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Persoonia : Molecular Phylogeny and Evolution of Fungi logoLink to Persoonia : Molecular Phylogeny and Evolution of Fungi
. 2012 Nov 12;29:39–54. doi: 10.3767/003158512X659500

Delimitation and characterisation of Talaromyces purpurogenus and related species

N Yilmaz 1,5, J Houbraken 1, ES Hoekstra 2, JC Frisvad 3, CM Visagie 1,4, RA Samson 1
PMCID: PMC3589794  PMID: 23606764

Abstract

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.

Keywords: Penicillium purpurogenum, rubratoxin, polyphasic taxonomy

INTRODUCTION

Penicillium purpurogenum was described by Stoll (1903–1904) and the type culture (CBS 286.36) was isolated as a culture contaminant of Aspergillus oryzae in Japan. This species was characterised by dark grey-green colonies with mycelium varying from pinkish to yellow and yellow red, as well as the production of red pigments on potato agar. In the same paper, Stoll (1903–1904) also described P. rubrum and this isolate was provided by Grassberger, who authorised Stoll to describe the species. It was characterised by dark-green colonies on sugar-gelatine agar. The culture Stoll used for his description is no longer available and therefore it was re-described by Raper & Thom (1949) based on strains NRRL 1062 (CBS 370.48) and NRRL 2120. According to Raper & Thom’s concept, P. purpurogenum forms spreading dark yellow-green colonies with rough-walled conidia while P. rubrum produces more restricted grey-green colonies with smooth-walled conidia. Pitt (1980) used a broader species concept for P. purpurogenum and considered the differences proposed by Raper & Thom (1949) to distinguish P. purpurogenum from P. rubrum to be insignificant. He also considered P. crateriforme to be conspecific with P. purpurogenum based on the red pigments produced and its ability to grow at 37 °C, and based on the original descriptions he also considered P. sanguineum and P. vanilliae synonyms (Pitt 1980).

Both P. purpurogenum and P. rubrum are claimed to produce rubratoxins (Wilson & Wilson 1962, Moss et al. 1968, Natori et al. 1970). Because P. rubrum was not accepted by Pitt (1980) and P. purpurogenum has been regarded as a producer of glauconic acid rather than rubratoxins, Frisvad (1989) considered P. crateriforme to be the correct name for the species producing rubratoxins. Rubratoxin B is mutagenic, hepatotoxic, nephrotoxic and splenotoxic to several animals (Burnside et al. 1957, Lockard et al. 1981, Surjono et al. 1985, Engelhardt et al. 1987, Kihara et al. 2001). The first human rubratoxicosis was reported by Richer et al. (1997). Three teens drinking homemade rhubarb wine, which had a high level of rubratoxin B became critically ill, with one requiring immediate liver transplant. Even though rubratoxin B has negative health effects, it has potential as an anti-tumor agent (Wang et al. 2007, Wada et al. 2010). Penicillium crateriforme has also been reported to produce the mouse mycotoxin spiculisporic acid (Oxford & Raistrick 1934, Fujimoto et al. 1988). Later, spiculisporic acid has been used as a commercially available biosurfactant (Ishigami et al. 2000). Isolates belonging to P. crateriforme also produces the clavine alkaloids rugulovasines A and B and chlororugulovasines A & B (Dorner et al. 1980, the producer ATCC 44445 was identified as P. rubrum) (see Table 2). Penicillium purpurogenum is an important species in biotechnology for its ability to produce enzymes such as xylanases and cellulases (Steiner et al. 1994, Belancic et al. 1995) and pigments, which are used as natural colorants and biosorption (Say et al. 2004, Mapari et al. 2009, Jeya et al. 2010, Zou et al. 2012). Penicillium purpurogenum inoculated oak chips are used in artificial aging of Italian wines (Petruzzi et al. 2010, 2012).

Benjamin (1955) introduced the name Talaromyces as a sexual morph and this genus was characterised as producing soft yellow ascomata that consist of interwoven hyphae. Following the concept of single name nomenclature, 40 species from Penicillium subg. Biverticillium were transferred and combined into Talaromyces (Samson et al. 2011). The morphologically circumscribed species Penicillium purpurogenum sensu Pitt (1980) is one of several complexes of cryptic phylogenetic species that occur in the genus.

In the current study, the T. purpurogenus species complex was revised based on a polyphasic approach incorporating macro- and micro-morphology, extrolite production and multi-gene derived phylogeny. The phylogenetic relationships between species of the T. purpurogenus complex and other members of Talaromyces are studied using ITS barcodes. For the detailed delimitation of phylogenetic species, sequences of four alternative genes, β-tubulin, calmodulin, RPB1 and RPB2, were used.

MATERIALS AND METHODS

Strains

Cultures used for comparisons in this study were obtained from the culture collections of the CBS-KNAW Fungal Biodiversity Centre, Utrecht, the Netherlands, the IBT culture collection, Lyngby, Denmark and fresh isolates deposited in the working collection of the Department of Applied and Industrial Mycology (DTO), housed at CBS. Strains studied are listed in Table 1.

Table 1.

Talaromyces strains used in this study.

