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Department of Botany, 3529-6270 University Blvd., University of British Columbia, Vancouver, British Columbia, V6T 1Z4 Canada
Somsak Sivichai
BIOTEC-Mycology, National Center for Genetic Engineering and Biotechnology, National Science and Technology Development Agency, Science Park, 113 Paholyothin Road, Klong 1, Klong Luang, Pathumthani 12120, Thailand
Mary L. Berbee
Department of Botany, 3529-6270 University Blvd., University of British Columbia, Vancouver, British Columbia, V6T 1Z4 Canada
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ABSTRACT |
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Three genera of asexual, helical-spored fungi, Helicoma, Helicomyces and Helicosporium traditionally have been differentiated by the morphology of their conidia and conidiophores. In this paper we assessed their phylogenetic relationships from ribosomal sequences from ITS, 5.8S and partial LSU regions using maximum parsimony, maximum likelihood and Bayesian analysis. Forty-five isolates from the three genera were closely related and were within the teleomorphic genus Tubeufia sensu Barr (Tubeufiaceae, Ascomycota). Most of the species could be placed in one of the seven clades that each received 78% or greater bootstrap support. However none of the anamorphic genera were monophyletic and all but one of the clades contained species from more than one genus. The 15 isolates of Helicoma were scattered through the phylogeny and appeared in five of the clades. None of the four sections within the genus were monophyletic, although species from Helicoma sect. helicoma were concentrated in Clade A. The Helicosporium species also appeared in five clades. The four Helicomyces species were distributed among three clades. Most of the clades supported by sequence data lacked unifying morphological characters. Traditional characters such as the thickness of the conidial filament and whether conidiophores were conspicuous or reduced proved to be poor predictors of phylogenetic relationships. However some combinations of characters including conidium colour and the presence of lateral, tooth-like conidiogenous cells did appear to be predictive of genetic relationships.
Key words: Acanthostigma, aero-aquatic, Dothideomycetes, Drepanospora, freshwater fungi, mitosporic fungi, Thaxteriella, Tubeufia, phylogeny
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONLITERATURE CITED |
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). They often are reported from terrestrial and freshwater environments (Nakagiri and Ito 1995, Tsui et al 2001b, Sivichai et al 2002). The aquatic species are considered aero-aquatic fungi because they exploit the decaying leaves in streams and ponds and their conidia form upon exposure to air (Kendrick 2003). Several aquatic isolates were capable of producing cellulases and xylanases (Yuen et al 1998, Bucher et al 2004), suggesting that they might contribute to wood and litter decay within freshwater ecosystems (Bucher et al 2004). Some strains of Helicomyces and Helicosporium produce bioactive compounds (Hanada et al 1996, Ohtsu et al 2003) with potential uses in biotechnology.
These fungi have been the subject of systematic studies because they are morphologically diverse and form unusual but elegant conidia for reproduction (Goos 1987). Helicoma produces nonhygroscopic, helically coiled conidia with thick conidial filaments and currently comprises ca 32 species (FIG. 1) (Goos 1986, Tsui et al 2001a, Kirk et al 2001). Helicoma sensu Linder (1929) is heterogeneous (Pirozynski 1972, Goos 1986) and polyphyletic (Tsui and Berbee 2006). Goos (1986) attempted to delineate the genus and divided it further into four sections, helicoma, atroseptatum, violaceum and monilipes, based on conidial characteristics and mode of conidium attachment (Goos 1986). The monophyly of the first three of these sections had not been tested with molecular phylogenetics. A phylogeny from SSU and partial LSU ribosomal gene data showed that sect. monilipes was clearly polyphyletic and three representatives had evolved independently from lineages outside of the Tubeufiaceae s. str. (Tsui and Berbee 2006). Conidia of Helicomyces and Helicosporium are relatively thin-walled and more hygroscopic (e.g. FIG. 2c, f, h) but are otherwise similar to those of Helicoma (Goos 1985, 1989). Helicosporium was distinguished from Helicomyces primarily by conidiophore morphology. Helicosporium has well developed, conspicuous conidiophores (e.g. FIGS. 2a, d, e; 3a), while those in Helicomyces are reduced or even lacking (e.g. FIGS. 2g, 3c) (Goos 1985, Goos 1989). Pirozynski (1972) and Goos (1989) recognized that the separation based on these morphological characters needed re-evaluation.
