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The polyphyletic nature of Paecilomyces sensu lato based on 18S-generated rDNA phylogeny

     BIOTEC, NSTDA Science Park, 113 Paholyothin Road, Khlong 1, Khlong Luang, Pathum Thani, Thailand

Robert A. Samson ¹

     Centraalbureau voor Schimmelcultures, P.O. Box 85167, NL-3508 AD Utrecht, The Netherlands

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 

Nuclear-encoded small-subunit ribosomal DNA was used to examine phylogenetic relationships in Paecilomyces sensu lato. Phylogenetic analysis of the 18S nr DNA demonstrates that Paecilomyces is polyphyletic across two subclasses, Sordariomycetidae and Eurotiomycetidae. The type species, Paecilomyces variotii, and thermophilic relatives belong in the order Eurotiales (Trichocomaceae), while mesophilic species related to Paecilomyces farinosus are in the order Hypocreales (Clavicipitaceae and Hypocreaceae). One species, Paecilomyces inflatus, had affinities for the order Sordariales. Within the Eurotiales, Paecilomyces is monophyletic. Within the Hypocreales, species of Paecilomyces are polyphyletic, although the data failed to fully resolve these relationships.

Key words: 18S rDNA, anamorph-teleomorph connections, Clavicipitaceae, Hypocreaceae, Paecilomyces, phylogenetics, Trichocomaceae

	INTRODUCTION

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The hyphomycete genus Paecilomyces was established by Bainier (1907) for Paecilomyces variotii characterized by verticillate conidiophores with divergent whorls of phialides, which have a cylindrical or inflated base tapering to a long and distinct neck. The conidia are typically hyaline, one-celled, smooth-walled and are produced in basipetal chains. The genus was revised by Brown and Smith (1957) and modified by Samson (1974), who accepted 31 species. There has been no comprehensive review of the genus since, but more than forty species now have been recognized in the genus Paecilomyces.

Brown and Smith (1957) significantly transferred the insect-pathogenic Isaria farinosa (Holm ex S.F. Gray) Fr. to Paecilomyces and with it other entomogenous species previously classified in Isaria or Spicaria. Samson (1974) considered all entomogenous Isaria with flask-shaped phialides tapering abruptly to thin long necks and catenate conidia as Paecilomyces and proposed several further combinations that generally have been accepted.

The cleistothecial ascomycete Byssochlamys Westling (Eurotiales: Trichocomaceae) was first described by Westling (1909) and the connection of a Paecilomyces anamorph with Byssochlamys was made by Stolk and Samson (1972). P. fulvus Stolk & Samson was found to be the anamorph of B. fulva Olliver & G. Smith. Other links include: B. zollerniae Ram with P. zollerniae Stolk & Samson and B. nivea Westling with P. niveus Stolk & Samson. Within the Trichocomaceae, Paecilomyces also is linked with the gymnothecial Talaromyces (T. byssochlamydoides Stolk & Samson; P. byssochlamydoides Stolk & Samson and T. leycettanus Evans & Stolk; P. leycettanus [Evans & Stolk] Stolk, Samson & Evans). In addition, Samson (1974) recognized P. crustaceus Apinis & Chesters as the anamorph of the cleistothecial Thermoascus crustaceus (Apinis & Chesters) Stolk.

With the inclusion of mesophilic, entomogenous Paecilomyces, further teleomorph connections were added. For these species teleomorph associations were assumed to be clavicipitaceous and within the Hypocreales (Samson 1974) with Cordyceps and Torrubiella as purported teleomorph connections. While the clear connection with a teleomorph was established for the thermophilic Paecilomyces spp., the insect taxa were not so clear with many purported connections regularly being disproved. In particular, Petch (1936) refuted the connection between Cordyceps militaris (L. : Fr.) Link and P. farinosus (Holm ex S.F. Gray) Brown & Smith while that between P. tenuipes (Peck) Samson and C. takaomontana Yakusiji & Kumazawa became accepted. Hywel-Jones (1993) confirmed a link between P. cinnamomeus (Petch) Samson & W. Gams and Torrubiella luteorostrata Zimm.

