Phylogenetic Relationships of the Marine Gasteromycete Nia Vibrissa
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Mycologia, 93(4), 2001, pp. 679-688. ? 2001 by The Mycological Society of America, Lawrence, KS 66044-8897 Phylogenetic relationships of the marine gasteromycete Nia vibrissa Manfred Binder INTRODUCTION David S. Hibbett1 Several lines of evidence suggest that fungi arose Biology Department, Clark University, Worcester from flagellated, aquatic ancestors and, along with Massachusetts 01610 USA plants, were among the first eukaryotes to colonize the land (Pirozynski and Malloch 1975, Berbee and Hans P. Molitoris Taylor 1993). Ascomycetes and basidiomycetes radi- Department of Botany, University of Regensburg, ated extensively in terrestrial ecosystems and now 93040 Regensburg, Germany comprise about 85% (60 000 species) of the known fungi (Hawksworth et al 1995). A few groups of fungi have secondarily become aquatic, including four gen- Abstract: Phylogenetic relationships of the marine era of marine basidiomycetes (Kohlmeyer and Kohl- et al Marine gasteromycete, Nia vibrissa, were investigated using meyer 1979, Hawksworth 1995). fungi often to four ribosomal DNA (rDNA) regions. Independent display unique morphological adaptations the environment, which makes it difficult to analyses of mitochondrial small-subunit (mt-ssu) aquatic their closest relatives among the terrestrial rDNA, mitochondrial large subunit (mt-lsu) rDNA, identify A is the taxonomically enig- nuclear small-subunit (nuc-ssu) rDNA, and nuclear fungi. prime example matic marine gasteromycete, Nia vibrissa. Moore and large subunit (nuc-lsu) rDNA all suggest that Nia vi- Meyers (1959) described Nia vibrissa as a deutero- brissa is in the euagarics clade. The mt-lsu, nuc-ssu, mycete. However, Doguet (1967, 1968) demonstrated and nuc-lsu datasets suggest that Nia vibrissa is closely that Nia vibrissa develops basidia and clamp connec- related to the Henningsomycescan- cyphelloid fungus, tions, and Brooks (1975) showed that Nia vibrissa has didus, but in all three datasets the monophyly of the dolipore septa. These characters indicate that Nia vi- is Anal- Nia-Henningsomycesgroup weakly supported. brissa is a homobasidiomycete, but do not reveal its yses of mt-ssu rDNA suggest that the sister group of exact taxonomic position. Nia vibrissa is Schizophyllum commune, but again the Nia vibrissa generates minute ([0.5] 1-3 [5] mm) relationship is weakly supported. A combined analysis subglobose, gasteroid fruiting bodies, which are ses- of all four rDNA regions strongly supports the sister sile or, rarely, stalked. The color ranges from pale group relationship of Nia vibrissa and Henningsomy- cream to white-orange and orange-brown (Doguet ces candidus. Schizophyllum commune and Fistulina he- 1967, Kohlmeyer and Kohlmeyer 1979, Barata et al patica form a strongly supported clade that is weakly 1997). Basidiocarps grown in culture exhibit poly- supported as the sister group of the Nia-Henningso- morphic peridial surfaces with or without peridial myces clade. Schizophyllum commune and Fistulina he- hairs (Schimpfhauser and Molitoris 1991). Slightly patica both resemble cyphelloid fungi in some as- curved or bifurcate curled hairs project from the out- pects of their hymenophore morphology, and it is er peridium in some collections, but are lacking in plausible that they could be closely related to Hen- others. This considerable spectrum in habit of basi- ningsomyces candidus. Eighteen genera of terrestrial diocarps may indicate the presence of a multi-species gasteromycetes were included in the analyses, but complex (Jones and Jones 1993). Within a gelatinous none are closely related to Nia vibrissa, which there- gleba, the statismosporic basidia produce 4-8 ovoid and one fore represents an independent origin of the gaster- basidiospores that have 4 lateral appendages Both oid habit in the homobasidiomycetes. terminal appendage (Doguet 1967). peridial hairs and to a Key Words: cyphelloid fungi, Fistulina hepatica, basidiospore appendages appear play role in and colonization. Kohlmeyer and Henningsomyces candidus, marine fungi, molecular dispersal Kohlmeyer (1979) suggested that the peridial hairs systematics, Schizophyllum commune trap air, allowing the basidiocarps to float after being detached from the substrate. It has also been sug- Accepted for publication February 1, 2001. gested that the appendages of the basidiospores an- ' Corresponding author, E-mail: [email protected] chor spores to substrates (Webster 1959, Leightley 679 680 MYCOLOGIA and Eaton 1979) or slow their sinking rate (Ingold voucher specimen of Nia vibrissa (culture and herbarium 1975, 1976, Rosello6 et al 1993). Whatever the precise accession number M200) used in this study are deposited function of the peridial hairs and