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Subglacial Lake Vostok (Antarctica) Accretion Ice Contains a Diverse Set of Sequences from Aquatic, Marine and Sediment-Inhabiting Bacteria and Eukarya

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Subglacial Lake Vostok (Antarctica) Accretion Ice Contains a Diverse Set of Sequences from Aquatic, Marine and Sediment-Inhabiting Bacteria and Eukarya Subglacial Lake Vostok (Antarctica) Accretion Ice Contains a Diverse Set of Sequences from Aquatic, Marine and Sediment-Inhabiting Bacteria and Eukarya Yury M. Shtarkman., Zeynep A. Koc¸er.¤a, Robyn Edgar, Ram S. Veerapaneni¤b, Tom D’Elia¤c, Paul F. Morris, Scott O. Rogers* Department of Biological Sciences, Bowling Green State University, Bowling Green, Ohio, United States of America Abstract Lake Vostok, the 7th largest (by volume) and 4th deepest lake on Earth, is covered by more than 3,700 m of ice, making it the largest subglacial lake known. The combination of cold, heat (from possible hydrothermal activity), pressure (from the overriding glacier), limited nutrients and complete darkness presents extreme challenges to life. Here, we report metagenomic/metatranscriptomic sequence analyses from four accretion ice sections from the Vostok 5G ice core. Two sections accreted in the vicinity of an embayment on the southwestern end of the lake, and the other two represented part of the southern main basin. We obtained 3,507 unique gene sequences from concentrates of 500 ml of 0.22 mm-filtered accretion ice meltwater. Taxonomic classifications (to genus and/or species) were possible for 1,623 of the sequences. Species determinations in combination with mRNA gene sequence results allowed deduction of the metabolic pathways represented in the accretion ice and, by extension, in the lake. Approximately 94% of the sequences were from Bacteria and 6% were from Eukarya. Only two sequences were from Archaea. In general, the taxa were similar to organisms previously described from lakes, brackish water, marine environments, soil, glaciers, ice, lake sediments, deep-sea sediments, deep-sea thermal vents, animals and plants. Sequences from aerobic, anaerobic, psychrophilic, thermophilic, halophilic, alkaliphilic, acidophilic, desiccation-resistant, autotrophic and heterotrophic organisms were present, including a number from multicellular eukaryotes. Citation: Shtarkman YM, Koc¸er ZA, Edgar R, Veerapaneni RS, D’Elia T, et al. (2013) Subglacial Lake Vostok (Antarctica) Accretion Ice Contains a Diverse Set of Sequences from Aquatic, Marine and Sediment-Inhabiting Bacteria and Eukarya. PLoS ONE 8(7): e67221. doi:10.1371/journal.pone.0067221 Editor: Michael Watson, The Roslin Institute, University of Edinburgh, United Kingdom Received September 17, 2012; Accepted May 20, 2013; Published July 3, 2013 Copyright: ß 2013 Shtarkman et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: The project was partially funded by the National Science Foundation (ANT 0536870) and Bowling Green State University. RE was supported in part by National Science Foundation 0131969 and United States Department of Agriculture NIFA_2011-68004-30104. The 454 sequencing services were supplied by 454 Life Sciences as part of a test for their 454 GS junior pyrosequencing system. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] . These authors contributed equally to this work. ¤a Current address: Department of Infectious Diseases, Division of Virology, St. Jude Children’s Research Hospital, Memphis, Tennessee, United States of America ¤b Current address: Department of Biological Sciences, Bowling Green State University, Firelands Campus, Huron, Ohio, United States of America ¤c Current address: Biological Sciences, Indian River State College, Fort Pierce, Florida, United States of America Introduction fewer mineral inclusions, as well as lower concentrations of ions, organic carbon, and biomass [8], [10], [11]. This relatively clear Lake Vostok is the largest of nearly 400 subglacial lakes that ice is known as ‘‘type II’’ (or type 2) accretion ice. have been found in Antarctica [1–5], at least some of which are Several studies have described the biotic and abiotic compo- connected by subglacial rivers and streams [6]. As the overriding nents from Lake Vostok accretion ice core sections [8], [12–19]. 