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Eukaryotic Phylotypes in Aquatic Moss Pillars Inhabiting a Freshwater Lake in East Antarctica, Based on 18S Rrna Gene Analysis

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Eukaryotic Phylotypes in Aquatic Moss Pillars Inhabiting a Freshwater Lake in East Antarctica, Based on 18S Rrna Gene Analysis Polar Biol (2012) 35:1495–1504 DOI 10.1007/s00300-012-1188-1 ORIGINAL PAPER Eukaryotic phylotypes in aquatic moss pillars inhabiting a freshwater lake in East Antarctica, based on 18S rRNA gene analysis Ryosuke Nakai • Takashi Abe • Tomoya Baba • Satoshi Imura • Hiroshi Kagoshima • Hiroshi Kanda • Yuji Kohara • Akiko Koi • Hironori Niki • Katsuhiko Yanagihara • Takeshi Naganuma Received: 2 December 2011 / Revised: 5 April 2012 / Accepted: 17 April 2012 / Published online: 3 May 2012 Ó The Author(s) 2012. This article is published with open access at Springerlink.com Abstract Aquatic mosses of Leptobryum species form a mini-biosphere. Batteries of 16S rRNA genotypes, or unique tower-like pillars of vegetation termed ‘‘moss pil- phylotypes, of eubacteria and cyanobacteria, but no archaea, lars’’ in Antarctic lakes. Moss pillars have distinct redox- have been identified in moss pillars. However, detailed affected sections: oxidative exteriors and reductive interiors. identification or phylogenetic analyses of the moss and their We have proposed that a ‘‘pillar’’ is a community and habitat associated eukaryotic microbiota have not been performed. of functionally interdependent organisms and may represent This study analyzed near-full-length 18S rRNA gene sequences obtained from two whole moss pillars. In total, 28 PCR clone libraries from two whole moss pillars were con- Electronic supplementary material The online version of this structed, and 96 clones from each library (total 2,688 clones) article (doi:10.1007/s00300-012-1188-1) contains supplementary material, which is available to authorized users. were randomly selected and sequenced. Molecular phylo- genetic analysis revealed that the phylotype belonging to R. Nakai Á A. Koi Á T. Naganuma (&) Bryophyta, considered to be derived from moss, was closely Graduate School of Biosphere Science, Hiroshima University, related (99.9 %) to the 18S rRNA gene sequence from 1-4-4 Kagamiyama, Higashi-Hiroshima, Hiroshima 739-8528, Japan Leptobryum pyriforme. Unexpectedly, phylotypes belong- e-mail: [email protected] ing to a novel clade of fungi dominated (approximately 27–75 %) the moss pillar libraries. This suggests that fungi R. Nakai may contribute to carbon cycling in the moss pillar as para- Japan Society for the Promotion of Science, Chiyoda-ku, Tokyo 102-8471, Japan sites or decomposers. In addition, phylotypes related to cil- iates and tardigrades were subdominant in the exterior, while Present Address: the phylotype of the ameba-like, single-celled eukaryote, R. Nakai Cercomonas (Cercozoa), was detected only in the interior. National Institute of Genetics, 1111 Yata, Mishima, Shizuoka 411-8540, Japan These features were shared by both moss pillars. The 18S rRNA gene-based profiles demonstrated that redox-related T. Abe factors may control distribution of some eukaryotic microbes Graduate School of Science and Technology, Niigata University, in a whole moss pillar. 8050 Ikarashi 2-no-cho, Nishi-ku, Niigata 950-2181, Japan T. Baba Á H. Kagoshima Á H. Niki Á K. Yanagihara Keywords Antarctic lake Á Moss pillars Á Biodiversity Á Transdisciplinary Research Integration Center, 18S rRNA gene Á Eukaryote Á Phylogenetic analyses 4-3-13 Toranomon, Minato-ku, Tokyo 105-0001, Japan S. Imura Á H. Kanda National Institute of Polar Research, 10-3 Midori-cho, Introduction Tachikawa, Tokyo 190-8518, Japan Several lakes with varying water qualities, ranging from H. Kagoshima Á Y. Kohara Á H. Niki National Institute of Genetics, 1111 Yata, Mishima, freshwater to hypersaline, are present in the ice-free areas Shizuoka 411-8540, Japan along the continental margin of Antarctica (Imura et al. 123 1496 Polar Biol (2012) 35:1495–1504 2003; Gibson et al. 2006). These lakes are model sites for strong odor of sulfur compounds, and thus, it is considered limnological and ecological studies investigating the effects that an oxygen gradient exists between the exterior and of recent global environmental changes (Convey 2006, interior (Kudoh et al. 2003a). Nakai et al. (2012) detected 2011; Laybourn-Parry 2009). Lake bottoms are known to phylotypes distributed throughout moss pillars and those in contain microbial mats consisting of algae such as cyano- each layer, using fatty acid analysis and molecular phylo- bacteria, diatoms, and green algae (Vincent 1988, 2000). The genetic analysis based on the 16S rRNA gene. Thus, bacterial lakes around the Syowa Station, situated in East Antarctica, communities differ between the exterior and interior of moss were reported to have a large moss community known as pillars and are hypothesized to participate in biogeochemical ‘‘moss pillars,’’containing not only algae but also the aquatic processes of elements such as carbon, nitrogen, and sulfur. moss of the genus Leptobryum (Imura et al. 1999). Moss Knowledge is growing about the morphological and pillars are unique biological communities forming tower- limnological features of