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). The teleomorphic genera are distinguished primarily on ascomata morphology (Barr 1980, Rossman 1987, Crane et al 1998). Thaxteriella produces brown to black ascomata and the type species is linked to a Helicoma anamorph (Pirozynski 1972), while Tubeufia species are more reddish and brightly colored and the type produces a Helicosporium anamorph (Barr 1980, Goos 1989). Acanthostigma species can have either Helicomyces or Helicosporium anamorphs but unlike the other genera their ascomata have setae (Réblová and Barr 2000, Kodsueb et al 2004). These generic concepts remain confusing and poorly investigated (Pirozynski 1972, Samuels et al 1979, Crane et al 1998, Réblová and Barr 2000), and Thaxteriella is variously retained as a distinct genus or made a section within Tubeufia. Tubeufia helicoma and Tubeufia amazonensis have been transferred to Thaxteriella (Crane et al 1998). Tubeufia clintonii recently was synonymized with Acanthostigma perpusillum (Réblová and Barr 2000).
To devise a natural classification, ideally, any morphological or molecular characters of the anamorph that indicate teleomorph affinities should be considered in generic delimitation (Seifert 1993, Seifert and Samuels 2000). The large hypocrealean genus Calonectria and its allies were segregated into a series of monophyletic genera that each had a distinctive anamorph and support from molecular data (Rossman et al 1999, Rossman 2000, Schoch et al 2000). Anamorph genera, along with molecular data, were useful also in delineating sections in Mycosphaerella (Crous et al 2000, 2001). Anamorph characters are not always phylogenetically informative, however and they did not always separate Ophiostoma from Ceratocystis (Hausner et al 2000).
Analysis of conserved ribosomal SSU and partial LSU data has shown that most species of Helicoma, Helicosporium and Helicomyces, and Tubeufia sensu (Barr 1980) are close relatives, clustering with strong bootstrap support in a clade designated "Tubeufiaceae s. str." (Tsui and Berbee 2006). In this study we sampled helicosporous fungi from each of these three genera as broadly as possible. We then analyzed sequences from the variable ITS regions and partial LSU regions with the goal of dividing the helicosporous species in the Tubeufiaceae into well supported clades. We sought morphological characters that correlated with monophyletic groups and compared the traditional genera with monophyletic groups identified by molecular analysis.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONLITERATURE CITED |
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). We sampled as many species as possible and included most of the available cultures from major public collections in the experiment. Cultures were maintained on PDA (potato-dextrose agar) or MEA (malt-extract agar) for a month. Sporulation of cultures was induced by inoculation onto SNA (synthetic nutrient-poor agar) (KH2PO4, 1 g; KNO3, 1 g; MgSO4·7H2O, 0.5 g; KCl, 0.5 g; glucose, 0.2 g; sucrose, 0.2 g; yeast extract, 0.5 g; agar, 20 g; distilled water, 1l) with sterile filter paper to confirm identities. Authentic and type specimens of helicosporous hyphomycetes also were borrowed from the Farlow Herbarium, Harvard (FH), and the New York Botanical Garden (NYBG) and compared with those sporulated in cultures for confirmation.
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).
Phylogenetic analysis.— –
Sequences were aligned with Clustal X (Thompson et al 1997) (distributed by the authors, <ftp://ftp-igbmc.u-strasbg.fr/pub/ClustalX/>) and adjusted manually with Se-Al v.1 d1 (Rambaut 1999). The alignment was analyzed with PAUP* 4.0b10 (Swofford 2003). Maximum parsimony (MP) analyses were conducted with a heuristic search with 1000 random-sequence addition replicates, TBR branch swapping algorithms, and MULPARS option on. All characters were equally weighted, unordered, and gaps were treated as missing data. Bootstrap support for the branches was based on 1000 MP heuristic searches with two random sequence addition replicates for each bootstrap replicate. We included sequences from Helicoon gigantisporum in the analysis because it is closely related to taxa within Tubeufiaceae s. str. Helicoma isiola (AY856890
[GenBank]
) and Cenococcum geophila (AY112935
[GenBank]
) were chosen as outgroups (Tsui and Berbee 2006). Maximum likelihood (ML) analysis was performed with a "general time-reversible + gamma distribution + invariants" model of molecular evolution. Under this model the proportion of invariable site was 0.452 and the gamma shape parameter was 0.59.
Bayesian inference of phylogeny was calculated with MrBayes v. 3.0 (Huelsenbeck and Ronquist 2001) with the general time reversible model of substitution and among site variation described by a gamma distribution. Four simultaneous Markov chains were run from random starting trees for 1 000 000 generations and sampled every 100 generations (generating 10 001 trees). The first 5000 trees were discarded as burn-in, hence inferences of posterior probability were calculated from 5001 trees.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONLITERATURE CITED |
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). The closest match to a LSU sequence from Helicomyces scandens was a Hymenoscyphus sp. (Leotiomycetes). Because it was unrelated to taxa within Tubeufiaceae s. str. we did not include the H. scandens sequence in the final analysis. The dataset consisted of 47 taxa, 683 characters from ITS, and 638 characters from partial LSU.
