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J, Enknryot. :\!il:rubitl/.• 50(6) , 20 03 pp. 483 ·4 87 f; 100 3 by the Society or Prorozootogists Small Subunit Ribosomal DNA Suggests that the Xenophyophorean corbicula' is a Foraminiferan

JAN PAWLOWSKI,. MARIA HOLZMANN,' JOSE FAHRNI' and SUSAN L. RICHARDSON" sDepartm ent of Zoology and Biology. University ofGeneva. Crl-lZl I Geneva 4. SWitzerland. and "Smithsonian Marine Station at Fort Pierce. 701 Seaway Drive. Fort Pierce. Florida 34949. USA

ABSTRACT. are giant deep- rhizopodial of enigmatic origins. Although were described as Fo­ raminifera or in the early literature, the xenophyophoreans are currently classified either as a of Rhizopoda or an inde­ pendent . To establish the phylogenetic position ofXenophyophorea, we analysed the small subunit (SSU) rRNA gene sequence of S yringammi na corbicula Richardson, a newly described xenophyophorean species from the Cape Verde Plateau. The SSUrDNA analyses showed that S. corbicula is closely related to Rhizammina algueformis, a tubular deep-sea foramin iferan. Both species branch within a group of monothalamous (single-chambered) , which include also such agglutinated genera as Toxisarcon, Rhab­ dammina, and Sac cammina, and the organic-walled genera Gloiogullmia and Cylindrogullmia. Our results are congruent with obser­ vations of similar cytoplasmic organisation in Rhizammina and Syrt ngammin a. Thus, the Xenophyophorea appear [0 be a highly spe­ cialised group of deep-sea foraminifera. Key Words. Deep-sea, Foraminifera, Phylogeny, Ribosomal RNA, Protista Xenophyophorea.