Thus, Paecilomyces in this broad sense can be considered polyphyletic across two ascomycete orders, the Eurotiales and the Hypocreales. To investigate the order relationships of mesophilic and thermophilic isolates of Paecilomyces with teleomorph genera, the 18S region of rDNA was sequenced. A single hypothesis was advanced for testing: The genus Paecilomyces is polyphyletic at the order level.

	MATERIALS AND METHODS

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Fungi used. – Paecilomyces species and strains were selected from material collected in Thailand and from the CBS collection (TABLE I). Representatives of known or purported teleomorphs of Paecilomyces also were used where available. Isolates were grown on malt-peptone broth and incubated at optimum temperature (25, 30 or 40 C, depending on species) for 3–4 d.

DNA amplification. – Amplification of the 18S rDNA was done using universal primers NS1-NS24 (White et al 1990, Gargas and Taylor 1992). PCR reactions were performed in 50 µL volume comprising 1 unit SuperTaq (HT Technologies), 2.5 mM MgCl₂, 200 µM dNTP, 0.2 µM primer, 1xbuffer and 10–50 ng DNA template. The PCR was performed using GeneAmp PCR System 9700 (Applied Biosystems) programmed as: 4 min denaturation step at 94 C, followed by 35 cycles of 1 min at 94 C, 1 min at 52–55 C and 1.5 min at 72 C, with a final extension of 7 min.

DNA visualization, quantification and purification. – Success of PCR reaction was confirmed by ultraviolet fluorescence after agarose gel electrophoresis and ethidium bromide staining of 5 µL of the reaction mix. Single-band PCR products were purified using GFX Purification Kit (Amersham Pharmacia 27-9602-01) and quantified for sequencing using DNA Smart Ladder on a 1% agarose gel (Gibco BRL, ultrapure) stained with 0.5 µg mL^–1 ethidium bromide.

DNA sequencing. – DNA sequence reactions were performed using a BigDye Terminator Sequencing Kit. Additional internal primers used for sequencing were NS3, NS5, NS23UBCR and NS 20 UCB (Gargas et al 1992). The SeqMan software program was used to compile and edit multiple sequences generated from each template.

Sequence alignment and phylogenetic analyses. – A preliminary alignment of the sequences obtained from this study and GenBank was performed with ClustalW incorporated in BioEdit version 5.06 (Tom Hall, Department of Microbiology, North Carolina State University, Raleigh) using default parameters. The positions of some gaps in the output of this program were adjusted manually with BioEdit to maximize for homology. Alignment gaps were treated as missing data. Eight hundred seventy-four uninformative and ambiguous characters in the alignment were excluded. Maximum-parsimony analysis was done in PAUP version 4 b10, using heuristic methods with characters first defined as unordered and having equal weights. Successive weighting was done to select for more consistent characters. Relative support for resulting trees was obtained from bootstrap analyses (Felsenstein 1985) using 500 heuristic searches with groups occurring at 50% or greater frequencies being retained in the consensus trees. All heuristic searches were performed by tree-bisection-reconstruction branch swapping with 100 random sequence addition and MULPARS option in effect. To test the robustness of the branches of the tree consistency index (CI), homoplasy index (HI), retention index (RI) and rescaled consistency index (RC) were calculated. The trees were rooted with Cookeina spp. (Pezizales: Sarcoscyphaceae) as outgroup.

	RESULTS

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An initial dataset of 14 18S sequences was obtained by sequencing isolates of thermophilic fungi made from soil samples and other substrates in Thailand plus CBS (type) isolates. In the mesophilic section Isarioidea the BIOTEC culture collection contained ninety Paecilomyces isolates from insects; these isolates were augmented with mesophilic Paecilomyces isolates made available from CBS. Of these, 31 isolates representing 22 species of Paecilomyces sensu lato were sequenced for the 18S region. These Paecilomyces isolates and an in-house database of 18S sequences of other members of the Clavicipitaceae was augmented with sequences of comparable length from GenBank.

