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Sciences du bois et de la forêt, Faculté de foresterie et de géomatique, Université Laval, Québec, QC, G1K 7P4, Canada
B. Laitung 2
Department of Biology, Mount Allison University, Sackville, New-Brunswick, Canada
J.A. Bérubé
Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Centre, 1055 du P.E.P.S., P.O. Box 3800, Québec, QC, G1V 4C7, Canada
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ABSTRACT |
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Foam from eight streams in boreal and mixed-wood forests in Québec were sampled in early and late fall 2002 to evaluate the biodiversity of their aquatic hyphomycete communities. Two regions were studied: 53–54°N and 46–49°N. A total of 54 species were identified. Twenty taxa were found only in the northern region, and four were unique to the southern region. A new aquatic hyphomycete, Dwayaangam colodena sp. nov., was found mostly in northern streams. It is described along with its taxonomic position.
Key words: Arachnopeziza, biodiversity, freshwater fungi, Hyaloscyphaceae, ITS, Orbilia
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSTAXONOMYDISCUSSIONLITERATURE CITED |
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) or aquatic hyphomycetes are mitosporic fungi that live and sporulate in streams (Ingold 1942, Bärlocher 1992). This group is purely an artificial cluster and has no taxonomic value. However it is a convenient ecological concept based on the freshwater habitat and the plant litter decaying activity of these fungi. Hyphomycetes are the asexual states of mostly Ascomycetes and some Basidiomycetes. More than 300 species of aquatic hyphomycetes have been described, with only about 10% of them having a known sexual stage (Webster 1992, Sivichai and Jones 2003). They are responsible for the degradation of leaf litter in woodland streams (Gessner et al 1997, Suberkropp 1998). The biomass of aquatic hyphomycetes reaches up to 10–15% of the total detrital biomass (Gessner and Chauvet 1994) and 90% of the microbial biomass (Baldy et al 1995, Weyers and Suberkropp 1996).
The key paper by Ingold (1942) was followed by many surveys of aquatic hyphomycetes from different regions of the world (Ingold 1973, 1974; Miura 1974; Sinclair et al 1983; Descals and Chauvet 1992; Webster et al 1994; Descals et al 1995a, b; Descals and Moya 1996; Marvanová 1997a; Santos-Flores and Bétancourt-López 1997; Descals 1998). Descals and Webster (1981) compiled the worldwide distribution of all known aquatic hyphomycetes. To date only a few surveys of aquatic hyphomycetes have been conducted in boreal and arctic regions; Greenland, Alaska, Sweden, Finland, and one site of northern Russia have been partially explored (Nilsson 1962, Müller-Haeckel and Marvanová 1979, Marvanová and Müller-Haeckel 1980). Ingold (1960) reported the first observations of 15 aquatic hyphomycetes in eastern Canada, namely in the Gaspé Peninsula and in Mont Tremblant (Québec). Surveys of the Canadian streams are limited to mixed forests of Ontario (Bärlocher and Kendrick 1974), New Brunswick and Nova Scotia (Bärlocher 1987, 2000; Marvanová and Bärlocher 1988, 1989, 1998a, Marvanová and Bärlocher b, c, 2000, 2001; Garnett et al 2000) and a report of a Geniculospora sp. from Labrador (Nolan 1972). The aquatic fungal biota of the boreal forest in the Canadian Shield is still unexplored. In this study we have sampled streams distributed along a latitudinal gradient of 46–54°N in eastern North America. Many known and a few unknown hyphomycetes were observed. A new species found in half of the investigated streams is described and its phylogeny analyzed.
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MATERIALS AND METHODS |
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Time of sampling and conidial harvest.— – Northern streams were sampled in mid-Aug and mid-Sep 2002. The southern streams were sampled during the first days of September and again during the first days of October. These sampling periods correspond to the leaf fall season in each region. The late samplings in both regions were done after the first nocturnal frost.
Conidia of aquatic hyphomycetes can be observed and isolated from the foam formed at the surface of running water. The foam was collected with a narrow-mesh net (10 cm diam) attached to a wire frame. The water flows through while the foam was retained. One mL of foam was plated on 0.1% malt agar plus antibiotics, penicillin and streptomycin sulfate (Descals 1997). Fifteen to twenty mL were poured into a small jar and a few drops of FAA (formaldehyde/glacial acetic acid/ethanol 94%: 1/3/16) added (Descals 1997) for future identification and reference. Single conidia were located on the 0.1% malt agar within 6 h under an inverted microscope at 100x, carefully removed with a modified Pasteur pipette (Descals 1997), transferred to 2% malt agar (malt extract 2%, agar 1.5%, BD BactoTM) in a 90 mm Petri dish and incubated at 20 C.