Species CBS no. Other numbers Substrate and locality ITS β-tubulin calmodulin RPB1 RPB2
T. amestolkiae DTO 173F3 Soil; Indonesia JX965223 JX965330 JX965189 JX965248
FRR 1097 Chicken feed suspected to be toxic; Victoria, Australia
IBT 20202 Greenhouse; Lyngby, Denmark
IMI 061385 = KCTC 6774 = IBT 4538 Paper pulp; UK, 1955
IMI 104624 = IBT 3968 Plastic; UK, 1963
IMI 147406 = KCTC 6773 = IBT 21723 Malus pumila; Belfast, North Ireland, UK, 1970
IBT 19715 Air, cake factory; Denmark
IBT 23821 Soil; Scafati, Italy
IBT 29986 Contaminant of agar plate; Denmark
252.31 NRRL 1034 Narcissus bulb; the Netherlands JX315668 JX315624 JX315654 JX315687 JX315706
263.93 Bronchoalveolar lavage of immunocompetent female patient with pneumonia by Nocardia JX315669 JX315625 JX315653 JX315688 JX315707
264.93 Bronchoalveolar lavage of male AIDS-patient; New Caledonia JX965247 JX965331 JX965196 JX965284 JX965319
274.95 Sculpture in castle Troja; Prague, Czech Republic JX965214 JX965321 JX965190 JX965249 JX965285
277.95 AK 128/94 = AK 188/94 Soil; Chvaletice, Czech Republic JX965215 JX965322 JX965191 JX965250 JX965286
329.481 ATCC 10445 = ATCC 8725 = CCTM 3641= CECT 2913 = DSM 2213 = IFO 5857 = IHEM 4008 = IMI 034912 = NRRL 1032a= QM 7562 Air contaminant; Washington DC, USA JX965216 JX965323 JX965192 JX965251 JX965287
353.93 DAOM 31954 = DSM 1184 Angiosperm wood; Ontario, Canada JX315672 JX315626 JX315652 JX315691 JX315710
365.482 ATCC 10486 = IMI 040035 = NRRL 1066= QM 1960
Unknown source; USA JX965217 JX965324 JX965193 JX965252 JX965288
379.97 Sputum; Leiden, the Netherlands JX965218 JX965325 JX965198 JX965253 JX965289
390.96 Contaminant of Coniothyrium minitans; Italy JX965219 JX965326 JX965194 JX965254 JX965290
433.62 Ground domestic waste; Verona, Italy JX965220 JX965327 JX965195 JX965255 JX965291
436.62 Alum solution; unknown origin JX965221 JX965328 JX965197 JX965256 JX965292
626.93 Ananas camosus cultivar; Martinique JX965329 JX965257
884.72 Manure; France JX315678 JX315622 JX315651 JX315697 JX315716
101305 Soil; Hong Kong, China JX965224 JX965332 JX965259 JX965293
101349 Soil; Hong Kong, China JX965225 JX965333 JX965260 JX965294
102303 Raw coffee beans; unknown origin JX965334
102689 Air; Japan JX965226 JX965335 JX965261 JX965295
113143 IMI 079195 = NRRL 1132 Contaminant of culture; Washington DC, USA, 1940
132695 DTO 189C1 = IBT 23485 Wheat; Italy JX965228 JX965338 JX965199 JX965262 JX965297
132696┬ DTO 179F5 Ex-type strain of Talaromyces amestolkiae. House dust; South Africa JX315660 JX315623 JX315650 JX315679 JX315698
132697 DTO 189D1 = IBT 28795 Coffee cherries; Uganda JX965227 JX965337 JX965296
132698 DTO 189B5 = IBT 20197 Greenhouse; Lyngby, Denmark JX965229 JX965336 JX965263 JX965298
T. purpurogenus DTO 173E6 Soil; Indonesia JX965230 JX965339 JX965264 JX965299
189B4 = IBT 18380; CCRC 32601 Dung of pig; Taipei City, Taiwan JX965231 JX965340 JX965265 JX965300
193H1 = IBT 12779 Oregano; imported to Denmark JX965232 JX965342 JX965266 JX965302
193H5 = IBT 3933 JX965233 JX965341 JX965267 JX965301
184.27 FRR 1047 = IMI 094165 = LSHB P154 = Ex-type of Penicillium crateriforme. Soil; Louisiana, USA JX315665 JX315637 JX315658 JX315684 JX315703
MUCL 29224 = ATCC 52215 = NRRL 1057 = KCTC 6784 = Thom 4894.13
286.36┬ IMI 091926 = CECT 20441 = KCTC 6821= LSHB P.48 = NCTC 586 = Thom 17 Ex-type strain of Talaromyces purpurogenus. Parasitic on a culture of Aspergillus oryzae; Japan JX315671 JX315639 JX315655 JX315690 JX315709
108923 Sputum; Leiden, Netherlands JX965236 JX965343 JX965200 JX965268 JX965303
113158 ATCC 20204 = IBT 4183 = IFO 5722 Unknown source; Japan JX965235 JX965344 JX965201 JX965269 JX965304
113161 IBT 11628 Wheat; Winnipeg, Canada JX965234 JX965345 JX965202 JX965270 JX965307
122411 IBT 17430 = DTO 49F6 JX965346 JX965305
132707 IMI 136128 = MR 008 = IBT 3658 = IBT 5015 = DTO 189A1 Mould field corn; Wisconsin, USA JX315661 JX315638 JX315642 JX315680 JX315699
1019653 Unknown source JX965237 JX965347 JX965306
1224344 DTO 49F7 = DTO 189 A4 = IBT 10612 = IBT 3560 = CCRC 31681 = BCRC 31681 = NCIM 762 = NRRL 1059 = ATCC 10064 = Thom 5694.11 Unknown source. Identified as Penicillium purpurogenum by Raper & Thom (1949); collected as Penicillium sanguineum by CBS JX315663 JX315640 JX315659 JX315682 JX315701
T. ruber DTO 189A7 = IBT 13594 = DAOM 215356 Soil in forest; Canada JX965238 JX965348 JX965203 JX965271 JX965308
FRR 1503 = ATCC 48975 = IAM 13746 Weathered preserved wood stakes; North Queensland, Australia.
NRRL 1180 = IBT 3940 Unknown source; USA
195.88 NRRL 1159 = IBT 4423 Chickens in cold storage; unknown JX965240 JX965350 JX965204 JX965273 JX965310
196.88 FRR 1714 = IBT 3951 Unknown JX315666 JX315627 JX315657 JX315685 JX315704
237.93 ACC 828-81 Unknown JX315667 JX315628 JX315656 JX315686 JX315705
368.73 Unknown JX965351 JX965274
370.485 ATCC 10520 = IMI 040036 = NRRL 1062= VKM F-345 = IBT 4431 = IBT 3927 Ex-neotype. Currency paper; Washington, USA JX315673 JX315630 JX315649 JX315692 JX315711
868.96 Tracheal secretion; Heidelberg, Germany JX315677 JX315631 JX315643 JX315696 JX315715
101144 IMI 178519 = IBT 10708 Ex experimental paint sample; Woolwich, UK JX965239 JX965272 JX965309
113140 DTO 193 H7 = IBT 19712 Air cake factory; Denmark JX965241 JX965352 JX965205 JX965275 JX965311
132699 DTO 189B7 = IBT 21772 Ex sandy soil; Marhaba Club Beach, Souse, Tunesia JX965242 JX965353 JX965206 JX965276 JX965312
132700 DTO 173G7 Soil; Indonesia JX965243 JX965354 JX965207 JX965277 JX965313
132703 DTO 193I3 = IBT 10708 = IMI 170519 Ex experimental paint sample; Woolwich, UK JX965314
132704NT DTO 193H6 = IBT 10703 = CBS 113137 Aircraft fuel tank; UK JX315662 JX315629 JX315641 JX315681 JX315700
T. stollii 169.916 NRRL 1033 Unknown substrate; South Africa identified as Penicillium funiculosum by Raper & Thom (1949) JX315664 JX315634 JX315647 JX315683 JX315702
265.93 Bronchoalveolar lavage of patient after lung transplantation (subclinical); France JX315670 JX315635 JX315648 JX315689 JX315708
372.877 Faeces of a woman; Hamburg JX965244 JX965355
408.93┬ Ex-type strain of Talaromyces stollii. AIDS patient; the Netherlands JX315674 JX315633 JX315646 JX315693 JX315712
581.94 Unknown JX315675 JX315632 JX315645 JX315694 JX315713
582.94 Unknown JX965245 JX965356 JX965208 JX965278
624.93 Ananas camosus cultivar; Martinique JX315676 JX315636 JX315644 JX315695 JX315714
625.93 Ananas camosus cultivar; Martinique JX965360 JX965211 JX965279 JX965316
100372 Pineapple; location unknown JX965357 JX965210 JX965282 JX965317
132705 DTO 172F7 Soil; Indonesia JX965358 JX965212 JX965280 JX965318
132706 DTO 28C1 Indoor air from bakery; Avenhorn, the Netherlands JX965246 JX965359 JX965213 JX965283 JX965320
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1 NRRL 1032a was identified as Penicillium funiculosum by Raper & Thom (1949).

2 Identified as Penicillium purpurogenum var. rubisclerotiorum by Raper & Thom (1949). It produced limited numbers of dark red sclerotia.

3 The isolate was sent to CBS by S. Ochiai, Jonquil Consulting Inc., Tokyo, Japan.

4 Raper & Thom (1949) reported faster growth and floccose margins for this strain. Pitt (1980) does not mention this strain.