The data presented here is derived from preliminary analyses (data not shown) and is a subset selected to present the maximum information with the minimum of ambiguity. This dataset contains 70 taxa, including 26 taxa of thermophilic and mesophilic Paecilomyces or their teleomorphs. The sequences represent members of two Ascomycete subclasses, the Sordariomycetidae and the Eurotiomycetidae (Kirk et al 2001).

Initial analysis of this dataset yielded 1394 trees with a tree length of 762 (CI = 0.423, RI = 0.823; RC = 0.348; HI = 0.577). Successive reweighting based on the RC value yielded six equally parsimonious trees with a tree length of 224.39 (CI = 0.671; RI = 0.936; RC = 0.628; HI = 0.329). A consensus tree of these MPTs was used to generate bootstrap values. These values then were superimposed upon a cladogram of the best tree as determined by the Kishino-Hasagawa test (FIG. 1). A bootstrap analysis was generated by a full heuristic search of the six most-parsimonious trees of 70 taxa, taking 500 replications with 10 random sequence additions at a time.

View larger version (73K): [in this window] [in a new window]   FIG. 1. Phylogenetic relationships of Paecilomyces species with selected anamorphs and teleomorphs of ascomycete genera based on 18S rDNA sequences. The cladogram represented was the best tree obtained from Kishino-Hasegawa Test in PAUP* version 4b10. The percentages above the branches are the frequencies with which a given branch appeared in 1000 bootstrap replications. Bootstrap values less than 50% are not displayed. The letters in bold above the branches represent these splits H: Hypocreales split; E: Eurotiales split.

View larger version (62K): [in this window] [in a new window]   FIG. 2. Phylogenetic relationships of Paecilomyces species with selected anamorphs and teleomorphs of ascomycete genera based on 18S rDNA sequences. The phylogram represented was the resulting best tree from Kishino-Hasegawa Test. The letters in bold above the branches represent these splits: H: Hypocreales split; E: Eurotiales split. The vertical lines on the far right show the division of Paecilomyces into three major clades spreading over two subclasses, Sordariomycetidae and Eurotiomycetidae. The tree was rooted with Cookeina sulcipes and Cookeina tricholoma as outgroup

Within the Hypocreales, three significant clades (FIG. 2) were identified based on the families Clavicipitaceae, Hypocreaceae and Nectriaceae. Paecilomyces (11 species) were predominant in the Clavicipitaceae with two species—P. niphetodes and P. penicillatus—present in the Hypocreaceae. With the current dataset no Paecilomyces were associated with the Nectriaceae. Also within the Sordariomycetidae, P. inflatus was sister to a clade of the Sordariales with 97% support (FIG. 2).

Within the Hypocreales clade were species of Paecilomyces with known affinities for insects. A major subclade (Clade I) with a bootstrap support of 79% included a recent Danish isolate of P. farinosus that Samson (1974) recognized as the type species for Section Isarioidea. This isolate (CBS 111113), derived from a specimen of a Lepidoptera pupa (CBS 6856) collected close to the type locality of Isaria farinose, now serves as the epitype (K.T. Hodge, personal communication). From our analysis the sister clade containing P. amoeneroseus and P. cateniobliquus (clade I?) needs further comparison with P. farinosus because these also might be part of a larger Isarioidea clade. Clade P was another well-defined (although poorly supported) sister clade of Paecilomyces species . and allies. Two species—P. carneus and P. marquandii—had uncertain affinities within the Clavicipitaceae. Finally, within the family Hypocreaceae were two further Paecilomyces species from which appear to be derived Hypocrea.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Within the Ascomycetes, Paecilomyces appears to be polyphyletic at the subclass and ordinal level. While Oborniík, Jirku and Dolezel (2001) recognized that Paecilomyces is polyphyletic at the ordinal level, these authors included only species of the section Isarioidea. Thermophilic species based on the type of Paecilomyces belong with gymnothecial teleomorphs in the Eurotiales, while most mesophilic Paecilomyces and Paecilomyces-like genera belong in the Hypocreales.