Antarctic moss pillars and their like structures and originating from algal mats on the lake bacterial species composition. However, with regard to bottom, with large pillars being 40 cm in diameter and 80 cm mosses and the eukaryotic microbiota, only microscopic in height (Imura 2006). It is not uncommon for bryophytes to observations have been reported and no detailed identifi- form communities on lake bottoms, and such communities cations have been performed. Mosses are the major com- have been reported in polar regions, including Greenland, ponents of moss pillars. In addition, their associated King George Island and Livingston Island (South Shetland eukaryotic microbiota are considered to play a key role in Islands, Antarctica), and the Dry Valleys (continental Ant- the production and decomposition of organic matter. We arctica) (Quesada et al. 2008). However, unusual structures used molecular phylogenetic analysis based on the 18S such as moss pillars have not been reported in regions other rRNA gene to elucidate the phylogeny and diversity of than Antarctica, making them extremely unique ecosystems. mosses and eukaryotic microbiota comprising these unique Since the first description of moss pillars by Imura et al. ecosystems in Antarctic lakes. Our findings will enable (1999), much work has been conducted, including the esti- further discussion of the phylogeography of mosses and mation of growth rate by radiocarbon (14C) dating (Imura eukaryotic microorganisms in polar environments. et al. 2000), moss species and attached algae (Ohtani et al. 2001), distribution of aquatic mosses around Syowa Station (Imura et al. 2003), carbon, nitrogen, and chlorophyll Materials and methods a contents (Kudoh et al. 2003a; Imura 2006), temperature and light environment of the moss habitat (Kudoh et al. Study area 2003b; Tanabe et al. 2008), and photochemical activities of apices and sides of pillars (Kudoh et al. 2003c, 2009). Dating Antarctic moss pillar specimens were harvested on January of lake sediments revealed that lakes in the ice-free areas 19, 2000, during the 42nd Japanese Antarctic Research around Syowa Station have been formed in the few Expedition, at Lake Hotoke-Ike (69°280S, 39°340E), 1,000 years since the retreat of ice sheets following the end Skarvsnes, about 50 km south of Syowa Station in East of the last ice age (Iwasa et al. 2000; Matsumoto et al. 2006). Antarctica (Fig. 1). The water quality of the lake has been Kimura et al. (2010) were the first to describe the vertical described previously (Kudoh et al. 2003b). Two specimens profiles of temperature, salt content, dissolved oxygen, and were harvested gently by SCUBA diving. Specimen A was pH in the Lake Hotoke-Ike where moss pillars were found, 22 cm in diameter and 30 cm in height. Specimen B, which clearly showing the existence of thermocline and salinocline was used to compare moss species and eukaryotic diversity between water depths of 1–2 m. Furthermore, long-term, between samples, was 20 cm in diameter and 27 cm in continuous observations of the lakes indicated that this height. The specimens were gently placed in buckets con- stratification disappeared immediately after the ice covering taining lake water and sealed tightly. The moss pillars are on the lake surfaces melted in summer (Tanabe et al. 2008; essentially composed of long moss shoots. They are con- Kudoh et al. 2009). siderably firm structures that are soft, but not fragile. The The exterior of moss pillars is green; the apices in par- specimens were immediately and gently transported to the ticular are bright green with adherent oxygen bubbles (Imura laboratory on board the icebreaker Shirase by a helicopter. et al. 2000). It is likely that the top surface of a moss pillar is After ensuring the structural integrity of the specimens, they in a state of oxygen oversaturation because of active pho- were stored in a freezer (-20 °C) until further analysis. tosynthesis by the moss and algae. Microscopic observations showed that the cyanobacterium Leptolyngbya sp. and the DNA extraction and PCR amplification green algae Oedogonium sp. and Cosmarium sp. are attached to the sides of moss pillars (Ohtani et al. 2001). However, the Each frozen moss pillar specimen was thawed partially interior is packed with brown plant residues and gives off a and sectioned into 14 samples (7 exterior, 7 interior) by 123 Polar Biol (2012) 35:1495–1504 1497 Fig. 1 Map of the study site. Lake Hotoke-Ike, formerly known as Lake B-4-Ike, is located in the Skarvsnes ice-free area near Syowa Station in East Antarctica. Black areas represent the ice-free areas separating the interior from the exterior layer and dividing Bry-R (50-GATTACCCAGGCCTACCG-30) were designed each specimen longitudinally into 7 horizontal sections. A using the 18S rRNA gene sequences for B. capillare sterile knife was used for sectioning the specimens. Exterior (AF205945), B. donianum (AF023704), B. caespiticium sections were labeled O1–O7, and interior sections were (AF023703), B. alpinum (AF023700), and B. argenteum labeled I1–I7, as described previously (Nakai et al. 2012). (BAU18529). The PCR-amplified product was approxi- Sections were prepared by freeze-drying and then grinding mately 1,300 bp in length.
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