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Phylogenetic Position of Freshwater and Marine Sigmoidea Species: Introducing a Marine Hyphomycete Halosigmoidea Gen

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Phylogenetic Position of Freshwater and Marine Sigmoidea Species: Introducing a Marine Hyphomycete Halosigmoidea Gen View metadata, citation and similar papers at core.ac.ukArticle in press - uncorrected proof brought to you by CORE provided by Tottori University Research Result Repository Botanica Marina 52 (2009): 349–359 ᮊ 2009 by Walter de Gruyter • Berlin • New York. DOI 10.1515/BOT.2009.006 Phylogenetic position of freshwater and marine Sigmoidea species: introducing a marine hyphomycete Halosigmoidea gen. nov. (Halosphaeriales) E.B. Gareth Jones1,*, Alga Zuccaro2, Julian three marine Sigmoidea species (S. luteola, S. marina, Mitchell3, Akira Nakagiri4, Ittichai Chatmala1,5 S. parvula sp. nov.). Identification keys to the genera and Ka-Lai Pang1,6 Halosigmoidea, Pseudosigmoidea and Sigmoidea, and Halosigmoidea species are provided. 1 BIOTEC Bioresources and Technology Unit, National Center for Genetic Engineering and Biotechnology, Keywords: 18S; 28S; Corollospora; Halosigmoidea gen. 113 Paholyothin Road, Khlong 1, Khlong Luang, nov.; Halosphaeriales; ITS rDNA; marine fungi; Pathum Thani 12120, Thailand, Sigmoidea. e-mail: [email protected] 2 Research Center for BioSystems, Land Use and Nutrition IFZ, Institute of Phytopathology and Applied Introduction Zoology (IPAZ), Justus-Liebig-University Giessen, 35392 Giessen, Germany Crane (1968) established the genus Sigmoidea for a sub- 3 School of Biological Sciences, University of merged freshwater hyphomycete with hyaline, scoleco- Portsmouth, King Henry Building, King Henry I Street, form conidia, Sigmoidea prolifera (R.H. Petersen) J.L. Portsmouth PO1 2DY, UK Crane that was originally placed in the genus Flagello- 4 National Institute of Technology and Evaluation, spora Ingold by Petersen (1963). The establishment of Biological Resource Center, 2-5-8, Kazusalamatari, the genus Sigmoidea was based on the presence of Kisarazu-shi, Chiba, 292-0818, Japan holoblastic rather than phialidic conidiogenous cells 5 Department of Microbiology, Faculty of Science, (Crane 1968, Marvanova´ and Descals 1987). Since then, Prince of Songkla University, Hat Yai, Songkhla, three additional freshwater species have been described: Thailand S. aurantiaca Descals, a taxon having wide falcate to sig- 6 Institute of Marine Biology, National Taiwan Ocean moid shaped conidia (Descals and Webster 1982); S. University, No. 2 Pei-Ning Road, Keelung 20224, praelonga Marvanova´ , from Czech waters, with longer Taiwan (R.O.C.) conidia than S. prolifera (Marvanova´ 1986) and S. contor- * Corresponding author ta Marvanova´ et Hywel-Jones, a pleoanamorphic species with macroconidia that have sympodial or rarely percur- rent conidiogenous cells and polyblastic microconidia Abstract borne on contorted thick-walled hyphal branches (Mar- vanova´ and Hywel-Jones 2000). The aquatic hyphomycete genus Sigmoidea, with fresh- Crane (1968) erected the genus Sigmoidea using water and marine representatives, is re-examined at the Petersen’s holotype specimen preserved in NY as type. morphological and molecular levels. Currently six species However, Crane’s specimen, 85-B-65 (sATCC 16660), are accepted, four from freshwater habitats (S. prolifera, also deposited as S. prolifera, differed from the type in S. aurantiaca, S. contorta, S. praelonga) and two marine not showing ampulliform sympodially elongating conidio- species (S. marina, S. luteola). Phylogenetic analyses of genous cells (Marvanova´ and Descals 1987). In 2000, the ribosomal small subunit rRNA gene sequences of Ando and Nakamura transferred Crane’s specimen to a freshwater and marine Sigmoidea species indicate that new genus, Pseudosigmoidea K. Ando et N. Nakamura the marine species are distantly placed from the fresh- with P. cranei K. Ando et N. Nakamura, as the type spe- water species, S. prolifera and Pseudosigmoidea cranei. cies (ATCC 16660), based on the presence of polyphial- The latter species are placed in the Dothideomycetes, in dic enteroblastic conidiogensis. Although there is no sister clades, with 81% bootstrap support. The phylo- doubt that these two specimens represent two different genetic placement of both marine Sigmoidea species, taxa, there is no evidence of polyphialdic enteroblastic inferred from large subunit rRNA gene sequences, was conidiogenesis from the illustrations in the protolog by within the genus Corollospora (Halosphaeriales, Sorda- Ando and Nakamura, and there is no indication of repeat- riomycetes, Pezizomycotina). An undescribed Sigmoidea ed production of conidia from the same conidiogenous species isolated from the Baltic Sea and one previously locus. The taxonomic position of these specimens there- incorrectly identified as S. marina from Japan (S. parvula fore remains