Samson (1974) represents the most recent monographic treatment of Paecilomyces and related genera. This work was significant for its recognition that within Paecilomyces there are two distinct groups, placed in two sections; the thermophilic section Paecilomyces, based on the type species P. variotii, while section Isarioidea was reserved for mesophilic, generally entomogenous species but also nonentomogenous taxa. Our work confirms that Samson’s section Paecilomyces belongs with the Eurotiales while section Isarioidea is either poly- or paraphyletic at the order level within the Sordariomycetidae.

While many species of Paecilomyces are known, definite teleomorph connections have been established for a few. And yet six teleomorphs have been accepted for Paecilomyces indicating a polyphyletic nature. The genus Paecilomyces sensu lato thus presents problems similar to those previously considered for Penicillium (Berbee et al 1995) and Geosmithia (Ogawa et al 1997). Ogawa et al (1997) noted that "Penicillium never appears outside Trichocomaceae." This is in contrast to Geosmithia (Ogawa et al 1997) and now Paecilomyces (in this study). While Berbee et al (1995) demonstrated that Penicillium was polyphyletic; it nevertheless was polyphyletic only within the Trichocomaceae. Geosmithia (Ogawa et al 1997) and Paecilomyces (in this study) appear to be polyphyletic within and without the Trichocomaceae (Geosmithia) and within and without the subclass Eurotiomycetidae (Paecilomyces).

Within the Eurotiomycetidae, Paecilomyces has been associated with four ascomycete genera, Aphanoascus, Byssochlamys, Talaromyces and Thermoascus. Samson (1974) described Paecilomyces aerugineus based on material isolated by Apinis (1962). Our phylogeny places this close to Aphanoascus cinnabarinus (FIG. 2), which was reported to have a Paecilomyces anamorph (Jong and Davis 1975). Zukal (1890) described A. cinnabarinus from alligator dung. However, Apinis (1968) proposed A. fulvescens (Cooke) Apinis as the type of the genus, accepting A. cinnabarinus as a synonym. Later, Udagawa and Takada (1973) re-introduced by neotypification of A. cinnabarinus with the Paecilomyces anamorph described by Jong and Davis (1975). Currah (1985) considered the description of Udagawa and Takada (1973) and Jong and Davis (1975) of dagger-like spines on the ascospores and a Paecilomyces anamorph, but he did not accept the neotypification "since these features differ from Zukal’s protologue, and since Zukal’s type is available." Aphanoascus was recognized by Currah (1985) to have a Chrysosporium anamorph, and he placed this genus in the Onygenaceae. Yaguchi et al (1993) erected a new genus Chromocleista for the new species C. malachita and combined A. cinnabarinus as a second species. The type species of Chromocleista is a typical Eupenicillium (Frisvad and Samson, unpublished), and therefore the taxonomic status of A. cinnabarinus remains unsolved. P. aerugineus differs significantly from other Paecilomyces in having conidia surrounded by a mucilaginous layer. Based on its Aphanoascus affinities and the presence of mucoid conidia we do not consider this species to fit with Paecilomyces sensu stricto.

Udagawa and Suzuki (1994) described Talaromyces spectabilis with a Paecilomyces anamorph. However, the morphology and molecular data suggest that T. spectabilis is better placed in Byssochlamys (R.A Samson, unpubl data). Accepting this we then have Clade B as a Paecilomyces clade with Byssochlamys as the exclusive teleomorph.

While the thermophilic Section Paecilomyces was confined to the Eurotiales, we found that section Isarioidea was present in two orders of the Sordariomycetidae. P. inflatus was grouped with the Sordariales, although we could not place it in this order with confidence. Samson (1974) accepted this species as "the only monophialidic species of Paecilomyces." Isolate CBS 259.39 is the type culture of Myceliophthora inflata and was isolated from the abdomen of a honeybee (Samson 1974). The genus Myceliophthora has been associated with the teleomorphs Arthroderma and Ctenomyces (both Onygenales) and with Corynascus (Chaetomiaceae; Sordariales). P. inflatus needs to be compared, therefore, with Myceliophthora and Corynascus.