basidiospore ap- in the herbarium of the University of Regensburg (REG). data were from four rDNA pendages, Nia vibrissa is obviously very successful at Sequence generated regions: partial mitochondrial small subunit (mt-ssu) rDNA, bound- dispersal. It is widespread in temperate and tropical ed by primers MS1 and MS2, partial mitochondrial large localities in the Atlantic, Pacific, and Indian Oceans, subunit (mt-lsu) rDNA, bounded by primers ML5 and ML6, and the Mediterranean Sea 1983, (Kohlmeyer Hyde nearly complete nuclear small subunit (nuc-ssu) rDNA, and Kuthubutheen 1986, Jones 1989). bounded by primers PNS1 and NS8, and partial nuclear Nia vibrissa has been collected on diverse woody large subunit (nuc-lsu) rDNA, bounded by primers LROR substrates, including driftwood, mangroves, and and LR5. In addition, mt-lsu and nuc-lsu sequences were sunken ship timbers, as well as Spartina culms and generated for Schizophyllum commune (isolate Scol, Ger- rhizomes (Kohlmeyer and Kohlmeyer 1979). It has many, REG) and a mt-lsu sequence was generated for the also been isolated by baiting with wooden test panels cyphelloid wood-decay fungus, Henningsomyces candidus (Cuomo et al 1988, Grasso et al 1989) and feathers (isolate R.G. Thorn 156, DAOM accession number 195432). An nuc-lsu of Fistulina (Rees and Jones 1985). A second species, Nia epider- unpublished sequence hepatica (iso- late TW351, Germany, REG) was provided by Tobias Wag- moidea, was detected by baiting with horsehair (Ros- ner (University of Regensburg), and a published nuc-lsu sello6 et al 1993), and a third species, Nia globospora, sequence of Henningsomyces candidus isolate R.G. Thorn was described from continuously submerged Spartina 156 was downloaded from GenBank accession number culms et al Nia (Barata 1997). Thus, species exploit AF287864; Hibbett et al 2000). Protocols and primer se- keratinic as well as lignocellulosic substrates. Like quences for amplification and sequencing have been de- many saprotrophs, Nia vibrissa grows well in culture, scribed elsewhere (Vilgalys and Hester 1990, White et al and several studies have investigated the light, tem- 1990, Bruns and Szaro 1992, Hibbett 1996, Bruns et al 1998, perature, and salinity requirements for growth and Moncalvo et al 2000, http:-www.botany.duke.edu-fungi- fruiting body production (Doguet 1968, Schimpfhau- mycolab-primers.htm; http:-plantbio.berkeley.edu- bruns- ser and Molitoris 1991, Jones and Jones 1993). Leigh- primers.html). The new sequences have been deposited in GenBank (AF334747-AF334754). tley and Eaton (1979) demonstrated a white rot pat- The sequences from Nia vibrissa, Schizophyllum commune, tern of wood decay in Nia vibrissa cultures (presence Henningsomyces candidus, and Fistulina hepatica were man- of phenol oxidase and laccase using the KIarig drop ually aligned to four published datasets. The mt-ssu and nuc- test confirmed the Bavendamm and illustrat- by test) ssu datasets are being published by Hibbett and Donoghue ed a decay micromorphology typical of terrestrial (in press) and include 127 and 111 sequences, respectively. white rot fungi. Sampling in that study was biased toward wood decay fungi, Different authors have suggested that Nia is closely especially members of the polyporoid clade (clade names related to several groups of terrestrial gasteromycetes. used in this paper follow Hibbett and Thorn 2001), which Nia has been classified in the Melanogastrales, either was represented by 49 mt-ssu sequences and 34 nuc-ssu se- in the Torrendiaceae (Dring 1973) or Melanogastra- quences. Nevertheless, the mt-ssu and nuc-ssu rDNA datasets each include of all clades of hom- ceae (Doguet 1969, Kohlmeyer and Kohlmeyer 1979), representatives eight major obasidomycetes recognized by Hibbett and Thorn. The mt- the Nidulariales (Rossell6 et al 1993), or in the Ni- ssu and nuc-ssu analyses were rooted with the heterobasidi- aceae, among the gasteromycetes incertae sedis (Jii- omycetes Auricularia, Dacrymyces, and Tremella. The mt-lsu lich several molecular datasets 1981). Recently, large dataset was published by Bruns et al (1998), and includes have been that resolve developed phylogenetic place- 153 sequences, most of which are from ectomycorrhizal spe- ments of many homobasidiomycetes (e.g., Hibbett et cies, including 67 sequences from the bolete clade. Forty-four al 1997, Bruns et al 1998, 2000, Moncalvo et al 2000). mt-lsu sequences represent unidentified species (e.g., Tomen- In the present study, we performed independent and tella sp.) or direct amplifications from mycorrhizae. There combined analyses of four different rDNA regions to are no representatives of the hymenochaetoid clade in the address the phylogenetic position of Nia vibrissa. mt-lsu dataset, but all of the other major clades of homobas- idiomycetes are represented. The