5 NRRL 1062 was used by Raper & Thom (1949) to describe Penicillium rubrum.

6 NRRL 1033 was identified as Penicillium funiculosum by Raper & Thom (1949).

7 Identified as Penicillium dendriticum. The isolate was received from Dr E. Dollefeld, Hamburg.

Morphological analysis

Macroscopic characters were studied on Czapek yeast extract agar (CYA), CYA supplemented with 5 % NaCl (CYAS), yeast extract sucrose agar (YES), creatine sucrose agar (CREA), dichloran 18 % glycerol agar (DG18), oatmeal agar (OA) and malt extract agar (Oxoid) (MEA). The strains were inoculated at three points on 90-mm Petri dishes and incubated for 7 d at 25 °C in darkness. All media were prepared as described by Samson et al. (2010). The temperature-growth response of strains was studied on CYA. Strains were inoculated at 3 points and incubated at 6, 9, 12, 15, 18, 21, 24, 27, 30, 33, 36 and 40 °C for 7 d in darkness. After incubation, the colony diameter on the various agar media was measured. The degree of sporulation, obverse and reverse colony colours and the production of soluble pigments were also determined. Colony colours were described using Kornerup & Wanscher (1967). Colonies were photographed with a Canon EOS 400D. Species were characterised microscopically by preparing slides from MEA. Lactid acid was used as mounting fluid. Specimens were examined using a Zeiss AxioSkop2 plus microscope, and the NIS-Elements D software package from Nikon was used for making photographs and taking measurements.

DNA extraction, PCR amplification and sequencing

DNA extractions were prepared from strains grown for 7 to 14 d on MEA using the Ultraclean™ Microbial DNA isolation Kit (MoBio, Solana Beach, USA). Extracted DNA was stored at -20 °C. The ITS regions and regions of the β-tubulin, calmodulin, RPB1 and RPB2 genes were amplified and sequenced according to previously described methods (Houbraken et al. 2007, 2011, 2012, Houbraken & Samson 2011, Samson et al. 2011).

Data analysis

Sequence contigs were assembled using Seqman from DNA-Star Inc. Newly generated ITS sequences were included in a dataset obtained from the Samson et al. (2011) study. For the alternative genes, only isolates belonging to the T. purpurogenus species complex were included in the analysis. Datasets were aligned using the Muscle software within MEGA5 (Tamura et al. 2011). Neighbour-joining analyses on individual datasets were performed in MEGA5 and node confidence determined using bootstrap analysis with 1000 replicates. Trichocoma paradoxa (CBS 788.83) was selected as outgroup for ITS analysis. For the alternative gene phylogenies, T. purpurogenus was selected as outgroup. Unique, newly generated sequences were deposited in GenBank and their accession numbers are shown in Table 1.

Extrolites

Extrolites were extracted from fungal strains grown on CYA, YES, and some strains were additionally grown on MEA and OA at 25 °C for 7 d for extrolite extraction. Three agar plugs of each medium were extracted as described in Nielsen et al. (2011) and Houbraken et al. (2012). The extracts were analysed by using high performance liquid chromatography with diode-array detection (HPLC-DAD) (Frisvad & Thrane 1987) for extracts made before 2011 and by UHPLC-DAD (Houbraken et al. 2012) for extracts made later. The compounds eluting and detected were identified by comparing retention time, retention index and UV spectra measured from 200–600 nm. The UV spectra were compared to a database of UV spectra (Nielsen et al. 2011), and to literature data (see for example the UV spectrum of pestalasin A shown in Nonaka et al. 2011).

RESULTS

Morphological examination of strains previously identified as T. purpurogenus showed the presence of four distinguishable morphological groups and these are treated here as distinct species (Fig. 1): T. purpurogenus, T. ruber comb. nov., T. stollii sp. nov. and T. amestolkiae sp. nov. Talaromyces purpurogenus is distinct from the other three species by its inability to grow below 18 °C, slow growth on the agar media CYA, the production of a bright red diffusing pigment on CYA at 25 °C and bright yellow and orange mycelium on DG18 at 25 °C. Talaromyces ruber has a velvety texture on both CYA and MEA at 25 °C and produces bright yellow and red mycelium on YES. It also produces a very distinct colony texture on MEA, where bundles of hyphae are produced underneath the velvety texture. Talaromyces amestolkiae and T. stollii are distinguished from T. ruber and T. purpurogenus by the production of acid on CREA. Talaromyces stollii, however, does grow faster on CYA at 36 °C than T. amestolkiae and some of the studied T. amestolkiae strains produced sclerotia after 2 wk incubation at 25 °C. Furthermore, T. stollii has soft synnemata-like or tufted structures at the centre of colonies on most media. Morphological data is supported by phylogenetic results, as discussed below (Fig. 2, 3).

Fig. 1.

Fig. 1

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Agar colonies of species of the Talaromyces purpurogenus complex on different media. Columns, left to right: T. ruber (CBS 370.48), Talaromyces sp. (NRRL 2120), T. ruber (CBS 132704NT), T. amestolkiae (CBS 132696┬), T. stollii (CBS 408.93┬), T. purpurogenus (CBS 132707), P. crateriforme (CBS 184.27┬), P. sanguineum (CBS 122434). Rows to bottom: MEA obverse, MEA reverse, CYA obverse, CYA reverse, DG18 obverse, DG18 reverse, YES obverse, YES reverse, OA obverse, OA obverse, CREA reverse incubated at 25 °C for 7 d.

Fig. 2.

Fig. 2

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Neighbour-joining tree of the ITS1-5.8S-ITS2 rDNA region, showing placement of species described in this paper and other closely related Talaromyces species. Numbers at branching nodes represent bootstrap values (1000 replicates), with bold branches indicating bootstrap values higher than 80 %. Trichocoma paradoxa was selected as outgroup. All strains in this phylogram are regarded as Talaromyces, although they are sometimes labelled as Sagenoma, Penicillium or Erythrogymnotheca.

Fig. 3.

Fig. 3

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Neighbour-joining trees of RPB1, RPB2, β-tubulin and calmodulin showing phylogenetic placement of the newly described species. Numbers at branching nodes represent bootstrap values (1000 replicates), with bold branches indicating bootstrap values higher than 80 %. Talaromyces purpurogenus was selected as outgroup. Species indicated in bold are treated in this paper.

Barcodes of the ITS locus were used to study the phylogenetic relationship between strains previously identified as T. purpurogenus and other Talaromyces species. The ITS alignment included eight strains and was 469 bp characters long. The results showed that strains belonging to T. amestolkiae, T. ruber and T. stollii form a phylogenetically distinct clade, separate from the distinctly related T. purpurogenus clade. ITS gave low bootstrap support within the clade where T. amestolkiae, T. ruber and T. stollii are located and thus detailed analysis was performed using four more variable protein-coding genes. For RPB1, RPB2, β-tubulin and calmodulin the alignments were, respectively, 850, 1050, 450 and 466 bp long and contained 19 taxa, five representative strains of each studied species. Because the clade containing T. purpurogenus and its synonyms are distinct from the other species discussed in this paper, T. purpurogenus was used as the outgroup for the multi-gene analysis. Except for calmodulin, which could not distinguish between T. amestolkiae and T. ruber, all gene sequences supported consistent and coherent clades with high bootstrap support. Strain CBS 196.88, designated as neotype of Penicillium minioluteum by Pitt (1980), is distinct from T. minioluteus (CBS 642.68┬) and resolved in the T. ruber clade (Fig. 2). Many strains previously identified as Penicillium purpurogenum var. rubrisclerotium were resolved in a clade with T. amestolkiae. However, the ex-type strain of P. purpurogenum var. rubrisclerotium (CBS 270.35┬) is resolved in a distinct clade closely related to T. mi- nioluteus (Fig. 2).

