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Phylogenetic Affiliations of Mesopelagic Acantharia And ARTICLE IN PRESS Protist, Vol. 161, 197–211, April 2010 http://www.elsevier.de/protis Published online date 30 December 2009 ORIGINAL PAPER Phylogenetic Affiliations of Mesopelagic Acantharia and Acantharian-like Environmental 18S rRNA Genes off the Southern California Coast Ilana C. Gilga,1,2, Linda A. Amaral-Zettlerb, Peter D. Countwaya, Stefanie Moorthic, Astrid Schnetzera, and David A. Carona aDepartment of Biological Sciences, University of Southern California, 3616 Trousdale Pkwy AHF 301, Los Angeles, CA 90089-0371, USA bThe Josephine Bay Paul Center for Comparative Molecular Biology and Evolution, Marine Biological Laboratory, 7 MBL Street, Woods Hole, MA 02543, USA cCarl-von-Ossietzky Universitat¨ Oldenburg, ICBM-Terramare, Schleusenstr. 1, D-26382 Wilhelmshaven, Germany Submitted March 20, 2009; Accepted September 19, 2009 Monitoring Editor: David Moreira Incomplete knowledge of acantharian life cycles has hampered their study and limited our understanding of their role in the vertical flux of carbon and strontium. Molecular tools can help identify enigmatic life stages and offer insights into aspects of acantharian biology and evolution. We inferred the phylogenetic position of acantharian sequences from shallow water, as well as acantharian-like clone sequences from 500 and 880 m in the San Pedro Channel, California. The analyses included validated acantharian and polycystine sequences from public databases with environmental clone sequences related to acantharia and used Bayesian inference methods. Our analysis demonstrated strong support for two branches of unidentified organisms that are closely related to, but possibly distinct from the Acantharea. We also found evidence of acantharian sequences from mesopelagic environments branching within the chaunacanthid clade, although the morphology of these organisms is presently unknown. HRP-conjugated probes were developed to target Acantharea and phylotypes from Unidentified Clade 1 using Catalyzed Reporter Deposition Fluorescence In Situ Hybridization (CARD-FISH) on samples collected at 500 m. Our CARD-FISH experiments targeting phylotypes from an unidentified clade offer preliminary glimpses into the morphology of these protists, while a morphology for the aphotic acantharian lineages remains unknown at this time. & 2009 Elsevier GmbH. All rights reserved. Key words: 18S rRNA phylogeny; Acantharea; CARD-FISH; deep-sea protist; novel protistan lineage; sarcodine. 1Corresponding author; fax +1 207 633 9661 e-mail [email protected] (I.C. Gilg). 2Current address: Bigelow Laboratory for Ocean Sciences, 180 McKown Point Rd., West Boothbay Harbor, ME 04575, USA. & 2009 Elsevier GmbH. All rights reserved. doi:10.1016/j.protis.2009.09.002 ARTICLE IN PRESS 198 I.C. Gilg et al. Introduction Acantharia are amoeboid, mixotrophic protists and common constituents of the microplankton community in euphotic oceanic ecosystems. They have traditionally been distinguished from other sarcodine protists such as the polycystine and phaeodarian radiolaria and foraminifera by the composition of their exquisite skeletons, which are comprised of SrSO4 in a Mullerian¨ arrange- ment of 20 (in rare cases, 10) spicules (Fig. 1). Most acantharia possess tens to hundreds of photosynthetic eukaryotic symbionts per cell (Michaels 1991; Michaels et al. 1995). Total primary production within the cytoplasmic network of these and other sarcodines has been measured at more than four orders of magnitude greater than that of an equivalent volume of surrounding water (Caron et al. 1995). High rates of primary productivity in these associations reflect the fact that the microenvironment of the sarcodine is highly enriched in algal biomass relative to the surrounding oligotrophic environment, and to the observation that symbionts are typically at or close to their maximal gross growth rates within these symbiotic associations (Stabell et al. 2002). Together, these factors suggest that symbiont photosynthesis can represent a significant portion of open ocean primary production when sarcodine abundances are high. Acantharia often numerically dominate other sarcodines in open ocean ecosystems (Caron and Swanberg 1990). During ‘‘bloom-like’’ conditions (Massera Bottazzi and Andreoli 1981, 1982; Zas’ko and Vedernikov 2003), acantharian abundances have been reported at integrated densities from 1.53 to 5.34 Â 105 mÀ2.Itis estimated that they comprise up to 41% of total integrated production during these events Figure 1.