ENOPHYO PHOREA are giant rhizopodial protists widely oda (Corliss 1994), or as an independent class or phylum within X distributed in the deep sea at bathyal and abyssal depths. Eukaryota (Lee et al. 2000). Because of a lack of molecular The xenophyophoreans are particularly abundant in regions of data, the Xenophyophorea have not been included in recent high food supply, for example, beneath productive surface wa­ taxonomic revision of the protists (Cavalier-Smith 2002). ters or on the summits and flanks of (Levin 1994 ; In this paper, we present the phylogenetic analysis of small Levin and Tomas 1988). Their often large, morphologically subunit (SSU) rRNA gene sequences obtained from Syringam­ complex tests provide a substrate, refuge, and source of food mina corbicula, a newly described species of Xenophyophorea for numerous small-sized metazoans and protists and may con­ (Richardson 200 I), indicating that this species is a foraminif­ tribute to the maintenance of high local species diversity in eran. areas where they are abundant (Gooday 1991 ; Le vin et al. 1986). MATERIALS AND METHODS The Xcnophyophorea are the largest deep-sea protists, rang­ DNA extraction. Living specimens of Syringammina cor­ ing in size from a few millimetres up to 25 em (Tendal 1990 ). bicula were collected in December 1998 , during cruise 159, leg Their main diagnostic morphological features are: (I) an agglu­ 7 of the R/V Knorr (Woods Hole Oceanographic Institution). tin ated composed of foreign particles ("xenophyae"), (2) All specimens were retrieved from a single site on the Cape a organised as a enclosed Verde Plateau (N 18" 27 .7 ', W 21" 01.6'), at a depth of3,106 within a branching system of organic tubes (granellare), (3) m using a multiple corer (Richardson 2001). A specimen des­ strings of stercomata (stercomare) closely associated with the ignated for molecular work was frozen at -80 "C imm ediately granellare system, and (4) numerous intracellular barium sul­ after being collected. It was transferred frozen to the laboratory phate crystals (granellae) (Tendal 1972). Some Xenophyopho­ in Geneva, where it was dissected under a binocular micro­ rea have been reported to possess granuloreticulopodia (Rich­ scope, in sterile conditions. Several fragments of granellare ardson 200 I), biflagellated , and heterokaryotic nuclei were isolated under UV-irradiated hood, using sterile tool s to (Tendal 1972). However, observations of living xenophyopho­ avoid contamination by foreign DNA. Each fragment wa s re ans are very rare (Gooday et al. 1993) and our knowledge of washed in sterile seawater and cleaned with brush under a bin­ their biology, , and cycle is limited. ocular microscope. The mi croscopic examination of all frag ­ The class of Xenophyophorea presently includes 14 genera ments of granellare taken for DNA extraction did not reveal the and almost 60 described species (Gooday and Tendal 2000; presence of any other protists. The DNEasy mini kit (Qia­ Tendal 1996). Identification of xenophyophoreans is often dif­ gen, Santa Clarita, CA) was used for DNA extraction. ficult because their fragile tests fragment easily, have relatively DNA amplification, cloning and sequencing. The SSUr­ few distinct morphological features, and are often morpholog­ DNA was amplified by PCR, following the protocol described ically variable. Xenophyophoreans can be easily mistaken for in Hol zmann et al. (2003). Several fragments of the SSUrRNA poorly preserved fragments of sponges, coelenterates, bryozo­ gene were obtained using foraminiferal specific primers (A I 0­ ans or ascidians, or regarded as inorganic conglomerates (Ten­ s13 ; s8f-sI7; sI4f-sB ) or, whenever it was possible, the eu­ dal 1972). The first xenophyophorean was described as a pr im­ karyotic universal primer pairs (s6-s14r; s 15r-s20r) (Table I) . itive foraminiferan (Brady 1883) . Later, Haeekel (1889) clas­ PCR products were cloned and sequenced as described in Hol z­ sified the xenophyophoreans as a group of deep-sea sponges, mann et al. (2003). For each PCR product, 2-3 clones were but his classification was strongly criticized by special­ sequenced in both directions, ists. Schultze (1907), who was the first to clearly demonstrate To ascertain that the obtained sequences originate from Syr­ the protistan nature of Xenophyophorea, considered them to be ingammina and not from an y other foraminiferal contaminant, an independent class of Rhizopoda. This taxonomic status has not only have we thoroughly cleaned the extracted material but been generally accepted in recent classifications, in also we have examined the sequences from 6 extractions of which Xenophyophorea are placed either as a class of Rhi zop- different fragments of granellare. Moreover, we used universal eukaryotic primers to check whether any other eukaryoti c DNA is present in our samples. Because all DNA extracts ga ve the Corresponding Author: Jan Pawlowski-Telephone number: 41 22 379 30 69; FAX number: 41 22 349 26 47; E-mail: jan.pawlowski@ same sequence, with both sp ecific and universal primers, we zoo. unige.ch assumed that the sequence is that of S. corbicula. I GenBank accession number for SSU rDNA sequence of S. corbic­ Phylogenetic analysis. Sequences were aligned manually to lila : AJ514856 the large database of for aminiferan sequences, using the Sea­ 483 484 J. EUKARYOT. MJCROBIOL., VOL. 50, NO.6, NOVEMBER-DECEMBER 2003

Table 1. List of primers used in this study.

Na01C Sequence Specificity Orientation

sA 10 5' eT C A.4A GAT TAA GCC ATG C."-A GTG G 3' foraminifera forward sl3 5' GCA ACA ATG ATT GTA TAG GC 3' foraminifera reverse s8f 5 ' T CG AT G GGG ATA GTT GG 3 ' foraminifera forward sl7 5 ' CGG TCA CGT TCG TTG C 3 ' foraminifera reverse sl4f 5 ' ACT TGA AGG ."-AT TGA eGG 3' foraminifera forward sB 5 ' TGA TCC TTC TGC AGG TTC ACC TAC 3' universal reverse s6 5' C ( CT ) G CGG TAA TTC CAG CTC 3' universal forward sl4r 5 ' CCG TCA ATT (TC) CT TTA AGT 3 ' universal reverse siSI' 5 ' GTG GTG CAT GGC CGT 3 ' universal forward s20r 5 ' GAC GGG CGG TGT GTA eM 3 ' universal reverse