Extrolite data

The four species treated here produce many extrolites. Talaromyces purpurogenus isolates can produce four different mycotoxins: rubratoxins (A & B) (Moss et al. 1968, 1971, Moss & Hill 1970), rugulovasines (A and B) and chlororugulovasins A and B (Cole et al. 1976, Dorner et al. 1980, Mapari et al. 2009), luteoskyrin (reported here) and spiculisporic acid (Oxford & Raistrick 1934) (Table 2, 3) (see Frisvad 1989, as P. crateriforme), in addition to mitorubrins (mitorubrin, mitorubrinol, mitorubrinol acetate, mitorubrinic acid) (Büchi et al. 1965, Chong et al. 1971), N-glutarylrubropunctamine, PP-R, monascin and monascorubramine (Mapari et al. 2009, as P. crateriforme) and purpactins (Nishida et al. 1991, Tomoda et al. 1991). We could confirm the production of rubratoxins, rugulovasines, luteoskyrin, mitorubrins, ‘Monascus red pigments’ and purpactins in T. purpurogenus (Table 3). The red azaphilone ‘Monascus pigments’ are diffusible in T. purpurogenus, but not in the other three species (Fig. 1).

Table 2.

Strains of Talaromyces purpurogenus previously identified as P. crateriforme, P. rubrum or P. purpurogenum and their production of mycotoxins.

Original number Other collection numbers Toxin reported Reference Isolate data
P-13 NRRL 3290 = NRRL A-11785 = ATCC 26940 = KCTC 6825 = BRCC 31680 = IBT 3936 Rubratoxin A and B* Wilson & Wilson (1962) From Dennis N. Cox, Georgia, USA
1968-10-28a IMI 136126 = MR 006 = IBT 10710 Rubratoxin A and B Moss & Hill (1970) Mould field corn, Wisconsin, EB Smalley
1968-10-28b IMI 136127 = MR 007 = IBT 5016 Rubratoxin A and B Moss & Hill (1970) Mould field corn, Wisconsin, EB Smalley
1968-10-28c IMI 136128 = MR 008 = IBT 3658 = IBT 5015 = DTO 189 A1 Rubratoxin A and B Moss & Hill (1970) Mould field corn, Wisconsin, EB Smalley
IMI 112715 = MR 185 = IBT 10712 Rubratoxin A and B* Moss & Hill (1970) Rhizospere of Trifolium alexandrinum, Egypt, A. El Esaily
IMI 129717 = MR 043/RC Rubratoxin A and B Moss & Hill (1970) PKC Austwick
IMI 129718 = MR 043/OB6 Rubratoxin A and B Moss & Hill (1970) PKC Austwick
IMI 129719 = MR 043/OA Rubratoxin A and B Moss & Hill (1970) PKC Austwick
IMI 129716 = MR 180 Rubratoxin B Moss & Hill (1970) Van der Walt, South Africa
NRRL 2019 = IBT 3549 Rubratoxin B Data reported here Unknown source
FAT 1141 ATCC 20204 = IBT 4183 = IFO 5722 = CBS 113158 Rubratoxin B* Data reported here Japan, S. Abe
CP 187 ATCC 44445 = IBT 4433 = IBT 10711 = KCTC 16067 = CBS 113159 Rugulovasine A* and B*, chlororugulovasine A and B Dorner et al. (1980) Field corn kernel, Georgia, RA Hill
ATCC 44445 Rubratoxin B* Data reported here Field corn kernel, Georgia, RA Hill
CBS 286.36 = IMI 091926 = CECT 20441 = KCTC 6821 = LSHB P.48 = NCTC 586 = NCTC Ad 36 = Thom 17 Data reported here Kral, Czech Republic (ex-type)
NRRL 1057 = CBS 124.27 = MUCL 29224 = LSHB P154 = ATCC 52215 = IMI 094165 = KCTC 6784 = Thom 4894.13 = FRR 1047 Rubratoxin B* Soil, Louisiana, Gilman and Abbott (ex-type of P. crateriforme)
NRRL 1059 = IBT 10612 = IBT 3560 = CCRC 31681 = BCRC 31681 = Thom 5694.11 = NCIM 762 = ATCC 10064 C.W. Emmons (P. sanguineum)
FA 184-WZ-15 IBT 11628 = CBS 113161 Rubratoxin B* Data reported here Wheat, Winnipeg, Canada, JT Mills
FA 158-B1-1X IBT 11632 Rubratoxin B* Data reported here Barley, Winnipeg Canada, JT Mills
FA 156-B1-1 IBT 11694 Rubratoxin B* Data reported here Barley, Winnipeg Canada, JT Mills
U-92-10 MB nr. 4 IBT 12779 Oregano imported to Denmark
U-92-5-6 IBT 13014 Oregano imported to Denmark
DANL 451(20) IBT 17318 = CBS 113162 Air in cake factory, Denmark
KELS 9a IBT 17326 Air in cake factory, Denmark
UAMH 8046 IBT 17340, IBT 17341, IBT 17342 = CBS 113160, IBT 17343 Rubratoxin B* Richer et al. (1997) Mouldy home-made rhubarb wine, Canada, L. Sigler
F1150 (B) IBT 17540 Unknown origin
CCRC 32601 IBT 18380 Dung of pig, Taipei City, Taiwan, S.S. Tzean
Pr IBT 20484 Rye flour, Denmark
Det 287/98 nr. 146 IBT 21742 Agricultural soil, Canada, Keith Seifert
Lee no. 3 IBT 23074 Soil, South Korea, H.B. Lee
Lucab 201_LAB01 IBT 30226 Soil, Serro de Cip, Brazil, Lucas Abreau
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* Confirmed chemically in this study.

Table 3.

Extrolite production by Talaromyces amestolkiae, T. purpurogenus, T. ruber and T. stollii as detected by HPLC-DAD.