The ML tree (–lnL 9874) shows seven major clades, each receiving 78% or more parsimony bootstrap support (FIG. 4). Parsimony analysis of the dataset resulted in 45 trees (1744 steps). Out of 1321 characters, 811 characters were constant and 382 were parsimony informative. In a separate MP analysis of the ITS regions alone for 43 taxa plus outgroup 17 trees were found (length = 1361 steps). The trees from ITS dataset had same topology as those from the full dataset but some branches received lower bootstrap support, so we focused on the trees from the combined data for discussion. The MP trees and the ML trees had similar groupings. The main differences were in the placement of Helicosporium gracile, H. guianensis, H. citreo-viride and Helicosporium sp. (CT43). Helicosporium gracile formed a sister relationship with Clade G with 79% bootstrap support in the MP tree. The other three Helicosporium spp. also formed a monophyletic group with Clade G and H. gracile but without bootstrap support in the MP trees. The 50% consensus tree from Bayesian analysis matched the topology from ML. The present data do not support Thaxteriella as monophyletic cluster (FIG. 4).
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). Each of the three clades that contained the type species of an anamorphic genus also contained at least one species of another genus (FIG. 4). No clades corresponded well to the current circumscriptions of Helicoma, Helicomyces, and Helicosporium, or to any of the four sections established in Helicoma. Species of Helicoma were scattered and distributed in five clades. Helicosporium species also were distributed into at least five clades. Helicomyces appeared polyphyletic and five species were distributed among three clades. Within the Tubeufiaceae, the anamorphic genera appeared to have little predictive value for phylogeny.
Identification issues.— –
Several isolates (TABLE I) began to sporulate on SNA, on pieces of sterile filter paper, after 4 wk. We compared the morphological features of these isolates with their descriptions from literature and with type or authentic specimens when available. In some cases phenotypic characters confirmed identification, even though ITS sequences did not differentiate between species. Conidia and conidiophores of Helicoma conicodentatum and H. ambiens were different in shape and size but they had identical ITS sequences. In Clade E Helicoma morganii and H. violaceum also had identical ITS sequences but their conidia differed in the number of septa.
It was impossible to confirm the identity or reconcile the inconsistencies between morphological and molecular data for cultures that remained sterile. For instance four isolates of Helicosporium vegetum were divided into two sister groups. Two isolates of Helicosporium vegetum from Thailand (CT110, 116) produced pale yellow to subhyaline conidia that were not as yellow as those from the type specimens. Based on ITS sequence divergence, these two isolates may represent a different species from isolates CT76 and CT58, which did not produce conidia on agar. In Clade A two Thaxteriella helicoma isolates did not form a monophyletic clade. Thaxteriella helicoma (CT65) produced a Helicoma-like anamorph, but its identity could not be verified without ascus and ascospore characters. Thaxteriella helicoma UBC F13877 [GenBank] clustered with Helicoma muelleri, which also did not sporulate on agar. The voucher specimen of Thaxteriella helicoma UBC F13877 [GenBank] was scanty and identification could not be unequivocally verified.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONLITERATURE CITED |
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). For this study we selected as many isolates as possible from species expected to be in the Tubeufiaceae s.str. These included 12 of the ca. 32 total species of Helicoma, 14 of the ca. 20 species of Helicosporium and five of the ca. 12 species of Helicomyces (Kirk et al 2001). Few of these species had been studied with molecular phylogenetics. All representatives of Helicosporium, Helicoma and Helicomyces, except Helicomyces scandens, did group with Tubeufiaceae s. str.. This confirmed that morphological characters of the helicosporous anamorphs in these three genera correctly predict relationships at the family level.
Below the level of the family the monophyly of Tubeufia sensu Barr (1980) is supported. In this broad sense, Tubeufia includes a list of genera (e.g. Thaxteriella, Acanthostigma) (FIG. 4). These taxa share conserved characters such as bitunicate asci and transversely multiseptate, hyaline ascospores. However the anamorph genera do not correspond to phylogenetic groups. This lack of correspondence indicates that the morphological characters of the conidia and the conidiophores that were used to define genera were difficult to interpret or have undergone convergent evolutionary change.