view software (Gallier et a!. ]996). For analyses of complete cently published phylogeny of monothalamous Foraminifera SSUrDNA, 1,081 sites were selected, including 506 variable (Pawlowski ct al. 2002). It is supported by high bootstrap val­ and 402 phylogenetically informative sites. Analyses of partial ues and it is the sister-group to the comprised of mon­ SSUrDNA were done using 595 sites, including 198 variable othalamous lineages, including Psammosphaera and some un­ and 128 phylogenetically informative sites. Phylogenetic anal­ identified allogrorniids, as well as the polythalamous yscs werc performed using the maximum likelihood (ML) and . The relationship between Syringammina and method using the tree-building algorithm of FASTDNAML Rhizammina is well supported in all types ofanalyses (Fig. IB). (Olsen et a!. 1994) and thc neighbor joining (N]) method, ap­ Our data showing that Syringammina corbicula is a forami­ plied to distances corrected using K2, HKY, and LogDet mod­ niferan would suggest that this species possesses the granulor­ els. All characters were equally weighted and the transition­ eticulopodia. Until now, all we know about xenophyophorean transversion ratio estimated from the data was set to 1.08 and was based on few observations of cytoplasmic ex­ 0.89 for analyses of complete and partial SSUrDNA, respcc­ tensions in fixed specimens (Riemann et al . 1993; Tendal 1972) tively, The reliability of internal branches was assessed by boot­ and observation of possible pseudopodia] traces surrounding in­ strapping (Fclsenstein 1985) with 1,000 resamplings for the NJ dividuals photographed in situ on the seafloor (Lernchc et al. and 100 resarnplings for the ML tree, respectively. The Phy­ 1976). Observations of granuloreticulopodia in S. corbicula lo.win program (Galt ier et al. 1996) was used for distance com­ (Richardson 200 I) could provide an independent line of evi­ putations using various models, NJ and ML tree-building, and dence for foraminiferan origins of Xenophyophorea. However, bootstrapping. The GenBank accession numbers for all se­ it remains to be determined if their organisation and ultrastruc­ quences used in our analyses are given in Table 2. ture conforms to the refined definition of foraminiferan reticu­ lopodia (Bowser and Travis 2002). RESULTS AND DISCUSSION Placement of Syringammina among Foraminifera based on Phylogenetic analysis of complete SSUrDNA sequences molecular data is in agreement with the initial classification of shows that Syringammina corbicula branches among Forami­ this as a large agglutinated foraminiferan (Brady 1883), nifera (Fig . IA). The group is very well supported in both anal­ and its subsequent placement in the foraminiferal families yses (100% bootstrap values), presenting a long stem lineage Rhabdamminidae (Rhumbler 1913), Hyperamminidae (Cush­ due to the numerous foraminiferal specific nucleotide substitu­ man 1950), or Astrorhizidae (Loeblich and Tappan 1964). Syr­ tions. The position of the Foraminifera in the eukaryotic tree ingammina was included among Xenophyophorca by Tendal (Fig. 1A) differs from the previously published SSUrDNA phy­ (1972), who pointed, however, to its strong similarity to Fora­ logenies (Pawlowski and Holzmann 2002). To avoid the long­ minifcra. The xenophyophoreans and foraminifcrans share sev­ branch attraction artefacts, we excluded all fast evolving eu­ eral common features, not only in gross morphology of their karyotic lineages from our analyses (Berney and Pawlowski test. Some Foraminifera (for example filosa) pos­ 2003). As a result, the Foraminifera group with the , sess a multinucleate plasmodium similar to that observed in in agreement with phylogenies derived using sequences from xenophyophoreans (Pawlowski et al. 1999). Other foraminif­ (Keeling 2001) and ubiquitine (Archibald et al. 2003). The erans are known to have nuclear dimorphism (Lee et a!. 1991), position of Foraminifera as the sister-group to the filosean perhaps similar to the differentiation of nuclei observed in some oviformis is congruent with analyses of actin and RNA xenophyophoreans (Tendal 1972). Hopwood et a!. (1996) drew polymerase sequences (unpubl. data). The topology obtained attention to similarities in the cellular organization of the xen­ using the ML method (Fig . IA) is congruent with the topology ophyophore A. ramuliformis and the foraminiferan Rhizammina of NJ trees obtained using HKY and LogDet substitution mod­ algaeformis. Interestingly, Rhizammina appears as closely re­ els, but it differs from the NJ trees obtained using K2 model, lated to Syringammina in our analyses. This is congruent with where long branch of Foraminifera cluster among the morphological similarities of both genera that have a basi­ (data not shown). cal1y tubular test , with tubes containing a thread of cytoplasm To establish the position of Syringammina corbicula among and strands ofstercomata (Cartwright et a!. 1989; Gooday, pel's. Foraminifera, we compared its sequence to the partial SSUr­ info.). DNA sequences of 29 foraminiferal species (Fig. IB). In all The distinction of xcnophyophorcans is based principally on analyses, S. corbicula clustered with Rhizammina algaeformis the presence of some specific features, such as the granellare, within a clade of monothalamous Foraminifera that includes the stcrcomare, and intracellular barite crystals. However, in also such agglutinated genera as Toxisarcon, Saccammina, and view of our study, these features should be interpreted as au­ Rhabdammina, and the organic-walled genera Gloiogullmia and tapomorphies of a derived group of deep-sea Foraminifera rath­ Cylindrogullmia. This clade corresponds to lineage C in a re­ er than those of an independent eukaryotic . Syringam-