Species Extrolite Strains producing the extrolite
T. amestolkiae Berkelic acid CBS 329.48, CBS 365.48, CBS 433.62, CBS 436.62, CBS 884.72, CBS 353.93, CBS 277.95, CBS 113143, CBS 132695, CBS 132697, FRR 1095, IBT 20202, IBT 23821, IMI 061385, IMI 104624, IMI 147406
N-Glutarylrubropunctamine CBS 365.48, CBS 436.62, IMI 147406
Mitorubrinic acid CBS 433.62, CBS 436.62, CBS 132695, FRR 1095, IBT 20202, IBT 23821
Pestalasin A CBS 252.31, CBS 365.48, CBS 433.62, CBS 436.62, CBS 884.72, CBS 113143, CBS 132695, FRR 1095, IBT 19175, IBT 23821, IMI 061385, IMI 147406
A purpactin CBS 433.62, CBS 436.62
Vermicellin CBS 433.62, CBS 132695, FRR 1095
‘m328’ (= berkeleyacetal) CBS 252.31, CBS 433.62, CBS 353.96, CBS 263.93, CBS 264.93, CBS 277.95, CBS 390.96, CBS 113143, CBS 132695, FRR 1095, IBT 20202, IBT 23821, IBT 29986, IMI 061385, IMI 147406
‘HHH’ (blue fluorescing) CBS 232.31, CBS 329.48, CBS 365.48, CBS 433.32, CBS 436.32, CBS 884.72, CBS 263.93, CBS 264.93, CBS 353.93, CBS 274.95, CBS 277.95, CBS 390.96, CBS 113143, CBS 132695, CBS 132697, FRR 1095, IBT 19175, IBT 20202, IBT 23821, IBT 29986, IMI 061385, IMI 104624, IMI 147406
‘m334’ CBS 465.48, CBS 433.62, CBS 884.72, FRR 1095, IBT 19175, IBT 20202, IBT 23821, IMI 147406
T. purpurogenus1 N-Glutarylrubropunctamine CBS 184.27, CBS 286.36, CBS 113160, IBT 11632, IBT 12779, IMI 112715, IMI 136126, IMI 136127, IMI 136128, NRRL 3290
Luteoskyrin ATCC 20204 (weak), CBS 113160, IMI 136127, IMI 136128, NRRL 1749, NRRL 3290
Mitorubrin, mitorubrinol, mitorubrinic acid ATCC 20204, ATCC 44445, CBS 184.27, CBS 286.36, CBS 113160, IBT 11632, IBT 12779, IBT 17540, IBT 31167, IMI 112715, IMI 136126, IMI 136127, IMI 136128, NRRL 1749, NRRL 3290
Purpactins ATCC 20204, ATCC 44445, CBS 286.36, CBS 113160, IBT 11632, IBT 12779, IBT 17540, IBT 31167, IMI 112715, IMI 136126, IMI 136127, NRRL 1749, NRRL 3290
Rubratoxin A & B ATCC 20204, ATCC 44445, CBS 184.27, CBS 286.36, CBS 113160, IBT 11632, IBT 12779, IBT 17540, IBT 31167, IMI 112715, IMI 136126, IMI 136127, IMI 136128, NRRL 1749, NRRL 2019, NRRL 3290
Rugulovasine A and B ATCC 444452, CBS 184.27, IBT 12779, IBT 31167, IMI 136127, IMI 136128, NRRL 3290
T. ruber Austin and austinol CBS 370.48, CBS 368.73, CBS 195.88, CBS 196.88, CBS 237.93, CBS 113140, FRR 1503, IMI 113729, IMI 139462, IMI 178519, NRRL 1180
N-Glutarylrubropunctamine CBS 196.88, IBT 22364
Mitorubrin CBS 368.73, CBS 237.93, CBS 132699, FRR 1503, NRRL 1180
Pestalasin A CBS 196.88, CBS 237.93, CBS 113140, FRR 1503, IMI 113729, IMI 139462, NRRL 1180
A purpactin CBS 237.93, CBS 132699, FRR 1503
Vermicellin CBS 368.73, CBS 196.88, CBS 237.93, CBS 132699, FRR 1503, IMI 139462, NRRL 1180
‘DDD’ CBS 368.73, CBS 195.88, CBS 196.88, CBS 237.93, CBS 868.96, CBS 113140, FRR 1503, IBT 22364, IMI 113729, IMI 139462, NRRL 1180
‘m334’ CBS 368,73, CBS 195.88, CBS 196.88, CBS 237.93, CBS 868.96, CBS 113140, CBS 132699, FRR 1503, IBT 22364, IMI 113729, IMI 139462, IMI 178519, NRRL 1180
T. stollii austins CBS 132706, CBS 100372
‘HHH’ CBS 408.93, CBS 132706, DTO 60-D5, CBS 265.93, CBS 582.94
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1 Spiculisporic acid was found in CBS 184.27 (Oxford & Raistrick 1934), but could not be detected by us using HPLC-DAD, as it has UV end-absorption below 200 nm.

Talaromyces ruber isolates produced austins, mitorubrins, Monascus pigments, pestalasin A, a purpactin, and chromophore groups ‘DDD’ and ‘m334’ and the antibiotic vermicellin (Fuska et al. 1979). Talaromyces stollii isolates produced austins and chromophore group ‘HHH’. Talaromyces amestolkiae produced berkelic acid, mitorubrinic acid, red ‘Monascus pigments’, a purpactin and vermicellin, and the chromophore groups ‘HHH’, ‘m328’ and ‘m334’. A strain identified as Penicillium rubrum was isolated from the acid and metal polluted Berkeley Pit Lake in Montana (Stierle et al. 2006), and this strain is probably T. amestolkiae. Of the extrolites extracted from this strain, berkelic acid was one of them. In addition to these extrolites, all species produce other extrolites that were unique to one of the species or in common between several of the four species.

Taxonomy

Talaromyces amestolkiae Yilmaz, Houbraken, Frisvad & Samson, sp. nov. — MycoBank MB801358; Fig. 4

Fig. 4.

Fig. 4

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Morphological characters of Talaromyces amestolkiae (CBS 132696┬). a. Colonies incubated on CYA, MEA, YES, CREA, from left to right (top row = obverse, bottom row = reverse); b. colony texture on MEA; c–g. conidiophores produced on MEA; h. conidia. — Scale bars: c = 50 μm; g = 10 μm and applies to d–h.

Etymology. Latin, amestolkiae: named in honour of Amelia C. Stolk, who pioneered taxonomic studies on Penicillium and Aspergillus at CBS from 1940–1976.

Typus. Herbarium CBS H-21050 (dried specimen), also maintained under CBS 132696, isolated from house dust from South Africa.

Conidiophores biverticillate, subterminal branches present, have a greenish to brownish pigmentation; stipes smooth walled, 93–164 × 2.5–3 μm; branches 2–3 when present, 15– 49 × 2–3 μm; metulae in verticils of 3–5, 11–13 μm across apex, 9.5–14 × 3–4 (av. ± stdev = 11.9 ± 1.2 × 3.4 ± 0.2) μm; phialides acerose, 3–6 per metula, 9.5–12 × 2.5–3 (av. ± stdev = 11.9 ± 1.0 × 2.6 ± 0.2) μm; conidia smooth, some rough, ellipsoidal, 2–3 × 1.5–2.5 (av. ± stdev = 2.6 ± 0.2 × 1.9 ± 0.2) μm.

Colony morphology — CYA, 7 d: 12 °C 5–7 mm, 15 °C 7–10 mm, 18 °C 10–14 mm, 21 °C 13–20 mm, 24 °C 21–30 mm, 27 °C 24–35 mm, 30 °C 30–35 mm, 33 °C 28–31 mm, 36 °C 8–14 mm, 40 °C no growth. CYA, 25 °C, 7 d: Colonies 29–30 mm, low, raised at centre, margins wide (2–3 mm), entire; mycelium white and yellow, red in centre; texture floccose with overlaying funicles and tufts; sporulation moderately dense to dense; conidia en masse greyish green (26E6–26E7); exudate absent; soluble pigment very weak, with inconspicuous red pigment in some strains, reverse coloration dark brownish red (11F8–12F8). MEA, 25 °C, 7 d: Colonies 33–42 mm, low, plane; margins very wide (3–5 mm), entire; mycelium white, red at centre; texture tufted at centre, elsewhere floccose with overlaying funicles, floccose at margins; sporulation moderately dense to dense; conidia en masse greyish to dull green (25D4–26D4); exudate absent; soluble pigment absent; reverse coloration dark brownish red (9F8) at centre, greyish yellow to greyish orange (3C5–5C5) at margins. OA, 25 °C, 7 d: Colonies 50–52 mm, low, plane; margins very wide (5–6 mm), entire; mycelium white and yellow, red at centre; texture floccose with overlaying funicles; sporulation dense; conidia en masse greyish green (25D4–25D6); exudate present in some strains, clear; soluble pigment absent; reverse coloration red (11E4) at centre, red pigmentation absent in some strains. DG18, 25 °C, 7 d: Colonies 17–18 mm, low, slightly raised at centre; margins narrow (1 mm), entire; mycelium white; texture velvety with overlaying funicles; sporulation moderately dense; conidia en masse similar to CYA; exudate present in some strains, clear; reverse coloration dark brown (8F8). YES, 25 °C, 7 d: Colonies 27–28 mm, low, sulcate; margins narrow (1–2 mm), entire; mycelium white, red at centre; texture floccose with tufts present; sporulation moderately dense, conidia en masse similar to CYA; exudate absent; soluble pigment absent; reverse coloration brownish red (11F8–12F8). CREA, 25 °C, 7 d: Colonies 15–24 mm, poor acid production, only within colony periphery. CYAS, 25 °C, 7 d: Typically no growth, some strains restricted growth, 6–8 mm.

