiverticillius in producing red diffusible pigments, but differs from the latter two species by the production of glauconic acid, purpuride and ZG–1494α and by the dull to dark green, thick walled ellipsoidal conidia produced. The type strain of Talaromyces atroroseus is CBS 133442

Delimitation and characterisation of Talaromyces purpurogenus and related species.

Taxa of the Talaromyces purpurogenus complex were studied using a polyphasic approach. ITS barcodes were used to show relationships between species of the T. purpurogenus complex and other Talaromyces species. RPB1, RPB2, β-tubulin and calmodulin sequences were used to delimit phylogenetic species in the complex. These data, combined with phenotypic characters, showed that the complex contains four species: T. purpurogenus, T. ruber comb. nov. and two new species T. amestolkiae sp. nov. and T. stollii sp. nov. The latter three species belong to the same clade and T. purpurogenus is located in a phylogenetic distant clade. The four species all share similar conidiophore morphologies, but can be distinguished by macromorphological characters. Talaromyces ruber has a very distinct colony texture on malt extract agar (MEA), produces bright yellow and red mycelium on yeast extract sucrose agar (YES) and does not produce acid on creatine sucrose agar (CREA). In contrast, T. amestolkiae and T. stollii produce acid on CREA. These two species can be differentiated by the slower growth rate of T. amestolkiae on CYA incubated at 36 °C. Furthermore, T. stollii produces soft synnemata-like structures in the centre of colonies on most media. Extrolite analysis confirms the distinction of four species in the T. purpurogenus complex. The red diffusing pigment in T. purpurogenus is a mixture of the azaphilone extrolites also found in Monascus species, including N-glutarylrubropunctamine and rubropunctatin. Talaromyces purpurogenus produced four different kinds of mycotoxins: rubratoxins, luteoskyrin, spiculisporic acid and rugulovasins and these mycotoxins were not detected in the other three species.

A taxonomic and phylogenetic revision of Penicillium section Aspergilloides.

Species belonging to Penicillium section Aspergilloides have a world-wide distribution with P. glabrum, P. spinulosum and P. thomii the most well-known species of this section. These species occur commonly and can be isolated from many substrates including soil, food, bark and indoor environments. The taxonomy of these species has been investigated several times using various techniques, but species delimitation remains difficult. In the present study, 349 strains belonging to section Aspergilloides were subjected to multilocus molecular phylogenetic analyses using partial β-tubulin (BenA), calmodulin (CaM) and RNA polymerase II second largest subunit (RPB2) sequences. Section Aspergilloides is subdivided into 12 clades and 51 species. Twenty-five species are described here as new and P. yezoense, a species originally described without a Latin diagnosis, is validated. Species belonging to section Aspergilloides are phenotypically similar and most have monoverticillate conidiophores and grow moderately or quickly on agar media. The most important characters to distinguish these species were colony sizes on agar media, growth at 30 °C, ornamentation and shape of conidia, sclerotium production and stipe roughness.

Taxonomic re-evaluation of species in Talaromyces section Islandici, using a polyphasic approach

The taxonomy of Talaromyces rugulosus, T. wortmannii and closely related species, classified in Talaromyces sect. Islandici, is reviewed in this paper. The species of Talaromyces sect. Islandici have restricted growth on MEA and CYA, generally have yellow mycelia and produce rugulosin and/or skyrin. They are important in biotechnology (e.g. T. rugulosus, T. wortmannii) and in medicine (e.g. T. piceus, T. radicus). The taxonomy of sect. Islandici was resolved using a combination of morphological, extrolite and phylogenetic data, using the Genealogical Concordance Phylogenetic Species Recognition (GCPSR) concept, with special focus on the T. rugulosus and T. wortmannii species complexes. In this paper, we synonymise T. variabilis, Penicillium concavorugulosum and T. sublevisporus with T. wortmannii, and introduce four new species as T. acaricola, T. crassus, T. infraolivaceus and T. subaurantiacus. Finally, we provide a synoptic table for the identification of the 19 species classified in the section.