Identification of aquatic hyphomycetes.— –
One mL of foam-FAA mixture was placed on a microscope glass slide, dried on a warm plate and stained with lacto-fuchsin (Descals 1997). Identifications of aquatic hyphomycete detached conidia were made at 400x magnification with a phase-contrast Reichert microscope. Drawings were done freehand, based on direct observations and photographs. Relative abundance of all species based on conidial numbers was recorded. Species richness is the number of identified species per site sampled.
Inducing aquatic hyphomycete sporulation.— –
To ascertain the identification of some of the species isolated, sporulation was induced from pure culture obtained from a single conidium and grown on 2% malt agar. Pieces of agar (5–8 mm x 20 mm) overgrown with the culture were placed in aerated sterile distilled water in a microcosm (Suberkropp 1991). Five mL of water from the microcosm were treated like the foam. Conidia were observed as described above.
DNA extraction, PCR, sequencing and sequence analysis.— –
A small plug (3–5 mm2) of the agar supporting the monosporal fungal culture in the Petri plate was used for extraction. DNA was extracted with a 2% cetyltri-methyl ammonium bromide (CTAB) procedure modified from Zolan and Pukkila (1986). Samples were crushed in 300 µL 2% CTAB 0.2%-ß-mercapto-ethanol at 65 C approximately 1 h, emulsified with 300 µL phenol: chloroform: isoamyl alcohol, and centrifuged at 9000 g 10 min. The supernatant was recuperated, precipitated with 300 µL of cold isopropanol, centrifuged at 2500 g 10 min, rinsed with ethanol 70%, dried and resuspended in 50 µL TE-8.
rDNA was amplified with the universal primer ITS-4 (White et al 1990) and the universal fungal primer ITS-1F (Gardes and Bruns 1993). The amplification cycle was performed on a MJ Research PTC-100 thermocycler. The PCR reaction mixture (25 µL volume) contained 20 mM TRIS (pH 8.4), 50 mM KCl, 3 mM MgCl2, 0.25 mM of each dNTP, 1 µM of each oligonucleotide primer, 1 unit TAQ polymerase (Invitrogen), and 3 µL of 1:10 dilution of ca. 10 ng/µL genomic DNA. PCR was as follows: 3 min at 94 C; 40 cycles at 92 C for 1 min, 56 C for 1 min, 72 C for 1.5 min, with a last cycle of 10 min at 72°C. Electrophoresis gels (1.4% agarose LE [Roche Diagnostics GmbH, Mannheim, Germany], in TAE 1x [Gibco]) were stained with ethidium bromide and photographed under UV light. The amplified DNA was purified with QIAquick PCR Purification Kit (QIAGEN, Sparks, Maryland) for sequencing.
Sequencing was done on a Genetic Analyzer ABI Prism 3100 (Applied Biosystem) sequencer. Sequences were aligned with Se-Al (Rambaut 1996, http://evolve.zoo.ox.ac.uk), Clustal X version 1.83 (Thompson et al 1997). Sequence lengths were adjusted to 465 nucleotides to include part of the 18S, the complete ITS1, 5.8S, ITS2 and part of the 28S of the ribosomal DNA. Molecular identification was performed with maximum parsimony using PAUP 4.0b10 (Swofford 2002). PAUP was conducted with a heuristic search with default parsimony settings; a random starting tree was obtained by 100 random stepwise additions and TBR (tree bisection-reconnection) branch-swapping; saved tree number was automatically increased by 100; all characters were unordered and equally weighted; gaps were treated as missing data; bootstrap analysis was done with 1000 resamplings and 100 additional sequence replicates to estimate the robustness of the trees. Bayesian analysis was performed with MrBayes 3.0b4 (Huelsenbeck and Ronquist 2001): Four Markov chains were run over 1 000 000 generations, sampling trees every 100th generation (10 000 trees saved) and the burnin value was set to 1000. The number of substitution type (nst) was set to 6 (GTR model). Sequences of aquatic hyphomycetes were deposited in GenBank. They were compared in a BLASTn with sequences in GenBank. Sequence alignments are available at http://www.treebase.org/treebase/index.html (accession number: S1524, matrix M2734).
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RESULTS |
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). Fifty-four hyphomycete species were identified from the eight sites. In addition 11 fungal taxa remained unidentified and were found mostly in northern streams (data not shown). Because of their scarcity none of the unidentified conidia could be isolated. The early samples showed a lower number of species and fewer conidia of each species; hence results of both samplings of the same site were analyzed together.