unclear. sp. nov.) formed a clade together with Corollospora quin- Two additional Sigmoidea species with sympodial queseptata and Varicosporina ramulosa, and were locat- conidiogenesis cells, curved (not sigmoid as indicated in ed in a sister group to S. luteola and S. marina. Based the original descriptions) conidia with the end cells lack- on morphological and phylogenetic evidence, Halosig- ing cytoplasmic contents were described: Sigmoidea moidea gen. nov. is proposed to accommodate the marina Haythorn et E.B.G. Jones (Haythorn et al. 1980) 2009/90 Article in press - uncorrected proof 350 E.B.G. Jones et al.: Halosigmoidea gen. nov. and Sigmoidea luteola Nakagiri et Tubaki (Nakagiri and caro et al. 2003). Ten strains of S. marina (Halosigmoidea Tubaki 1982). The teleomorph of S. luteola is Corollo- marina), were isolated from Fucus serratus thalli collected spora luteola Nakagiri et Tubaki (Nakagiri and Tubaki during a study on Helgoland, North Sea, of which TUB 1982), while no teleomorph is known for S. marina.An 270 was used in this study. TUB 156, isolated from Nord- additional Sigmoidea species, S. littoralis Phillips, col- deich, North Sea was also used in this study. Two Sig- lected from decomposing material of the red alga Geli- moidea sp. isolates (TUB 7952 and TUB 7956) were dium coulteri Harv., from Hopkins Marine Station, Pacific isolated from Enteromorpha sp. from Niendorf, Baltic Grove, California in 1979, was listed in Index fungorum Sea. Four isolates of Corollospora angusta Nakagiri et (CABI website, this reference has now been removed), Tokura were isolated from F. serratus collected from but to our knowledge a description of this species has Helgoland, North Sea, but only TUB 1 was used in this never been published nor has an isolate been deposited study. Other freshwater Sigmoidea species were not anywhere. Additional collections were made from Rho- available to us for study as existing isolates were subject doglossum affine (Harv.) Kyl. in California and Prasiola to commercial confidentiality. meridionalis S. et G. at Cattle Point, San Juan Island, Fungi were maintained on freshwater or seawater Washington (G.K. Phillips, personal communication); cornmeal agar (Difco, Criterion, Santa Maria, USA: 30 g unfortunately, no specimens or isolates are available for l-1 maize meal, 20 g l-1 agar) as appropriate. Cultures were morphological or molecular analysis. grown in GYP broth (homemade: 4 g l-1 glucose,4gl-1 During a study of fungi associated with marine plants yeast extract, 2 g l-1 peptone) in filtered natural seawater and algae in Germany, many isolates belonging to the except for Sigmoidea prolifera and Pseudosigmoidea genus Sigmoidea were recovered from Fucus serratus L. cranei, which were grown in a CMA freshwater medium. collected on Helgoland, North Sea (Zuccaro et al. 2003, Fungal biomass was harvested by filtration and washed 2008) and identified as Sigmoidea marina. Others col- with sterile distilled water. lected from a variety of substrata located at different sites Isolates TUB 6989 and TUB 407 were cultured on arti- in the Baltic Sea also could not be identified according ficial seawater (Meersalz, Wiegandt GmbH, Krefeld, Ger- to the descriptions of known species (Crane 1968, Hay- many) glucose-peptone-yeast extract agar GYP (0.1 g l-1 thorn et al. 1980, Descals and Webster 1982, Nakagiri glucose, 0.1 g l-1 yeast extract, 0.5 g l-1 peptone, 20 g l-1 and Tubaki 1982, Marvanova´ 1986, Marvanova´ and Des- agar, 15 g l-1 sea salt) at 14, 20, and 258C in the dark for cals 1987, Marvanova´ and Hywel-Jones 2000). These morphological description. For molecular analysis, these isolates, together with three Sigmoidea sp. (originally two isolates were grown on glucose-peptone-yeast identified as S. marina) collected from sea foam in Japan, extract agar (0.1 g l-1 glucose, 0.1 g l-1 yeast extract, shared several morphological characteristics typical of S. 0.5gl-1 peptone, 20 g l-1 agar, 15 g l-1 sea salt) at room marina, but differed by having shorter conidia (Nakagiri temperature for 1 week. 1989). Because the marine Sigmoidea species are mor- phologically different from S. prolifera in having predom- DNA isolation and PCR amplification inantly C- or U-shaped conidia with end cells lacking For the strains isolated from Germany, up to 500 mg of cytoplasm, irregular sympodial conidiogensis cells, fresh mycelium was removed from the surface of the and are marine in habitat, a molecular phylogenetic study agar plates with a sterile loop and extracted using the was undertaken to resolve the taxonomic relationship FastDNA SPIN Kit for soil (BIO 101 Systems, Macherey- between the freshwater and marine species. Nagel, Du¨ ren, Germany). DNA fragments were used as templates for the polymerase chain reaction (PCR) using Materials and methods the 28S rDNA primers NL209–NL912 (Zuccaro et al. 2003) or the ITS primers ITS1–ITS4 (White et al.
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