Distinguishing characteristics — Talaromyces amestolkiae belongs to the same clade as T. ruber and T. stollii. It is distinguished from T. ruber and T. purpurogenus by acid production on CREA, and floccose and funiculose texture on MEA. It is distinguished from T. stollii by its slower growth at 37 °C.

Talaromyces purpurogenus (Stoll) Samson, Yilmaz, Frisvad & Seifert — MycoBank MB560667; Fig. 5

Fig. 5.

Fig. 5

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Morphological characters of Talaromyces purpurogenus (CBS 132707). a. Colonies incubated on CYA, MEA, YES, CREA, from left to right (top row = obverse, bottom row = reverse); b. colony texture on MEA; c–g. conidiophores produced on MEA; h. conidia. — Scale bars: c = 50 μm; g = 10 μm and applies to d–h.

Basionym. Penicillium purpurogenum Stoll, Beitr. Morph. Biol. Char. Penicill.: 32. 1904.

  • = Penicillium sanguineum Sopp, Skr. Vidensk.-Selsk. Christiania, Math.-Naturvidensk. Kl. 11: 175. 1912.

  • =Penicillium crateriforme J.C. Gilman & E.V. Abbott, Iowa State Coll. J. Sci. 1: 293. 1927.

Typus. CBS 286.36┬ (the ex-type strain is deteriorated, CBS 132707 can be regarded as typical for the species).

Conidiophores strictly biverticillate, subterminal branches absent; stipes smooth walled, 150–250 × 2.5–3.5 μm; metulae in verticils of 3–5, 9–13 μm across apex, 12–14.5 × 2.5–4 (av. ± stdev = 13.2 ± 0.8 × 3.2 ± 0.5) μm; phialides acerose, 3–6 per metula, 12–13.5 × 2–3 (av. ± stdev = 12.8 ± 0.5 × 2.4 ± 0.3) μm; conidia smooth, ellipsoidal, 3–3.5 × 2–2.5 (av. ± stdev = 3.1 ± 0.2 × 2.3 ± 0.1) μm.

Colony morphology — CYA, 7 d: 12 °C no growth, 15 °C no growth, 18 °C no growth, 21 °C 6–15 mm, 24 °C 11–20 mm, 27 °C 18–27 mm, 30 °C 18–27 mm, 33 °C 18–25 mm, 36 °C 14–25 mm, 40 °C no growth. CYA, 25 °C, 7 d: Colonies 20–25 mm, moderately deep, sulcate; margins very narrow (0.5–1 mm); mycelium white and red; texture floccose; sporulation sparse to moderately dense; conidia en masse dull green (27D3–28D3); exudate absent, soluble pigment typically bright red, absent in some isolates; reverse coloration dark brown to violet brown (9F8–11F8) fading to reddish brown (9D8), in non-soluble pigment producers pale and light red. MEA, 25 °C, 7 d: Colonies 33–41 mm, low slightly at point of inoculation; margins wide (3–4 mm), entire; mycelium orange and white; texture floccose, with some velvety areas, some strains covered by white sterile mycelium; sporulation moderately dense, in some strains absent, conidia en masse dull green (26E4–26E5); exudate absent, sometimes clear droplets; soluble pigment absent; reverse coloration brownish yellow to brownish orange (5C7–6C7). OA, 25 °C, 7 d: Colonies 28–35 mm, low, plane; margins wide (2–3 mm), entire; mycelium white and orange; texture velvety and floccose; sporulation moderately dense to dense, conidia en masse dull green (26E4–26E5); exudate absent; soluble pigment absent; reverse coloration dull red (9C4), colour lacking in some. Colonies produce an apple-like fruity odour. DG18, 25 °C, 7 d: Colonies 11–15 mm, low, plane; margins wide (1–2 mm), entire; mycelium white and bright orange; texture velvety, some floccose mycelium present; sporulation sparse to moderately dense, conidia en masse dark green (27F5); exudate absent; soluble pigment absent; reverse coloration light to brownish orange (5A4–5C4). YES, 25 °C, 7 d: Colonies 25–35 mm, low, sulcate; margins wide (1–2 mm), entire; mycelium white and orange, yellow in strains; texture floccose; sporulation moderately dense, conidia en masse dull to greyish green (26E4–26E5); exudate absent; soluble pigment absent; reverse coloration light yellow to brown (4A5–6D7), some strains dark red to dark brown (8F4). CREA, 25 °C, 7 d: Colonies 7–11 mm. Typically no acid production; strain CBS 122434 has poor acid production. CYAS, 25 °C, 7 d: No growth to microcolonies of up to 5 mm.

Distinguishing characteristics — Talaromyces purpurogenus is distinct from the other three very similar species. It is not able to grow at temperatures below 18 °C, grows slower and produces a bright red diffusing pigment on CYA at 25 °C and has bright yellow and orange mycelium on DG18 at 25 °C.

Talaromyces ruber (Stoll) Yilmaz, Houbraken, Frisvad & Samson, comb. nov. — MycoBank MB801360; Fig. 6

Fig. 6.

Fig. 6

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Morphological characters of Talaromyces ruber (CBS 132704┬). a. Colonies incubated on CYA, MEA, YES, CREA, from left to right (top row = obverse, bottom row = reverse); b. colony texture on MEA; c–g. conidiophores produced on MEA; h. conidia. — Scale bars: c = 50 μm; g = 10 μm and applies to d–h.

Basionym. Penicillium rubrum Stoll, Beitr. Morph. Biol. Char. Penicill.: 35. 1904.

Typus. Since no holotype is known herbarium CBS-H-21052 (dried specimen) is here designated as neotype. It is derived from CBS 132704, isolated from aircraft fuel tank from United Kingdom. CBS 370.48 was used by Raper & Thom to describe Penicillium rubrum, but it no longer displays all diagnostic characters.

Conidiophores biverticillate; stipes smooth walled, 110–232 × 2.5–3 μm; metulae in verticils of 3–5, 7.5–11 μm across apex, 7.5–10.5 × 2.0–3 (av. ± stdev = 9.6 ± 1.0 × 2.3 ± 0.3) μm; phialides acerose, 3–6 per metula, 9–12 × 2–2.5 (av. ± stdev = 9.8 ± 2.8 × 2.1 ± 0.2) μm; conidia smooth, ellipsoidal, 2.5–3.5 × 1.5–2 (av. ± stdev = 2.9 ± 0.2 × 1.8 ± 0.1) μm.