Conidial morphology.— –
Thickness of the conidial filament was considered important in distinguishing Helicoma from Helicosporium and Helicomyces (Linder 1929, Moore 1954, Goos 1986). Another Helicoma character, the presence of nonhygroscopic conidia, was difficult to interpret because the ability of conidia to uncoil when wet seemed to depend on age. These conidial characters did not help identify monophyletic groups. Helicoma species with thick conidial filaments were distributed among five out of the seven strongly supported clades in the Tubeufiaceae. Additional Helicoma species evolved independently in other fungal lineages in the Dothideomycetes, outside the Tubeufiaceae (Tsui and Berbee 2006). Representatives from three Helicoma sections were included in this investigation but only Helicoma sect. helicoma seemed to predict genetic relationships at all. Taxa in sect. helicoma produce brown conidia with U-shaped or V-shaped basal cells (FIG. 1b–d) (Goos 1986, Carris 1989). Four species in this section clustered in Clade A. Even sect. helicoma was not monophyletic and Helicoma vaccinii clustered in Clade G while Helicoma chlamydosporum grouped with Helicoon gigantisporum with 93% support (FIG. 4). Helicoma chlamydosporum has muriform chlamydospores (FIG. 1e) (Shearer 1987) and does not resemble Helicoon gigantisporum with its barrel-shaped conidia (Goh and Hyde 1996). Section violaceum contained species with conidia that are broadly attached to the conidiophores and that bear scars when detached (FIGS. 1f, g; 3e, f ) (Goos 1986). Five species from sect. violaceum were distributed in three clades. Helicoma violaceum, and Helicoma morganii clustered with 100% bootstrap support in Clade E along with species of Helicomyces and Helicosporium. Helicoma sp. (CT100) was in Clade C even though it produced hyaline, acrogenous conidia like those of H. morganii and H. violaceum from Clade E. Helicoma palmigenum, from sect. monilipes, produced brown conidia (Goos 1986) but clustered with Helicosporium indicum that had hyaline conidia (Goos 1989) with a high Bayesian posterior probability.
Drepanospora was established to accommodate Helicosporium spp. with thick conidial filaments (>5 µm) and secondary conidia (Pirozynski 1972). The genus was considered as an intermediate between Helicosporium and Helicoma and it contained two species. Goos (1989) transferred Helicosporium linderi to Drepanospora pannosa but this species appears in Clade A, nested among other Helicoma species with 91% bootstrap support. The phylogenetic position of Drepanospora will remain unresolved until molecular data from the second (type) species are available.
Conidial color did appear to correlate with clades. Five out of seven well supported clades contained species that shared the same conidial color. Clade A contained species producing brown to pale brown conidia, while taxa in Clade G produce yellow or hyaline conidia. Conidia from most species in clades B, C, D and E are hyaline (FIGS. 2f, h; 3e, f ). However there are exceptions and the predictive relationships may not hold when more taxa are included. Both Helicoma pulchra and Helicoma perelegans (as Helicoma intermedium in ATCC 22621) produce brown conidia of a similar shape and size (FIG. 1f, g) (Goos 1986, Casteñeda Ruíz et al 1998), but they did not form a monophyletic lineage or cluster with Clade A. Helicoma perelegans was basal in Clade C and the phylogenetic position of H. pulchra was unresolved.
Conidiophore morphology and conidiogenesis.— –
Helicosporium (FIG. 2a, d, e) has been distinguished from Helicomyces (FIG. 2g) by its erect, elongate and conspicuous conidiophores (Linder 1929, Goos 1989), but the conidiophore features do not correlate well with clades. Multiple species of Helicosporium and Helicomyces occur in numerous, well supported clades throughout Tubeufiaceae s. str. (FIG. 4).
Molecular data revealed several small clusters with species from both Helicomyces and Helicosporium (FIG. 4). Helicosporium talbotii grouped with Helicomyces roseus in clade B and Helicosporium griseum (FIG. 3a) with Helicomyces bellus (FIG. 3c) in clade E. Also in clade E, Helicomyces torquatus (producing conidia with the largest diameter) (Lane and Shearer 1984, Goos 1985) was related to Helicosporium panacheum. Whether the conidiophores are reduced or lacking or erect and conspicuous are unreliable characters for generic differentiation.
Pirozynski (1972) proposed dividing the species of Helicoma into two groups based on conidiogenesis. The first group produced acrogenous conidia from sympodial, denticulate conidiogenous cells (FIG. 1a), while the second group contained species with affinities to Helicosporium and Drepanospora (FIG. 2b, d) producing conidia from proliferating pegs borne laterally on setiform conidiophores (Pirozynski 1972). Our molecular data do not fully support his proposition, but species in his first group are concentrated in Clade A.