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). The total number of southern stream-identified species observed in foam were Valcartier 29, Écorces 6, Chigoubiche 22 and Noire 17. In northern streams they were Mintuwataw 26, Kapichinikaw 35, Castor 36 and Asasuch 31 (TABLE I). Southern streams together had 34 species. A total of 54 species were identified including an unknown species with stauroconidia. It was observed in four of the streams, and we describe it as a new species. |
TAXONOMY |
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Holotypus: CBS 118913
Etymology: modified from the Russian word for cold, with reference to the boreal habitat.
Conidia stauroform, hyaline, multicellular, spanning out 80–110 µm. Septa distinct in lacto-fuchsin. Secession presumably schizolytic. Conidium main axis in stream foam, 2–4 septate, 15–22 µm x 1.5 µm at the thinnest part to 5 µm at the apex. The conidial axis forms a primary short dichotomy at its apex. Each arm of this dichotomy forms a secondary dichotomy, which becomes asymmetrical while its proximal arm forms a tertiary dichotomy whereas the distal arm remains unbranched. Usually six arms, sometimes five, rarely four, 30–55 µm x 3–5 µm each, usually tapering at the end, resulting in a 6–7-pike conidium.
Cultures. – Pure culture from one conidium on MA 2% (malt extract 2%, agar 1.5%, BD BactoTM) at 20 C: Colony slow growing (3–5 mm/mo to a maximum of 3 cm diam). Dense, white becoming yellowish white to yellowish brown, margin irregular. Sometimes with white sectors developing with age. Hyphae septate, hyaline. Conidiophores not seen. Sporulation erratic and sparse on 2 mo old colony slivers (MA2%) submerged in aerated sterile distilled water. No conidia produced in standing water or on malt agar.
Ecology. –
D. colodena has been observed in boreal stream foam and isolated as an important needle endophyte of P. mariana (Sokolski et al 2006).
Known distribution. – D. colodena has been observed in foam from these streams in Quebec (Canada): Chigoubiche, Asasuch, Castor and Kapichinikaw.
Phylogeny. –
The phylogenetic analysis (FIG. 2) includes the closest ITS sequences available in GenBank, Arachnopeziza aurata U57496
[GenBank]
, a member of the Hyaloscyphaceae. Because Dwayaangam junci Kohlm., Baral et Volkm.-Kohlm has a teleomorphic stage in the Orbiliaceae, some Orbilia spp. were included in the analysis. Mollisia sp. AY354269
[GenBank]
was outgroup. The Bayesian and the parsimony trees showed identical topologies (FIG. 2) when bootstrap values > 50% and Bayesian probabilities > 0.75% were considered. The Bayesian analysis of the ITS places D. colodena close to the Hyaloscyphaceae.
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Paratype of D. colodena. CANADA, QUÉBEC: Valcartier. Isolated from Picea mariana fresh needles. Monosporal V3.10B. 17 Oct 2003, Sokolski (CBS 118912).
Comments. –
Dwayaangam colodena conidia showed some variation during the 6 mo incubation of the fungus on P. mariana needles as substratum in aerated water in microcosm. Sporulation is greatly affected by artificial bubbling, water quality and possible by-product accumulation between water changes. We observed that cells tend to swell and conidia to break apart. The conidial main axis shortens and becomes one-celled when sporulation is induced in vitro for more than 1 mo or from an old culture (FIG. 3). Without water changes sporulation rapidly decreases. After 30 d incubation in aerated distilled water in microcosm, pure cultures on malt agar slivers produced conidia for 1 mo. The low sporulation rate gave a peak production of two conidia per mL of water per day, with an average of one per mL. The production of conidia stopped in 1 mo.
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DISCUSSION |
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, Chauvet 1992) and the rate of conidial production varies widely among species. Collecting aquatic hyphomycete conidia by membrane filtration gives a more accurate representation of various conidial types occurring in the column (Shearer and Webster 1985). Nevertheless analysis of stream foam remains a quick and easy method to evaluate the species richness of a stream (Descals 1997) and made it possible to provide the first overview of species richness and distribution of aquatic hyphomycetes along a significant north-south gradient in a conifer-dominated environment. The Écorces stream had a significantly low number of species compared with the other sites. At the sampling site the Écorces stream became wider before entering a pond and foam was scarce, indicating probable poor water aeration, which might explain such a difference.