With the exception of P. inflatus, all other Paecilomyces of section Isarioidea (after Samson 1974) were within the Hypocreales. Most of these could be placed within the family Clavicipitaceae with two species placed in the Hypocreaceae. Both P. penicillatus and P. niphetodes were basal in the Hypocreaceae clade, which had 100% support. Our isolate of P. penicillatus significantly was from a mushroom, but the type specimen was found on dead moss and rotting wood and it grouped into a clade of fungicolous genera/species. P. niphetodes is known from decaying wood of Fagus sp. and Mercurialis perennis. Further work is needed to determine the teleomorph associations of these two species within the Hypocreaceae.

Within the Clavicipitaceae, Paecilomyces section Isarioidea also appeared to be polyphyletic as concluded by Oborník et al (2001). However, the genus Cordyceps is large and several phylogenies (Nikoh and Fukatsu 2000, Artjariyasripong et al 2001, Oborník et al 2001) suggest that it too is polyphyletic within the order Clavicipitaceae. We included two species of Cordyceps in our dataset. C. militaris (the type species) was sister to the Isaria clade (Clade I ), while C. takaomontana was placed well within Clade I with a bootstrap support of 79% and sister to P. farinosus (CBS 111113). We recognize Clade I as an Isaria clade based on the epitype P. farinosus (CBS 111113). Support for the C. militaris sister clade of Clade I, which contained P. amoeneroseus and P. cateniobliquus, was not strong at 58%. Other topologies (not shown) suggest also that P. amoeneroseus and P. cateniobliquus probably belong in an Isaria clade.

Another major clade (Clade P) that we identify in the Clavicipitaceae is based on pinkish or purple colonies or spores. In the phylogeny presented here, there is no support while other phylogenies (not shown) indicate a weak support of just over 50%. Within this clade P. cinnamomeus groups with a Torrubiella teleomorph as reported by Hywel-Jones (1993) and confirmed by phylogenetic analysis using the 28S region of the rRNA (Artjariyasripong et al 2001). Sister to this was a clade that included Nomuraea atypicola from spiders and P. lilacinus. A Cordyceps teleomorph is known for N. atypicola although no teleomorph has been reported for P. lilacinus. Although P. marquandii and P. carneus both are placed in the Clavicipitaceae, it was not possible to determine their relationships further based on the dataset available.

Our work clearly shows Paecilomyces to be polyphyletic at the order level. The genus Paecilomyces therefore should be retained only for eurotiaceous species with affinities for P. variotii and with a Byssochlamys teleomorph. Those within the Hypocreales fall in section Isarioidea of Samson (1974), but there is evidence that this section also is not monophyletic (Oborník et al 2001, this study).

	ACKNOWLEDGMENTS

 
This work was supported by the Biodiversity Research and Training Program in Thailand (BRT Grant No. BRT 143008) with co-financing from the National Center for Genetic Engineering and Biotechnology (BIOTEC). Angelina Kuijpers, Eric Dekker and Jos Houbraken kindly assisted with supplying strains and sequence data. Dr Richard Humber kindly supplied a Paecilomyces tenuipes strain from the ARSEF collection collected close to the type locality of Isaria tenuipes. Drs Mikako Sasa, Henning Knudsen and Thomas Læssøe kindly collected and isolated the epitype material of Isaria farinosa. We thank Dr Keith Seifert for his helpful comments to improve the manuscript.

	FOOTNOTES

 
Accepted for publication February 20, 2004.

¹ Corresponding author. Telephone: 030 2122656. Fax: 030 2512097. E-mail: Samson{at}CBS.knaw.nl

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This Article Abstract Full Text (PDF) Services Similar articles in this journal Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Luangsa-ard, J. J. Articles by Samson, R. A. Search for Related Content PubMed Articles by Luangsa-ard, J. J. Articles by Samson, R. A. Agricola Articles by Luangsa-ard, J. J. Articles by Samson, R. A.