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A New Genus of Xenophyophores (Foraminifera) from Japan Trench: Morphological Description, Molecular

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A New Genus of Xenophyophores (Foraminifera) from Japan Trench: Morphological Description, Molecular Zoological Journal of the Linnean Society, 2009, 156, 455–464. With 5 figures A new genus of xenophyophores (Foraminifera) from Japan Trench: morphological description, molecular phylogeny and elemental analysiszoj_493 455..464 BÉATRICE LECROQ1*, ANDREW JOHN GOODAY2, MASASHI TSUCHIYA3 and JAN PAWLOWSKI1 1Department of Zoology and Animal Biology, University of Geneva, Switzerland 2National Oceanographic Center, Southampton, Empress Dock, European Way, Southampton, SO14 3ZH, UK 3Institute for Research on Earth Evolution, Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokosuka, Kanagawa 237-0061, Japan Received 28 April 2008; accepted for publication 19 June 2008 The deep-sea floor is inhabited by a number of unusual and enigmatic taxa, unknown in shallow waters. These include the xenophyophores, a group of giant protists that construct fragile agglutinated tests. Here, we describe Shinkaiya lindsayi gen. et sp. nov., a new xenophyophore collected by the submersible Shinkai 6500 at a depth of 5435 m near the Japan Trench. The phylogenetic analysis performed on its complete small-subunit ribosomal DNA (SSU rDNA) sequence confirms that Sh. lindsayi sp. nov. is a foraminiferan that is closely related to another xenophyophore, Syringammina corbicula Richardson, 2001, and to a monothalamous (single-chambered) foramin- iferan Rhizammina algaeformis Brady, 1879. In terms of morphology, the new genus resembles Syringammina, but its test wall is thicker, softer, and more weakly cemented. Moreover, the SSU rDNA sequences of the two genera are highly divergent. Mass spectra analyses reveal unusually high concentrations of some elements, such as lead, uranium, and mercury. The granellare system (the cytoplasm and the organic sheath that encloses it) is apparently devoid of barite crystals, which are usually abundant as intracellular inclusions in xenophyophores, but is rich in mercury (with 12 times the concentration of mercury found in the surrounding sediment). Fecal pellets retained within a tubular system (stercomare) concentrate heavy metals, including lead and uranium (respectively, two and six times more than that of the sediment). Based on a comparison of the compositions of the agglutinated test wall, the granellare, the stercomare, and the surrounding sediment, we discuss the impact of xenophyophores on their habitat. © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 156, 455–464. ADDITIONAL KEYWORDS: deep-sea – mass spectrometry – microscopy – ribosomal DNA – xenophyophorea. INTRODUCTION morphologies. Xenophyophores are often very fragile, easily fragmented, and have no proven fossil record Despite many years of study, the fauna of the deep- (Levin, 1994). This may be one of the reasons why sea remains poorly known. The xenophyophores are they were poorly studied until recently, despite their one particularly enigmatic group. These spectacularly wide occurrence in the deep sea, and their importance large protists are extremely abundant in productive for bioturbation. Indeed, the enhanced particules parts of the deep ocean. They are benthic deposit deposition in their vicinity would provide food and feeders that build an agglutinated test, often greater refuge to their associate fauna, which increase the than 10 cm in diameter, consisting mainly of foreign biological mixing of the sediment (Levin et al., 1986). particles (xenophyae), and with a wide variety of Syringammina fragilissima Brady, 1883, the first species to be described, was classified as a foramin- iferan. Later, however, xenophyophores were *Corresponding author. E-mail: [email protected] considered successively as sponges (Haeckel, 1889), © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 156, 455–464 455 456 B. LECROQ ET AL. members of an independent class of Rhizopoda MATERIAL AND METHODS (Schulze, 1907), or as a new eukaryotic phylum SAMPLE COLLECTION (Lee, Leedale & Bradbury, 2000). Recently, molecular The single specimen was collected by an MBARI-type studies showed that Syringammina corbicula push core during the RV Yokosuka cruise YK07/15 to Richardson, 2001 is indeed related to monoth- the Japan Trench off Sanriku, using the submer- alamous foraminiferans (Pawlowski et al., 2003). sible Shinkai 6500 (dive 1037; 38°14.8175′N, Nevertheless, the monophyly of the group remains 147°00.1885′E; water depth, 5435 m; October 2007). unproven. After recovery, the specimen was split into two main Fourteen genera and almost 60 species of xeno- pieces: one to be deposited in the National Museum of phyophores are now described (Gooday & Tendal, Nature and Science, Tokyo, and