Colony morphology — CYA, 7 d: 12 °C 3–5 mm, 15 °C 5–10 mm, 18 °C 9–13 mm, 21 °C 15–20 mm, 24 °C 17–25 mm, 27 °C 20–30 mm, 30 °C 24–30 mm, 33 °C 20–26 mm, 36 °C 14–17 mm, 40 °C no growth. CYA, 25 °C, 7 d: Colonies 22–30 mm, low, radially sulcate, in CBS 370.48┬ colonies are pink with no sporulation; margins low, wide (2–3 mm), entire; mycelium white, yellow and red; texture velvety, sometimes with funicles near margins; sporulation moderately dense, conidia en masse bright olive green to greyish green (26D4–27D4); exudate present in some strains, small clear and red droplets; soluble reddish pigment typically present, absent in some strains; reverse coloration brownish red (8E8–8F8). MEA, 25 °C, 7 d: Colonies 35–38 mm, low, plane; margins low, very wide (5–6 mm), entire; mycelium, white and yellow; texture velvety, ropes of mycelium produced very close to media and sometimes inside the medium (Fig. 6b) sporulation dense, conidia en masse greyish green (26D4–26E4), some strains a lighter greyish green (26B3); exudate absent; soluble pigment absent; reverse coloration brownish red to dark brown (8F8–8C8) at centre, elsewhere greyish yellow to greyish orange (4B4–4C4–5B4). OA, 25 °C, 7 d: Colonies 40–42 mm, low, plane; margins very wide (4–5 mm), entire, low; mycelium white and yellow; texture velvety and floccose; sporulation moderately dense, conidia en masse dull to dark green (27D4–27F8); exudate absent, in some strains clear; soluble pigment absent; reverse coloration reddish brown (8D7). DG18, 25 °C, 7 d: Colonies 14–16 mm, plane, low, with a brownish orange colour; margins narrow (2–3 mm), entire; mycelium white; texture floccose; sporulation sparse, conidia en masse similar to CYA; exudate small clear droplets; soluble pigment absent; reverse coloration greyish green (30D6–30E6) at centre, elsewhere greenish white (30A2). YES, 25 °C, 7 d: Colonies 22–30 mm, low, raised at centre, radially and concentrically sulcate; margins low, narrow (1–2 mm), entire; mycelium white and yellow, red in some strains, e.g. CBS 868.96; texture floccose; sporulation sparse to moderate dense, conidia en masse greyish green (27C5–27E6–27E7); exudate clear small droplets; reverse coloration greyish brown to brown (5F8–5F3) near centre, at margins brownish orange to light brown (5C4–5D4). CREA, 25 °C, 7 d: Colonies 10–14 mm, restricted growth, no acid production. CYAS, 25 °C, 7 d: Typically no growth, sometimes microcolonies up to 4 mm.

Distinguishing characteristics — Talaromyces ruber can be distinguished from T. purpurogenus by growth at lower temperatures, having a velvety texture on MEA, yellow mycelia and bright green conidia on YES after 7 d incubation at 25 °C. Talaromyces ruber can be distinguished fromT. stollii and T. amestolkiae by absence of acid production on CREA. Talaromyces ruber has a velvety structure on both CYA and MEA at 25 °C, produces a very distinct colony texture on MEA and produces bright yellow and red mycelia on YES.

Talaromyces stollii Yilmaz, Houbraken, Frisvad & Samson, sp. nov. — MycoBank MB801359; Fig. 7

Fig. 7.

Fig. 7

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Morphological characters of Talaromyces stollii (CBS 408.93┬). a. Colonies incubated on CYA, MEA, YES, CREA, from left to right (top row = obverse, bottom row = reverse); b. colony texture on MEA; c–g. conidiophores produced on MEA; h. conidia. — Scale bars: c = 50 μm; g = 10 μm and applies to d–h.

Etymology. Latin, stollii: named in honour of Otto Stoll, a pharmacist who first described P. rubrum and P. purpurogenum for his PhD thesis at the K. Bayr Julius Maximilians University in Würzburg, Germany in 1905.

Typus. Herbarium: CBS H-21053 (dried specimen), derived from CBS 408.93, isolated from an AIDS patient, the Netherlands.

Conidiophores biverticillate, subterminal branches present, have a greenish to brownish pigmentation; stipes smooth walled, 94–247 × 3–4.5 μm; metulae in verticils of 3–5, 9.5–10 μm across apex, 11.5–14.5 × 2–3.5 (av. ± stdev = 12.5 ± 0.9 × 2.9 ± 0.4) μm; phialides acerose, 3–6 per metula, 13–17 × 2–2.5 (av. ± stdev = 14.2 ± 1.2 × 2.1 ± 0.2) μm; conidia smooth to lightly roughed, ellipsoidal, 2.5–4 × 2–2.5 (av. ± stdev = 3.2 ± 0.3 × 2.1 ± 0.2) μm.

Colony morphology — CYA, 7 d: 12 °C 4–6 mm, 15 °C 5–10 mm, 18 °C 13–18 mm, 21 °C 19–25 mm, 24 °C 30–35 mm, 27 °C 36–43 mm, 30 °C 38–44 mm, 33 °C 35–44 mm, 36 °C 24–35 mm, 40 °C no growth. CYA, 25 °C, 7 d: Colonies 38–42 mm, low, raised at centre, lightly radially sulcate; margins wide (2–3 mm), entire; mycelium white and red; texture floccose; sporulation sparse, conidia en masse greyish to dull green (27C4–27D4); exudate present, small pinkish or yellowish droplets; soluble pigment absent; reverse coloration dark brown (8F8) at point of inoculation, elsewhere greyish red (7B3). MEA, 25 °C, 7 d: Colonies 45–50 mm, low, plane; margins wide (3–4 mm), entire; mycelium white, at centre sometimes red, sometimes yellow; texture floccose and funiculose, white sterile tufts covering colonies; sporulation moderately dense, conidia en masse greyish to dull green (27C4–27D4); exudate absent; soluble pigment absent; reverse coloration brownish orange to brownish yellow (5C6–6C7). OA, 25 °C, 7 d: Colonies 44–48 mm, low, plane; margins very wide (4–7 mm), entire; mycelium white; texture floccose, with funiculose that rise from colony centre similar to synnemata; sporulation sparse, conidia en masse similar to CYA; exudate present, clear; soluble pigment absent; reverse coloration reddish at centre, green elsewhere, some strains yellowish. DG18, 25 °C, 7 d: Colonies 18–25 mm, low, plane; margins low, wide (2–3 mm), entire; mycelium white; texture floccose; sporulation absent; exudates absent, sometimes yellow droplets; soluble pigment absent; reverse coloration pale, some strains brownish orange (5C6) at centre, fading into pale yellow (4A3) at margins. YES, 25 °C, 7 d: Colonies 33–38 mm, low, lightly sulcate; margins wide (3–4 mm), entire; mycelium white; texture floccose; sporulation very sparse; exudate absent; soluble pigment absent; reverse coloration similar to CYA. CREA, 25 °C, 7 d: Colonies 20–30 mm; sparse sporulation, poor acid production, only within colony periphery. CYAS, 25 °C, 7 d: No growth to microcolonies of up to 5 mm.

Distinguishing characteristics — Talaromyces stollii is distinguished from T. ruber and T. purpurogenus by acid production on CREA. Talaromyces stollii does, however, grow faster on CYA at 36 °C than T. amestolkiae. In addition, T. stollii has unique soft synnemata-like or tufted structures in the centre of colonies on most media.