L ~~ - ~~~_- _ PAWLOWSKI ET AL. -PHYLOGEN ETIC PO SITI O N OF SYRINGAM M INA CORBlCUI.A 485

,..----- proteus A Hartmanella vermiformis AMOEBOZOA '---- castellanii .------Mytilus edulis Actinia equina OPISTHOKONTA ,------Amanita muscaria 95/ 100 venosus B .-.0.021 Het erostegina depressa Schizosaccharomyces pombe 95199 Bolivina sp. 78198 Blepharisma americanum Bolivina spothulata .....l L---Arenoparre/la mexicana L...-..__ Oxytricha nova ALVEOLATA Jadammina macrescens '------ bigemina Haplaphragmoides wilberti Prorocentrum concavum Trochammina sp. 71/100 Psammosphaera sp. 1018 Ectocarpus siliculosus Uniden. allogromiidAI83 Chrysolepidomonas dendrolepidota Uniden. allogromiid 1212 '----- Apodachlya brachynema Uniden. allogromiidAI 195 ,..---Uniden. allogromiidA313 Cafeteria roenbergensis HETEROKONTA 941100 '----Uniden. allogromiidA2I3 ,..--- Dunaliella salina Uniden. allogromiid A26 Helianthus annuus Saccammina sphaerica Gloiogul/mia sp. Mesostigma viride Rhabdammina discreta Compsopogon coeruleus RHODOPHYTA Toxisarcon synsuicidica Rhizammina algaeformis Rhodochaete parvula Syringammina corbicula .----- Coccolithus pelagicus Cylindrogullmia alba Pavlova salina HAPTOPHYTA Hemisphaerammina bradyi Notodendrodes antarctikos 100/100 Acanthometra sp. Psammophaga simplora Chaunacanthid sp. crystallifera chromatophora 100/100 Astrammina triangularis Astrammina rara rotunda

L..- Cercomonas longicauda Chlorarachnion reptans CERCOZOA Lotharella vacuolata ,..--- Gromia oviformis 1 Bolivina spathulata Nummulites venosus Trochammina sp. Syringammina corhicula '----- Allogromia sp. FORAMINIFERA 0.047 ...--- Cribrothalammina alba 100/100 68169 '---- Reticulomyxafilosa Astrammina rara 95/100 Astrammina triangularis

Fig. I. Phylogenetic position of xenophyophorean Syringa mmina corbicula among (A) and Foraminifera (B) inferred from small subunit rRNA gene sequences. Doth trees were obtained using the maximum likelihood method. Numbers at the nodes in both trees indicate bootstrap support values. higher than 60%, for maximum likelihood and neighbor joining analyses, respectively. mina corbicula possesses all typ ical xenophyophorean mo rpho­ AC KNOWLEDGMENTS logical features and therefore it can be conside red as represen­ We thank And y Gooday , Ol e Tcndal, and Sam Bowser for tative of the entire group. Nevertheless, 10 test the monoph yly comments on the manu scr ipt, and Cedric Berney for alignment of Xcnophyophorea and confirm their forarniniferan origins, the of eukaryotic SSU rRN A. This work was supported by a grant molecular study of other species and ultrastructural examination from the Sw iss National Science Foundation (3 1-59 145.99, of their pseudopodia will be necessary. 31OOAO-l 00415). Th e collection of live specimens was sup­ PA WLO\VSKI ET AL.-PHYLOGENETIC POSITION OF SYRINGAM/14lNA CORBICULA 485