the other to be used 2000). Large species are epifaunal, but a few for analyses. Fragments of the specimen were either smaller, infaunal species are also known. Most fixed in formalin (for morphology investigations) or resemble agglutinated foraminifera, in having a test guanidine buffer (for DNA analyses); the rest was composed of foreign particles. The internal organi- immediately frozen at -20 °C. zation of xenophyophores is distinctive. The multi- nucleate cytoplasm and the organic tube that encloses it comprise together the granellare system. MICROSCOPY Faecal pellets (stercomata) enclosed within an Fragments of Shinkaiya lindsayi gen. et sp. nov. were organic sheath form the stercomare system. Another broken open and examined with a light microscope. distinctive feature of the xenophyophores is the Nuclei were observed under a UV microscope after presence of barium sulphate crystals (granellae) the granellare strands had been stained for 3 min throughout the cytoplasm, and sometimes within in a 50% solution of 4′,6-diamidino-2-phenylindole the stercomare. The crystallography of these crys- (DAPI). Other fragments were critical-point dried, tals has been investigated (Hopwood, Mann & before being coated with platinium and examined in a Gooday, 1997), but their function, if any, is still a scanning electron microscope (SEM), operating at matter of debate. 1.5 kV (Jeol 6300F, field emission). For transmission Xenophyophores are often abundant beneath pro- electronic microscopy observations (TEM; Phillips ductive waters, where the flux of organic matter to CM12, tungsten filament), fragments of the specimen the seafloor is high (Tendal, 1972). Their diets prob- were dehydrated in a series of graded alcohols and ably comprise detrital particles obtained by suspen- propylene oxide before being embedded in EPON sion feeding (Tendal, 1972), surface-deposit feeding resin. Semithin sections (0.6–0.7-mm thick) were (Lemche et al., 1976), or by being trapped within stained with a mixture of methylene blue and Azur II. the folds and spaces of the often morphologically Thin sections (60–70-nm thick) were contrasted with complex test (Levin & Thomas, 1988). It is possible lead citrate and uranyl acetate, and were viewed that organic material concentrated in this way is on coated 200-mm nickel grids in a graphite holder. digested within invaginations of the cell wall, and Energy dispersive X-ray spectrographic microanaly- that the indigestible remnants are accumulated into ses (EDAX) was performed in conjunction with TEM. stercomata (Tendal, 1979; Hopwood et al., 1997). It has also been suggested that stercomares are used to cultivate bacteria as an additional food source MASS SPECTROMETRY (Tendal, 1979). Some support for this idea is pro- Fragments were analysed by inductively coupled vided by studies of lipid biomarkers, which suggest plasma mass spectrometry (ICPMS; Agilent 7500). a diet rich in bacteria (Laureillard, Méjanelle & Pieces of the test, stercomare, and granellare were Sibuet, 2004). Large, epifaunal xenophyophores may separately dissolved in a mixture of nitric and hydrof- constitute important habitat structures on the sea- luoric acid prior to being analysed. Two additional floor, providing refuges and possibly sustenance for sediment samples were prepared in the same way: numerous small metazoans (Levin & Thomas, 1988; one from the same site as Shinkaiya (1037), Levin & Gooday, 1992) and foraminifera (Hughes & the other from another site (1036; 39°24.1602′N, Gooday, 2004). 144°26.1275′E; water depth, 6406 m; October 2007) In this paper, we describe a new species and genus approximately 145 nautical miles away. of xenophyophore from the North-West Pacific, and discuss its phylogenetic position according to the com- plete small-subunit ribosomal DNA (SSU rDNA) MOLECULAR AND PHYLOGENETIC ANALYSES sequence. We also performed a chemical analysis of The complete SSU rDNA of Sh. lindsayi sp. nov. was different parts of the organism, and compared this obtained by PCR amplifications and cloning according with the surrounding sediment. to the protocol described in Schweizer et al. (2008). © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 156, 455–464 A NEW GENUS OF XENOPHYOPHORES (FORAMINIFERA) 457 Figure 1. Schematic representation of the small-subunit ribosomal DNA (SSU rDNA) sequence of Shinkaiya lindsayi gen. et sp. nov., showing the conserved regions, as well as the largest insertion and primers used for DNA amplifications. Several overlapping fragments of SSU rDNA were reticulated structure composed of bar-shaped elements separately amplified using foraminiferal-specific (~0.5 cm in diameter), separated by open spaces. Test primers: A10, 5′-CTCAAAGATTAAGCCATGCAAGT with smooth outer surface; wall relatively thick, soft, GG-3′; s4F, 5′-TCTAAGGAACGCAGCAGG-3′; s13, weakly cemented,
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