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Phylogenetic Relationships Between the Acantharea and the Polycystinea: a Molecular Perspective on Haeckel’S Radiolaria

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Phylogenetic Relationships Between the Acantharea and the Polycystinea: a Molecular Perspective on Haeckel’S Radiolaria Proc. Natl. Acad. Sci. USA Vol. 94, pp. 11411–11416, October 1997 Evolution Phylogenetic relationships between the Acantharea and the Polycystinea: A molecular perspective on Haeckel’s Radiolaria LINDA AMARAL ZETTLER*†,MITCHELL L. SOGIN*, AND DAVID A. CARON‡ The Josephine Bay Paul Center in Comparative Molecular Biology and Evolution, Marine Biological Laboratory, 7 MBL Street, Woods Hole, MA 02543; and ‡Biology Department, Woods Hole Oceanographic Institution, 324 Redfield Building, Woods Hole, MA 02543 Communicated by Andrew H. Knoll, Harvard University, Cambridge, MA, August 11, 1997 (received for review May 9, 1997) ABSTRACT Polycystine radiolaria are among few pro- mitochondria, golgi, and other major cellular machinery from tistan groups that possess a comprehensive fossil record the extracapsular region that contains the axopodial network available for study by micropaleontologists. The Polycystinea of the cell. Phaeodarian and polycystine radiolaria possess and the Acantharea, whose skeletons do not become fossilized, pores in their central capsules whereas acantharia do not. were once members of the class ‘‘Radiolaria’’ (‘‘Radiolaria’’ Despite these differences, the common use of radial symmetry sensu lato: Polycystinea, Phaeodarea, and Acantharea) origi- in cell body plan and shell architecture often results in a similar nally proposed by Haeckel but are now included in the general appearance among members of the Acantharea and superclass Actinopoda. Phylogenetic relationships within this the polycystine order Spumellarida. superclass remain largely enigmatic. We investigated the Today, the term ‘‘radiolaria’’ is generally an informal taxo- evolutionary relationship of the Acantharea and the Poly- nomic descriptor for members of the Polycystinea (Spumel- cystinea to other protists using phylogenetic analyses of larida and Nassellarida) and the Phaeodarea, even though 16S-like ribosomal RNA (rRNA) coding regions. We circum- Ernst Haeckel (5) used the term to include members of the vented the need to culture these organisms by collecting and class Acantharea. Of the 4417 species of organisms described maintaining reproductive stages that contain many copies of from collections of the Challenger Expedition, 3508 were new their genomic DNA. This strategy facilitated extraction of genomic DNA and its purification from symbiont and prey species of Radiolaria (5, 6). In his classification of the ‘‘Ra- DNA. Phylogenetic trees inferred from comparisons of 16S- diolaria,’’ Haeckel included four legions: the Acantharia, the like coding regions do not support a shared history between Spumellaria, the Nassellaria, and the Phaeodaria. This classi- the Acantharea and the Polycystinea. However, the monophyly fication was later modified (7–10) to exclude the Acantharia of the Acantharea and the separate monophyly of the Poly- from the Spumellaria, Nassellaria, and Phaeodaria. Despite cystinea (Spumellarida) are well supported by our molecular- later taxonomic revision, many of Haeckel’s original descrip- based trees. The acantharian lineage branches among crown tions of the Challenger Radiolaria persist today. Modern organisms whereas the polycystine lineage diverges before the systematists place acantharia in a class distinct from polycys- radiation of the crown groups. We conclude that the Actino- tines and phaeodaria but generally agree that these classes are poda does not represent a monophyletic evolutionary assem- members of the Actinopoda (2, 3, 11–13). blage and recommend that this taxonomic designation be The presence of axopodia and a central capsule are the discarded. predominant shared characters of the Acantharea and the Polycystinea. Most similarities occur between the Acantharea The superclass Actinopoda (1) includes protists with special- and the Polycystinea belonging to the order Spumellarida. ized microtubule-stiffened pseudopodia called ‘‘axopodia.’’ Most acantharia are polynucleated, but the presence of a single Current taxonomic schemes of the superclass Actinopoda nucleus in the acantharian genus Haliommatidium is a feature include the Acantharea, Polycystinea, and Phaeodarea and shared with the polycystines, which usually have only one most members of the Heliozoea (except the pedinellids and nucleus. Similarities also occur between the ‘‘gelatinous pel- heliomonads) (2, 3). licle’’ of some acantharia and that of certain Sphaerellarina, a One of the major distinctions between the Acantharea and suborder in the Spumellarida (14, 15). Both classes use SrSO4. the Polycystinea is the composition, architecture, and symme- Members of the Acantharea build entire skeletons of SrSO4 try of the skeleton, when present. Polycystines have a rich fossil whereas adult vegetative colonial spumellaria and swarmer record due to the presence of skeletal material comprised of cells of reproductive spumellaria contain individual crystals of silica, which is secreted by many members of this class and SrSO4 (2, 16–18). which becomes preserved in marine sediments. Polycystine The molecular diversity of the superclass Actinopoda is skeletons exhibit a range of morphologies from simple spicules unexplored. We sequenced the 16S-like rRNA genes of rep- to more elaborate latticed shells possessing radial spines. All resentatives of the Acantharea and Polycystinea to test the acantharia form skeletons comprised of monocrystals of stron- hypothesis that the Acantharea and the Polycystinea share a tium sulfate (SrSO ), which come together at the center of the 4 common evolutionary history. According to phenotypic sim- cell in a symmetrical fashion known as Mu¨ller’s Law (4). ilarities, the taxa chosen for this study represent the most Acantharian skeletons, however, are susceptible to dissolution closely related classes in the Actinopoda. Therefore, this study and are therefore absent from the fossil record. In all phae- odaria, polycystines, and members of the acantharian order addresses the appropriateness of the higher taxon designation Arthracanthida, the central capsule or capsular wall divides the Actinopoda and rekindles the debate over the best definition cell into an intracapsular region that includes the nucleus, of ‘‘Radiolaria.’’ The publication costs of this article were defrayed in part by page charge Abbreviations: rRNA, ribosomal RNA; SrSO4, strontium sulfate; FITC, fluorescein isothiocyanate. payment. This article must therefore be hereby marked ‘‘advertisement’’ in Data deposition: The sequence in this paper have been deposited in accordance with 18 U.S.C. §1734 solely to indicate this fact. the GenBank database (accession nos. AF018158–AF018163). © 1997 by The National Academy of Sciences 0027-8424y97y9411411-6$2.00y0 †To whom reprint requests should be addressed. e-mail: amaral@ PNAS is available online at http:yywww.pnas.org. evol5.mbl.edu. 11411 Downloaded by guest on September 25, 2021 11412 Evolution: Amaral Zettler et al. Proc. Natl. Acad. Sci. USA 94 (1997) MATERIALS AND METHODS hybridizations on acantharia were carried out as described (26) using biotinylated probes and detection with fluorescein iso- Sample Collection. Individual specimens were collected by thiocyanate (FITC)–avidin solution (20 mgyml in 100 mM divers using glass or polycarbonate jars. Specimens were NaHCO3-buffered saline, pH 8.2). Acantharia were fixed for maintained in 0.22 mm of filtered Sargasso Sea water in glass 1 h at 4°C in 1X Histochoice fixative (Amresco, Euclid, OH) culture tubes with brine shrimp (Artemia salina) as food. All diluted in 0.22 mm of filtered Sargasso Sea water. Individuals acantharia were collected off of the southwestern coast of were then transferred to gel-subbed slides, overlaid with 0.05% Bermuda in September 1994. Acantharian samples included agarose, and allowed to dry overnight. Probe was added to a Haliommatidium sp. (BBSR 235: Order: Symphyacanthida, final concentration of 5 ngyml. Probe experiments consisted of Family: Pseudolithidae) and Chaunacanthid 218 (BBSR 218: a negative control (incubation in fluorescein-labeled avidin Order: Chaunacanthida). Polycystine radiolarian specimens with no probe added), a positive control (biotinylated EUK included one solitary and three colonial forms, all from the 1209Rbio added), and two separate acantharian-specific probe order Spumellarida. The solitary spumellarian Thalassicolla experiments using A497bio and A899bio oligonucleotides, nucleata (BBS 3: Family: Thalassicollidae) was collected in respectively. Hybridizations were carried out at 42°C for 6–8 May 1992, colonial spumellarian Collosphaera globularis- h and washed at 45°C. Cells were mounted in Citifluor huxleyi (BBSR 173: Family: Collosphaeridae) in May 1994, and immersion oil (Citifluor, Kent, U.K.) and viewed on a Zeiss colonial spumellaria Sphaerozoum punctatum (CR4: Family: Axiophot equipped for epifluorescence microscopy. Sphaerozoidae) and Collozoum serpentinum (CR16: Family: We used colorimetry-based in situ hybridizations for the Sphaerozoidae) in May 1995. Specimens used for in situ colonial spumellarian samples to avoid severe autofluores- hybridizations were collected in September and October of cence. Hybridizations were carried out on colonial spumellar- 1995. ian samples using the GIBCOyBRL In Situ Hybridization and DNA Extraction, Amplification, Cloning, and Sequencing. Detection System with the following modifications for use with A natural amplification of DNA occurs before swarmer cell rRNA and larger sarcodines. Colonies were preserved in 1X release from reproductive acantharia and
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