Lateral, tooth-like/denticulate conidiogenous cells on conidiophores were features of Pirozynski’s (1972) second group (FIGS. 2d, 3a–d) but occurred in three clades D, E and G. All taxa in Clade D and four taxa in Clade E produce tooth-like conidiogenous cells pleurogenously and have hyaline, multiseptate conidia, showing that these characters are either plesiomorphic or convergent. Helicosporium guianensis and H. citreo-viride have pleurogenous, bladder-like conidiogenous cells (FIG. 2e) and also grouped together even though without strong bootstrap support.
Some combinations of morphological features seemed to be phylogenetically predictive. For example most taxa in Clade A have denticulate, sympodial, acrogenous conidiogenous cells and produce brown conidia on brown conidiophores. Species in Clade D produce hyaline conidia and possess lateral, tooth-like conidiogenous cells on hyaline conidiophores. However Clade E is heterogeneous, having representatives from three genera with diverse morphological features (FIG. 3). Species in Clade E shared no common features except hyaline conidia (FIG. 3e, f).
Implications for nomenclature.— –
rDNA phylogenies cast doubt on the separation of Thaxteriella from Tubeufia. Thaxteriella was erected based on perithecial characters including color (Crane et al 1998), but the differences in morphology were not corroborated by sequence data. Instead of forming a clade with Thaxteriella helicoma, Thaxteriella amazonensis (=Tubeufia amazonensis) grouped in Clade D with the type species of Tubeufia with 92% bootstrap support (FIG. 4). Thaxteriella perhaps should be synonymized with Tubeufia but a reexamination of the type specimen of Thaxteriella remains to be done.
The clustering of an isolate representing the type species of Acanthostigma, A. perpusillum (=Tubeufia clintonii) in Clade G along with Tubeufia cerea with 97% bootstrap support is problematic. The Tubeufiaceae was erected in 1979 based on Tubeufia, which was described in 1897 (Barr 1979). Acanthostigma, erected in 1863, had been considered a synonym of Nemastoma within Pseudoperisporiaceae until recently being redescribed and placed in the Tubeufiaceae (Réblová and Barr 2000). If Clades A–G are to comprise a single genus (FIG. 4) all species of Tubeufia would have to be transferred to Acanthostigma, which has priority as a generic name. This could result in numerous, undesirable name changes. Recognizing two teleomorphic genera, Tubeufia for species in Clades A–F and Acanthostigma for Clade G, might partly solve the problem. However the current circumscription of Acanthostigma does not accommodate T. cerea. The phylogenetic relationships of other Acanthostigma species perhaps should be investigated to determine whether they form a monophyletic group that includes the type. Our data from a broad sampling of Tubeufia species including the type species and associated anamorphs should facilitate future investigations of whether Thaxteriella or Acanthostigma and Tubeufia could be recircumscribed as monophyletic genera.
For some fungi including Mycosphaerella (Crous et al 2001) and Calonectria (Rossman et al 1999, Rossman 2000, Schroers 2000) anamorphic genera could be delineated so that they correlated with phylogenetic groups. In Tubeufia establishing phylogenetically based anamorphic genera will be difficult. Based on the genus-for-genus hypothesis (Rossman 2000) Tubeufia sensu Barr (1980) should be correlated with one anamorph genus. This would require transferring all taxa of Helicosporium and Helicoma into Helicomyces, which is the oldest genus of helicosporous fungi. This unfortunately would involve a large number of name changes and would create a large, morphologically heterogeneous genus. The Tubeufiaceae contains anamorphs that are not helicosporous (Barr 1980) and their phylogenetic relationships to the seven clades established in this investigation remain unknown. It might be beneficial to include these nonhelicosporous fungi, as well as additional teleomorphic taxa, in future molecular systematics studies before revising nomenclature.
Many dematiaceous hyphomycetes develop reduced, atypical conidiophores under some nutritional conditions (Shearer 1987). The degree of mycelial maturity can affect the extent of branching, making it difficult to tell whether the conidiogenous cells are on repent hyphae or on erect conidiophores and thus making it difficult to distinguish Helicomyces from Helicosporium. This may explain why a fungus identified as "Helicomyces bellus" was identical in ITS sequence to Helicosporium griseum. It similarly may explain why one isolate of Helicomyces roseus (type species of Helicomyces) was in Clade B, clustering with a Helicosporium, while the second fell in Clade C. Neither Helicomyces isolate sporulated well in culture, so we were unable to tell which was correctly named.
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CONCLUSION |
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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1 Corresponding author. E-mail: clement{at}mail.botany.ubc.ca
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