The total number of species identified in this study, 54, is comparable to the results in other surveys (Bärlocher and Kendrick 1974; Miura 1974; Sinclair et al 1983; Marvanová 1984, 1997b; Bärlocher 1987, 2000; Descals 1987; Gönczöl and Révay 1992; Descals et al 1995a, 1995b; Harrington 1997; Laitung and Chauvet 2005). Other studies of foam in arctic region streams (Marvanová and Müller-Haeckel 1980) reported 17 species in common with those found in Québec. Most of the species identified in this study have been mentioned in other surveys, including Bärlocher (1987, 2000). However six species are first records for North America: Anguillospora rosea, Colispora elongata, Flagellospora fusarioides, Gemmulina botryosa, Porocladium aquaticum, Tricellula taiwanensis plus the newly described species, Dwayaangam colodena.
Six out of the eight streams are surrounded by spruce species (Picea spp.), and most of the riverbanks are lined with alder (A. rugosa). Seven of the aquatic hyphomycetes known to have an endophytic phase in Picea glauca (Moench) Voss. roots were recorded in this study: Articulospora tetracladia, Geniculospora sp., Heliscus lugdunensis, Mycocentrospora sp., Tetracladium setigerum, Varicosporium elodeae and V. giganteum (Sridhar and Bärlocher 1992a, b). Roots of Alnus glutinosa (L.) Gaertner also are hosts of endophytic aquatic hyphomycetes (Fisher et al 1991, Marvanová et al 1997). Among these hyphomycetes, eight were recorded in stream foam from Québec forests: A. tetracladia, Clavariopsis aquatica, H. lugdunensis, Lunulospora curvula, Mycocentrospora sp., Tricladium splendens, V. elodeae and Fontanospora fusiramosa. More aquatic hyphomycetes are likely to be found as endophytes in roots or aerial plant parts.
The northern streams we sampled flow mainly through woodlands dominated by one tree species. They harbor 50 identified species (TABLE I) and 11 unidentified taxa (data not shown). This relatively high number of species identified from northern sites compared to the southern sites seems to contradict the results of Laitung and Chauvet (2005). These authors observed a clear relation between riparian vegetation richness and the 79 aquatic hyphomycete species in 10 streams over a year in southwestern France. More samples, combining water filtration and foam observations over longer periods in both regions will be needed to understand this phenomenon.
D. colodena taxonomy.— –
The genus Dwayaangam has been established by Subramanian (1977) on the basis of Triposporina quadridens Drechsler. Hitherto described species of the genus are D. quadridens (Drechsler) Subram. (Subramanian 1977), D. yakuensis (Matsush.) Matsush. (Matsushima 1981), D. cornuta Descals (Descals and Webster 1982), D. dichotoma Nawawi (Nawawi 1985), D. heterospora GL Barron (Barron 1990), D. gamundiae Cazau, Arambarri et Cabello (Cazau et al 1993), D. junci Kohlm., Baral et Volkm.-Kohlm. (Kohlmeyer et al 1998). D. colodena, where a threefold dichotomous branching of conidia including one deficient dichotomy is the norm, departs from the other species with typically twofold dichotomies. However threefold dichotomies also were observed in D. cornuta and D. yakuensis but only as exceptions. (For comparisons between Dwayaangam species conidia see Kohlmeyer et al [1998]). Nevertheless, in spite of the peculiar shape of the conidia of D. colodena, this species is closer to this genus than any other. Neither sequence nor cultures of other Dwayaangam spp. were available. Therefore it was impossible to compare the sequences. Orbilia junci Kohlm., Baral et Volkm.-Kohlm., teleomorph of Dwayaangam junci, had no sequence in GenBank/EMBL. The closest Orbilia spp. ITS rDNA sequences available were included in the phylogenetic analysis (FIG. 2). Because the available sequences of Orbilia spp. show absolutely no correspondence with those of D. colodena, we cannot assume of a teleomorphic stage in Orbilia or even Orbiliaceae. Its phylogenetic relatedness with Arachnopeziza aurata (FIG. 2), the closest species according to GenBank, tends to temporarily classify it in the mitosporic Hyaloscyphaceae. The anamorphic genus Dwayaangam probably is present in more than one teleomorphic genus.
D. colodena geographical distribution –
Dwayaangam colodena is present in stream foam and has been observed in most of the rivers sampled in the northern as well as the southern parts of the Quebec boreal forest. Similarly shaped but smaller conidia were reported from mountain streams of Scotland by Ingold (1965, 1973, 1974). A similar conidium from Catalonia is presented as a probable Dwayaangam sp. by Descals and Moya (1996). Because no cultures or collections are available we lack data to confirm that they belong to the same species, thus the distribution outside Canada of D. colodena remains questionable.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 Present address: UMR 1210, Université de Bourgogne- Institut National de la Recherche Agronomique-ENESAD, 21065 Dijon, France. 
1 Corresponding author. E-mail: serge.sokolski.1{at}ulaval.ca
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