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Scrippsiella Velellae Sp. Nov. (Peridiniales) and Gloeodinium Viscum Sp

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Scrippsiella Velellae Sp. Nov. (Peridiniales) and Gloeodinium Viscum Sp MOLECULAR ANALYSIS OF PORPHYRA 517 dophyta) in North America. I. Biogeographic trends in mor- Waaland, J. R., Dickson, L. G. & Duffield, E. C. S. 1990. Con- phology. Phjcologia 23:383-96. chospore production and seasonal occurrence of some Por- Sogin, M. L. & Edman, J. C. 1989. A self-splicing intron in the phjra species (Bangiales, Rhodophyta) in Washington State. small subunit rRNA gene of Pneumocjstis carinzz. Nurleir Acids Hjdrobiologia 204/205:453-9. Res. 17:5349-59. Wang, J-C. & Chiang, Y-M. 1977. Notes on the marine algae of Sogin, M. L., Gunderson, J. H., Elwood, H. J., Alonso, R. A. & Taiwan. 11. The genus of Porphp. Taiwania 22:105-12. Peattie, D. A. 1989. Phylogenetic meaning of the Kingdom White, T.J., Bruns, T., Lee, S. & Taylor, J. 1990. Amplification concept: an unusual ribosomal RNA from Giardia lamblia. and direct sequencing of fungal ribosomal RNA genes for Sciencp (Wash. D.C.)243:15-7. phylogenetics. In Innis, M. A., Gelfand, D. H., Sninsky, J. J. Tokida, J. 1935. Phycological observations. 11. On the structure & White, T. J. [Eds.] PCR Protocols: A Guide to Mpthods and ofPorphjra onoi Ueda. Trans. Sapporo ‘Vat. Hist. Sac. 14: 11 1-4. Applications. Academic Press, San Diego, pp. 3 15-22. Van de Peer, Y., Neefs, J-M. & De Wachter, R. 1990. Small Wilcox, L. W., Lewis, L. A., Fuerst, P. A. & Floyd, G. L. 1992. ribosomal subunit RNA sequences, evolutionary relation- Group I introns within the nuclear-encoded small-subunit ships among different life forms, and mitochondria1 origins. rRNA gene of three green algae. Mol. Biol. EL~o~.9:1103-18. J. Mol. Errol. 30:463-76. Woese, C. R. & Olsen, G. J. 1986. Archaebacterial phylogeny: van Oppen, M. J. H., Olsen, J. L. & Stam, W. T. 1993. Evidence perspectives on the Urkingdoms. Sjst. Appl. Microbial. 7: 16 1- for independent acquisition ofgroup I introns in green algae. 77. Mol. Biol. Evol. (in press). J. Phycol. 29, 517-528 (1993) SCRIPPSIELLA VELELLAE SP. NOV. (PERIDINIALES) AND GLOEODINIUM VISCUM SP. NOV. (PHYTODINIALES), DINOFLAGELLATE SYMBIONTS OF TWO HYDROZOANS (CNIDARIA)’.’ Anastazia T. Banaszak, Roberto Iglesias-Prieto, and Robert K. TrenchS Department of Biological Sciences, University of California at Santa Barbara, Santa Barbara, California 93106 ABSTRACT dophyta, Bacillariophyta, Chlorophyta, Prasinophy- The alga symbiotic with the “By the Wind Sailor” Ve- ta, Pyrrophyta). Such a wide phyletic distribution of lella velella L. (Hjdrozoa, Chondrophora) collected off symbionts and hosts is consistent with the concept the coast of Galijornia, and the alga symbzotic with the of a polyphyletic origin of microalgal-invertebrate hydrocoral Millepora dichotoma Forskal (Hydrotoa, symbiosis (Trench 1992). Symbioses between dino- Milleporina) from the Gulf of Aqaba, were isolated and flagellates (Pyrrophyta) and invertebrates dominate brought into unialgal, axenic culture. Based on laght mi- the marine environment (Trench 1987a, 1992), are croscopj and ultrastructural analyses by transmission and essential to the high primary productivity of coral scanning electron microscopy, the algal population from reefs (Muscatine 1980), and are sensitive indicators V. velella is described as Scrippsiella velellae sp. nov. of ecological perturbations in such shallow water (Peridiniales). The algal population from the dark morph ecosystems (Iglesias-Prieto et al. 1992). The concept of M. dichotoma is described as Gloeodinium viscum of a monophyletic origin of dinoflagellate-inverte- sp. nov. (Phytodiniales). These are the first descriptions of brate symbioses was founded on the premise that sjmbiotic dinoflagellates belongzng to the orders Perzdinia- symbiotic dinoflagellates are restricted to the genus les and Phqtodiniales. When viewed with descriptions of Symbiodinium. This concept is giving way to one of symbiotic dinoflagellates belonging to the Prorocentrales polyphyletic origins of dinoflagellate-invertebrate and Gymnodinzales, the evidence currentlq points to seven symbioses (Trench 1992) that currently embrace genera in four orders of dtnojagellates havzng represen- several species of Symbiodinium (Blank and Trench tataves that haw entered a symbiotic mode of existence. 