r----­ A Hartmanella vermiformis AMOEBOZOA '---- Leptomyxa retieulata Aeanthamoeba eastellanii .------Mytilus edulis Aetinia equina OPISTHOKONTA B ...----- Amanita musearia 95/100 Nummulites venosus 0.021 Heterosteginadepressa I------< Schizosaeeharomyees pombe 95199 Bolivina sp. 78/98 Blepharisma amerieanum Bolivina spaihulata .....l'---Arenoparrella mexicana '---- Oxytricha nova ALVEOLATA Jadammina macrescens L- Babesia bigemina Haptophragmoides wilberti Proroeentrum eoneavum Trochammina sp. 711100 Psammosphaera sp. 1018 Eetocarpus silieulosus Uniden. allogromiid A183 Chrysolepidomonas dendrolepidota Uniden. allogromiid 1212

L--- Apodaehlya braehynema Uniden. allogromiid A1195 r---Uniden. allogromiidA313 Cafeteria roenbergensis HETEROKONTA 941100 '----Uniden. allogromiid A213 r--- Dunaliella salina Uniden. allogromiid A26 Helianthus annuus VIRIDIPLANTAE Saccammina sphaerica Gloiogullmia sp. Mesostigma viride Rhabdammina discreta Compsopogon coeruleus RHODOPHYTA Toxisarcon synsuicidica Rhizammina algaeformis Rhodoehaete parvula Syringammina corbicula r--- Coceolithus pelagicus Cylindrogullmia alba Pavlova salina HAPTOPHYTA 1001100 Hemisphaerammina bradyi Notodendrodes antarctikos 100/100 Aeanthometra sp.ACANTHAREA Psammophaga simplora Chaunacanthid sp. Allogromia crystallifera Paulinella ehromatophora 100/1QQ. Astrammina triangularis Astrammina rara Euglypha rotunda ,-=---,-,-=­-=­ Cercomonas longicauda Chlorarachnion reptans CERCOZOA Lotharella vacuolata r--- Gromia oviformis i

FORAMINIFERA 0.047 ---, 100/100 68/69

95/100

Fig. 1. Phylogenetic position of xenophyophorean Syringammina corbicula among eukaryotes (A) and Foraminifera (B) inferred from small subunit rRNA gene sequences. Both trees were obtained using the maximum likelihood method. Numbers at thc nodes in both trees indicate bootstrap support values, higher than 60%, for maximum likelihood and neighbor joining analyses, respectively. mina corbicula possesses all typical xcnophyophorean morpho­ ACKNOWLEDGMENTS logical features and therefore it can be considered as represen­ We thank Andy Gooday, Ole Tendal, and Sam Bowser for tative of the entire group. Nevertheless, to test the comments on the manuscript, and Cedric Berney for alignment of Xenophyophorca and confirm their foraminifcran origins, the of eukaryotic SSU rRNA. This work was supported by a grant molecular study of other species and ultrastructural examination from the Swiss National Science Foundation (31-59145.99, of their pseudopodia will be necessary. 31 00AO-100415). The collection of live specimens was sup­ 486 J. EUKARYOT. MICROI3JOL., VOL. 50. NO.6. NOVEMBER-DECEMBER 2003

Table 2. GenBank accession number of all sequences used in this ported in part by NSF grant OCE-9730932 to Dan McCorkle. work. This is Contribution no . 569 of the Smithsonian Marine Station at Fort Pierce, Florida, USA. Accession Phylum Species number LITERATURE CITED Amoebozoa Amoeba proteus AJ314604 Archibald, J. M., Longer, D., Pawlowski, J. & Keeling, P. J. 2003. A Hartmanella vermiformis AF426I 57 novel polyubiquitin structure in Cercozoa and Foraminifera: evidence Leptomyxa rcticulata AF293898 Acanthameoba castcllanii M13435 for a new eukaryotic supergroup. Mol. BioI. Evol., 20:62··66. Opisthokonta Mytitus edulis L33448 Berney, C . & Pawlowski. J. 2003. Revised small subunit rRNA analysis Actinia equina AJI33552 provides further evidence that Foraminifera are related to Cercozoa. Amanita muscaria AF02663I J. Mol. Evol.. 57: 1-8. Schizosaccharomyces pombe X58056 Bowser, S. S. & Travis, J. L. 2002. 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