Phylogeny of xerophilic aspergilli (subgenus Aspergillus) and taxonomic revision of section Restricti

Aspergillus section Restricti together with sister section Aspergillus (formerly Eurotium) comprises xerophilic species, that are able to grow on substrates with low water activity and in extreme environments. We adressed the monophyly of both sections within subgenus Aspergillus and applied a multidisciplinary approach for definition of species boundaries in sect. Restricti. The monophyly of sections Aspergillus and Restricti was tested on a set of 102 isolates comprising all currently accepted species and was strongly supported by Maximum likelihood (ML) and Bayesian inferrence (BI) analysis based on β-tubulin (benA), calmodulin (CaM) and RNA polymerase II second largest subunit (RPB2) loci. More than 300 strains belonging to sect. Restricti from various isolation sources and four continents were characterized by DNA sequencing, and 193 isolates were selected for phylogenetic analyses and phenotypic studies. Species delimitation methods based on multispecies coalescent model were employed on DNA sequences from four loci, i.e., ID region of rDNA (ITS + 28S), CaM, benA and RPB2, and supported recognition of 21 species, including 14 new. All these species were also strongly supported in ML and BI analyses. All recognised species can be reliably identified by all four examined genetic loci. Phenotype analysis was performed to support the delimitation of new species and includes colony characteristics on seven cultivation media incubated at several temperatures, growth on an osmotic gradient (six media with NaCl concentration from 0 to 25 %) and analysis of morphology including scanning electron microscopy. The micromorphology of conidial heads, vesicle dimensions, temperature profiles and growth parameters in osmotic gradient were useful criteria for species identification. The vast majority of species in sect. Restricti produce asperglaucide, asperphenamate or both in contrast to species in sect. Aspergillus. Mycophenolic acid was detected for the first time in at least six members of the section. The ascomata of A. halophilicus do not contain auroglaucin, epiheveadride or flavoglaucin which are common in sect. Aspergillus, but shares the echinulins with sect. Aspergillus.

Four novel Talaromyces species isolated from leaf litter from Colombian Amazon rain forests

Various Talaromyces strains were isolated during a survey of fungi involved in leaf litter decomposition in tropical lowland forests in the Caquetá and Amacayacu areas of the Colombian Amazon. Four new Talaromyces species are described using a polyphasic approach, which includes phenotypic characters, extrolite profiles and phylogenetic analysis of the internal transcribed spacer region (ITS) barcode, and beta-tubulin (BenA) and calmodulin (CaM) gene regions. Talaromyces amazonensis sp. nov., T. francoae sp. nov. and T. purgamentorum sp. nov. belong to Talaromyces section Talaromyces, and T. columbiensis sp. nov. is located in section Bacillispori. The new species produce several bioactive compounds: T. amazonensis produces the potential anticancer agents duclauxin, berkelic acid and vermicillin, and T. columbiensis produces the effective anticancer agent wortmannin (together with duclauxin). In addition to the new species, T. aculeatus and T. macrosporus were isolated during this study on leaf litter decomposition.

Taxonomic annotation of public fungal ITS sequences from the built environment – a report from an April 10–11, 2017 workshop (Aberdeen, UK)

Abstract Recent DNA-based studies have shown that the built environment is surprisingly rich in fungi. These indoor fungi – whether transient visitors or more persistent residents – may hold clues to the rising levels of human allergies and other medical and building-related health problems observed globally. The taxonomic identity of these fungi is crucial in such pursuits. Molecular identification of the built mycobiome is no trivial undertaking, however, given the large number of unidentified, misidentified, and technically compromised fungal sequences in public sequence databases. In addition, the sequence metadata required to make informed taxonomic decisions – such as country and host/substrate of collection – are often lacking even from reference and ex-type sequences. Here we report on a taxonomic annotation workshop (April 10–11, 2017) organized at the James Hutton Institute/University of Aberdeen (UK) to facilitate reproducible studies of the built mycobiome. The 32 participants went through public fungal ITS barcode sequences related to the built mycobiome for taxonomic and nomenclatural correctness, technical quality, and metadata availability. A total of 19,508 changes – including 4,783 name changes, 14,121 metadata annotations, and the removal of 99 technically compromised sequences – were implemented in the UNITE database for molecular identification of fungi (https://unite.ut.ee/) and shared with a range of other databases and downstream resources. Among the genera that saw the largest number of changes were Penicillium, Talaromyces, Cladosporium, Acremonium, and Alternaria, all of them of significant importance in both culture-based and culture-independent surveys of the built environment.