1985, Trench and Blank 1987, Blank and Huss 1989, Rowan and Powers 1992), two species of Amphidi- Key index words: Dinophyceae; dizwsity; Gloeodini- nium (,,. L. Taylor 1974, Trench and Winsor 1987), um viscum sp. nov.; Pyrrophyta; Scrippsiella velellae two species of Gymnodinium (Lee 1980, Spero 1987), sp. nov.; symbiosis Aureodinium hindler and Hemleben 1980). and ,I Prorocentruin (famasu 1988). A wide phyletic range of invertebrates harbors The dinoflagellate symbiont of the “By the Wind endosymbiotic microalgae (used here to include Sailor” Velplla velplla L. was originally named zoo- cyanobacteria) representing S~eraldivisions (Rho- xanthella (Brandt 1881, 1882) or Philozoon sifhonoph- oruvn (Geddes 1882a, b) and, subsequently, Endodi- nium chattonii (Hovasse 1922, 1923) (Blank and ’ Received 14 December 1992. Accepted 19 April 1993. We dedicate this paper to the memory of the late Professor Trench 1986)*More using v’ velella from Luigi Provasoli, a mentor and friend to R.K.T. the Mediterranean, D. L. Taylor (1971a, 1974) $Author for reprint requests. claimed that the alga in culture was amphidinioid 518 ANASTAZIA T. BANASZAK ET AL. and assigned the alga to Amphidinium [as A. chattonii cells were fixed and processed as described previously (Trench (Hovasse) D. L. Taylor]. However, this generic des- 1974, Trench and Blank 1987). The methods used for exami- ignation was disputed by Hollande and CarrP (1 974), nation of motile stages by scanning electron microscopy (SEM) who, although they studied only ‘the coccoid phase were those described by Spero (1987). hospite of the symbiont of Mediterranean velella, in V. RESULTS nonetheless felt justified in retaining the alga in En- dodinium. The alga was never described in detail by Scrippsiella velellae sp. nov. (Figs. 1- 15) Brandt, Geddes, nor Hovasse, who regarded it as a Order, Peridiniales; Family, Calciodinellaceae parasite related toBlastodinium (Hovasse 1922, 1923). Unicellularis alga status sjmbiosis cum Velella velella D. L. Taylor and Hollande and CarrP described in (Pactjica), locatus in hospite ac coccoidales (non-mobiles) detail the ultrastructure of the alga in hospite but cellulae diametro 17-18 pm intra endodermatibus cel- offered no description of the alga in culture. We lulae gonophorum et medusarum, dividens status mitosis have successfully isolated the symbiotic alga from V. in statu coccoidales in hospite et in cultura. Magna nu- velella collected off the coast of California and have cleus cum circa 90 chromosomatibus; inuolucrum nuclei maintained it in unialgal, axenic culture. We de- compositus duarum membrana cum areoles. Involucrum scribe the alga as Scrippsiella zelellae sp. nov. Light chloroplastium coinpositus triuin membrane; thjlakoidea and electron microscopic descriptions of coccoid chloroplastium maximum partern binae aggregatae; dua stages in hospite and in culture and of the dinomas- pjrenoides cum inuadens chloroplasts thjlakoides. “Ac- tigote stage in culture are provided. cumulate corpora” praesens in hospite et in cultura. Schonwald et al. (1987) described studies of “pho- Trichocjsta praesens in hospite et in cultura. to-adaptation” of photosynthesis in light- and dark- Status dinomastigota peridinoide in cultura; ualuae de- colored colonies of the hydrocoral Millepora diclio- signatus pp x 4’3a 7“ 5c 3s 5“ Op 2”; 17-20 pm in toma Forskil from the reefs off Eilat, Israel. We have longitudine; cellulae demonstratus lateralis in statu ec- isolated the algae from both types of hydrocoral and djsis. Trichocjsta p raesens. brought them into culture. While the alga associated Unicellular alga symbiotic with Velella idella L. with the light morph of M. dichotoina conformed in (Pacific), located in hospite as coccoid (non-motile) its morphology to a species of Synbiodinium (R.K.T., cells 1’7-1 8 pm in diameter, within endodermal cells unpubl.), the alga isolated from the dark morph did of the gonophores and medusae, dividing mitotically not. A description of the ultrastructure of the coc- in the coccoid state in lzospite and in culture. Large coid cells in culture is provided. We have not been nucleus with approximately 90 chromosomes; nu- able to study the dinomastigote stage in detail. clear envelope comprised of two membranes with pores. Chloroplast envelope comprised of three MATERIALS AND METHODS membranes; chloroplast thylakoids predominantly Colonies of Vrlrlln 1vlrlln L. were collected during “blooms” in groups of two; two pyrenoids with invasive chlo- in 1988 and 1991 off the coast of Santa Barbara, California. After roplast thylakoids. “Accumulation body” present in the animals were transferred to the laboratory, the gonozooids host and in culture. Trichocysts present in hospite were dissected from the colony, and released medusae were col- and in culture. lected, fixed, and prepared for light and electron microscopic Dinomastigote stage in culture peridinioid; thecal examination, as described later. The algal cells were isolated by blending several medusae or gonozooids in a Virtis blender, fil- plate designation pp x 4‘ 3a 7” 5c 3s 5” OP 2””; 17- tering the slurry through cheese cloth, and repeatedly washing 20 Prn in length. Cells demonstrate lateral ecdysis. by centrifugation and resuspension in sterile sea water (Trench Trichocysts present. 1971). Samples of the crude isolates were immediately fixed for The
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