(A) An example of Acanthometra sp. 1 in (Michaels 1988). These values represent signifi- its vegetative state. (B) The same organism, after cant amounts of carbon fixation in the oligotrophic releasing swarmers. The swarmers are visible as euphotic oceans and demonstrate the potential small dots around the skeleton. Note that the central for acantharia to exert a substantial influence on skeletal junction, an important feature for taxonomic marine carbon budgets. Furthermore, acantharian identification, is only visible after swarmers have blooms may contribute significantly to export flux been released. Scale bars=50 mm. (particularly Sr flux) from surface waters given their large cell size and dense skeletons (Michaels and Silver 1993; Michaels et al. 1995). swarmer cells produce individual crystals of Acantharia are thought to exert the most SrSO4 (Anderson 1983). Strontium was consid- significant biological influence on strontium bud- ered a conservative element in marine environ- gets in the ocean due to their unique celestite ments until slight variations in the Sr/Cl ratios of skeletons (Bernstein et al. 1987). Acantharia are the upper 400 m were detected (Brass and the only protists known to make their skeletons Turekian 1974). Studies that followed implicated entirely from SrSO4, although some radiolarian the crystallization and dissolution of acantharian ARTICLE IN PRESS Discovery of Acantharian-like Protists 199 celestite as the cause of this strontium flux et al. 2002; Lopez-Garcia et al. 2001; Lovejoy et al. (Bernstein et al. 1987; Bernstein and Byrne 2004; 2006; Not et al. 2007). Acantharian-like clones De Deckker 2004). Seawater is highly under- from deep-sea and mesopelagic environmental saturated with respect to strontium, so acantharia clone libraries have been observed in the Atlantic must continuously expend energy to create the (Countway et al. 2007) and in the San Pedro unique cellular structures that constitute their Channel off the coast of California (Countway skeletons. Sinking acantharian celestite from both et al. submitted; Schnetzer et al. in preparation) skeletons and cysts is thought to dissolve by respectively. Countway et al. (2007) reported 900 m, where stabilization of the Sr/Cl ratios has significant percentages (up to 17%) of the total been observed (Bernstein et al. 1987). The protistan phylotypes from 2500 m in the Sargasso selective removal of Sr from surface waters, where Sea belonging to acantharia or acantharian-like vegetative acantharia are most abundant, also organisms. Acantharian-like sequences have also accounts for the variability of Sr/Ca ratios in the been reported in clone libraries from the Sargasso euphotic zone (De Deckker 2004) and helps Sea (Moon-van der Staay et al. 2001; Not et al. interpret anomalies in historical sea-surface data 2007) from 2000 m at the Antarctic polar front sets constructed from Sr/Ca ratios from corals. (Lopez-Garcia et al. 2001), sediment collected Acantharia have also been implicated in other from the mid-Atlantic ridge (Lopez-Garcia et al. elemental cycling, most notably barium, which 2003), sediment in the southern Guaymas vent can comprise up to 0.4% of the skeleton. These field (Edgcomb et al. 2002), aphotic Arctic waters concentrations are ten times greater than that of (Lovejoy et al. 2006), the anoxic Caricao basin seawater (Bernstein et al. 1999) and may be the (Stoeck et al. 2003), and from an anoxic hypersa- source of mysteriously abundant strontium-rich line basin (Alexander et al. 2009). This is striking barite particles in the deep ocean (Bernstein and because, to our knowledge, acantharia have not Byrne 2004). been observed at such depths based on micro- Despite their important biogeochemical influ- scopical analyses. Heavily skeletonized forms ences in the ocean, relatively little is known about such as reproductive cysts have been observed acantharian biology or ecology. Study of their as deep as 900 m (Bernstein et al. 1987) but biology has been hindered by the fact that they, dissolution of the skeleton is presumed to occur like most large planktonic sarcodine protists, below this depth and the fate of the cells is cannot be maintained in culture through succes- unknown. The abundance of acantharian-like sive generations or even maintained very long sequences at depths greater than 900 m suggests after capture. Although acantharia have not been that there may be uncharacterized mesopelagic or cultured in the laboratory, formation and release of deep-sea life cycle stages that are presently ‘swarmer’ cells from freshly-collected organisms unrecognizable by morphology alone. has been observed. This process involves the Molecular diversity studies that have identified reorganization of the multinucleated vegetative possible acantharia often have not presented cytoplasm or cyst into tens of thousands of complete sequences of these phylotypes and flagellated, mononuclear cells (Caron and Swan- some have not performed the phylogenetic berg 1990). It has been hypothesized that certain analyses necessary for conclusive identifica-
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