DISCUSSION

Cultures that previously were identified as P. purpurogenum orP. rubrum were analysed in this study and phylogenetic, morphological and extrolite results show that the T. purpurogenus complex consists of four distinct species. The species described below are quite common on textiles, paper, soil, dung, plant debris, coffee-berries, corn, indoor air and dust, and are distributed worldwide. Talaromyces purpurogenus has been implicated in the biodeterioration of cellulose materials such as textiles, paper and adhesives, while it also has the ability to grow on plant material such as corn, where it may produce mycotoxins (Moss et al. 1971). Talaromyces purpurogenus produces four types of mycotoxins: rubratoxin A & B, rugulovasins, spiculisporic acid and luteoskyrin, and none of the other three species treated have been found to produce mycotoxins. The newly described species T. amestolkiae and T. stollii grow well at 37 °C and some strains were isolated from AIDS patients and might be opportunistic pathogens. It is not yet known if any other species in this group can be opportunistic pathogens. Talaromyces purpurogenus was reported as the causal agent of a disseminated mycosis in a German shepherd dog (Zanatta et al. 2006), but it remains unknown if this species identification is correct using the newly proposed taxonomy. This group is also biotechnologically important, because of their production of enzymes (Carvallo et al. 2003, Jeya et al. 2010) and extrolites. For example, the mycotoxin rubratoxin A & B produced by T. purpurogenus has been shown to act as cancer metastasis suppressors (Wada et al. 2010) and spiculisporic acid can be used as a detergent (Ishigami et al. 2000). From a biotechnological point of view we would recommend using T. ruber for enzyme production, because T. purpurogenus produces four types of mycotoxins and T. amestolkiae and T. stollii are potentially pathogenic to immuno-compromised persons. However, it is not known whether the enzymes reported from T. purpurogenus (Steiner et al. 1994, Belancic et al. 1995) are indeed from this species or one of the other three taxa treated here or even any of them.

Most of the isolates produced the extrolites characteristic of the species (Table 3), but some isolates should be grown on other media to examine whether they can also produce the remaining extrolites found in productive strains. Most extrolites supported the phylogram in Table 3. Production of purpactin, pestalasin A, vermicellin and ‘m334’ supported that T. ruber and T. amestolkiae are closely related. On the other hand common production of ‘HHH’ indicated that T. amestolkiae and T. stollii are closely related, while common production of austin indicates that T. ruber and T. stollii are closely related. Purpactin was produced by the outgroup T. purpurogenus but also by T. ruber and T. amestolkiae. Rubratoxins, spiculisporic acid, rugulovasins, chlororugulovasins and luteoskyrin were autapomorphic for T. purpurogenus, while berkelic acid and ‘m328’ were autapomorphic for T. amestolkiae. Metabolite ‘DDD’ was autapomorphic for T. ruber and a larger number of derivatives of ‘HHH’ were autapomorphic for T. stollii. It should be noted that some of these extrolites are also found outside the T. purpurogenus complex. For example, luteoskyrin is produced by T. islandicus (Uraguchi et al. 1961) and spiculisporic acid is produced by T. trachyspermus (Clutterbuck et al. 1931) and T. ucrainicus (Fujimoto et al. 1988).

The species in this complex generally produce yellow, orange and red pigments in the mycelium or as diffusing pigments. Extrolites responsible for these colours are two groups of azaphilone polyketide pigments the mitorubrins (mitorubrin, mitorubrinol, mitorubrinol acetate and mitorubrinic acid) (Büchi et al. 1965) and the Monascus red pigments (N-glutaryl monascorubramin, N-glutarylrubropunctamin, monascorubramine, monascin, PP-R and others (Mapari et al. 2009)). These azaphilone polyketides are produced by all the species treated in this paper and several other species in Talaromyces, but they appear to be produced in different ratios and amounts in different isolates and species (Frisvad et al. 1990, van Reenen-Hoekstra et al. 1990, Samson et al. 2011). Also, especially on MEA, we observed that when a strain that produced red pigment was transferred to another MEA plate, the strain sometimes lost the ability to produce the red pigment. However, red pigment production was consistent on CYA. Apart from the medium employed for extrolite production, the age of the strain may also play a role: older strains of T. purpurogenus, such as isolates formerly called P. crateriforme and P. sanguineum, have lost their ability to produce high amounts of diffusible red pigments. The red pigments have resulted in some confusion, especially in the concept of T. purpurogenus and T. ruber. Talaromyces purpurogenus and T. ruber were described by Stoll (1903–1904). Raper & Thom (1949) considered the species as distinct. Talaromyces purpurogenus was distinguished from T. ruber by the production of spreading dark yellow green colonies and smooth-walled conidia in the latter species. This is in comparison to the sometimes more restricted dark green colonies and rough-walled conidia they observed in T. purpurogenus. Although Pitt (1980) synonymised T. ruber with T. purpurogenus, our data indicate that these two species are distinct and they are re-described below. Talaromyces ruber can be distinguished from T. purpurogenus by growth at lower temperatures, its velvety texture on MEA, yellow mycelium and bright green conidia on YES after 7 d incubation at 25 °C. With regards to conidia ornamentation, all strains examined of both these species produced smooth-walled conidia and this character is thus not diagnostic for species recognition. No type material was designated for T. ruber, therefore Raper & Thom (1949) centred their description of T. ruber on NRRL 1062 and NRRL 2120. Our analysis shows these two strains belong to different species. NRRL 1062 (= CBS 370.48) is designated here as the neotype of T. ruber, while NRRL 2120 represents a new phylogenetically unrelated species (Fig. 2).

Penicillium sanguineum and P. crateriforme are considered synonyms of T. purpurogenus. In Sopp’s description of P. san- guineum, he states that this species produces bright red pigments, which colours the entire gelatine medium, as well as producing yellow coloured mycelium (Sopp 1912). Although no type material exist for this species, the description by Sopp (1912) indicates that it belongs to the T. purpurogenus complex. Penicillium crateriforme (CBS 184.27┬) is resolved in a clade together with the ex-type cultures for T. purpurogenus (CBS 286.36┬) and is considered a synonym of T. purpurogenus.

Pitt (1980) neotypified P. minioluteum using strain IMI 89377ii (CBS 196.88). CBS 642.68┬ is a subculture of the same strain obtained from the IMI in 1968, but it morphologically fits Biourge’s description of P. minioluteum. It was therefore considered the correct neotype of the species as discussed in earlier studies (van Reenen-Hoekstra et al. 1990). Our phylogenetic data show that T. minioluteus (CBS 642.68) remains in a clade distantly related to T. ruber (CBS 196.88).

This study resulted in the delimitation of T. amestolkiae and T. stollii, two new species closely related to T. ruber. Talaromyces amestolkiae and T. stollii are distinguished from T. purpurogenus and T. ruber by their acid production on CREA and floccose to funiculose texture of MEA. Compared to T. amestolkiae, T. stollii grows faster on CYA at 36 °C, as well as pro- ducing unique synnemata/tufted mycelium on most media. Talaromyces amestolkiae and T. stollii share the production of the ‘HHH’ family of extrolites. Although these species are resolved amongst known sexual species, we did not observe cleistothecia for strains studied. Future studies that aim to induce sexual reproduction would be interesting, especially for explaining the morphological and genetic variation observed between T. stollii strains. Also, sclerotia were produced by T. amestolkiae strains, but these never matured into cleistothecia. Many strains previously identified as P. purpurogenum var. rubrisclerotium were resolved in a clade with T. amestolkiae. However, the ex-type strain of P. purpurogenum var. rubrisclerotium (CBS 270.35┬) is resolved in a distinct clade closely related to T. minioluteus (Samson et al. 2011).

This paper addressed the taxonomic difficulties experienced in the T. purpurogenus complex. Results showed that this complex contains four distinct species and that they can be identified using morphological characters, extrolites and/or genetic data. The ITS barcodes could reliably separate the four species within this complex. However there is only one base pair difference between T. ruber and T. amestolkiae, and thus the alternative genes were needed for taxon identification. Although calmodulin could not resolve T. amestolkiae from T. ruber, RPB1, RPB2 and β-tubulin gave a clear species delineation and can be used for identifying species within this clade.

Acknowledgments

We thank Dr Uwe Braun for nomenclatorial advice and Dr Keith Seifert for helpful suggestions. We also acknowledge Dr Seifert for hosting Ellen Hoekstra in 1998 for her sabbatical.

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