21 4 km-thick glacier moves across Lake Vostok at a rate of 3 m yr , Mean cell concentrations in the accretion ice ranged from ,1to lake water freezes (i.e., accretes) to the bottom of the glacier several hundred cells ml21. In most studies, the highest creating a lake-water record that is a linear and temporal concentrations of cells and highest sequence diversities were representation of the surface contents of the lake [7], [8]. At the reported in accretion ice from within or near the embayment in Vostok 5G ice core drill site on the far side of the lake (relative to the southwest corner of the lake near the entry point of the glacier. the glacier entry site), the meteoric ice is 3538 m thick, and the Additionally, we and others demonstrated that the concentrations accretion ice is more than 231 m thick [9]. At that location, the of total cells and viable cells were higher in the accretion ice than glacier has passed over an embayment, near a peninsula/ridge, in the meteoric ice above [12], [14–16]. In the same studies, we and then over part of the southern main lake basin [2], [8]. Ice cultivated, sequenced (rDNA regions) and identified 18 unique that accreted in the vicinity of the embayment has relatively high isolates of Bacteria and 31 unique isolates of Fungi from the same concentrations of ions, organic carbon, biomass and mineral Lake Vostok accretion ice core sections. All were phylogenetically inclusions (termed ‘‘type I’’ – or type 1 - accretion ice) [8], [10], closest to species from aquatic, lake/ocean sediment, cold, polar [11]. Over the majority of the lake, the accretion ice contains far and/or deep-sea environments. The compilation of results suggests PLOS ONE | www.plosone.org 1 July 2013 | Volume 8 | Issue 7 | e67221 Lake Vostok Metagenomics that organisms are living and reproducing in Lake Vostok. For the strand synthesis reaction consisted of the RNA and hexamer present metagenomic/metatranscriptomic study, we examined primers (above) in 50 mM Tris-HCl [pH 8.3], 75 mM KCl, two ice core sections that accreted in the vicinity of the 3 mM MgCl2, 10 mM DTT (dithiothreitol), 500 mM of each embayment (at depths 3563 and 3585 m), and two ice core dNTP (dATP, dCTP, dGTP, and dTTP), in a 20 ml volume. After sections that accreted over the southern main lake basin (at 3606 mixing, 200 U of SuperScriptH II RT (reverse transcriptase) was and 3621 m). The results of this research provide a detailed view added and mixed. This was incubated at 37uC for 1 h, and then of the potential life in Lake Vostok. placed on ice. The second strand synthesis reaction consisted of the first strand synthesis reaction in the following solution: 25 mM Materials and Methods Tris-HCl [pH 7.5], 100 mM KCl, 5 mM MgCl2,10mM + (NH4)2SO4, 0.15 mM ß-NAD , 250 mM each dNTP, 10 U The ice core sections were selected from the USGS NICL DNA ligase, 4 U DNA pol I, 2 U RNase H and 1.2 mM DTT, (United States Geological Survey, National Ice Core Laboratory, in a total volume of 150 ml. The solution was mixed and incubated Denver, CO), and were shipped frozen to our laboratory. Sample at 16uC for 2 h, then placed on ice. Next, 10 U of T4 DNA V5 consisted of Vostok 5G core sections at 3563 and 3585 m (type polymerase was added, and the reaction mix was incubated at I ice), corresponding to ice that accreted in the vicinity of the 16uC for 5 min, and then was stopped by the addition of EDTA to embayment. Sample V6 included core sections 3606 and 3621 m a final concentration of 30 mM. Then, 150 ml of chloroform/ (type II ice), corresponding to ice that accreted over a portion of isoamyl alcohol (24:1) was added and the contents of the tubes the southern main basin of Lake Vostok. Each core section was were mixed vigorously to form an emulsion. After 2 min of surface sterilized using a method that had been previously centrifugation at 16,0006g, the aqueous layer was transferred into developed, tested, described and utilized [14], [15], [20], [21]. a new tube and the nucleic acids were precipitated with 0.5 M Briefly, quartered ice core sections, 6–16 cm in length (total NaCl and cold 80% ethanol. The nucleic acids were precipitated volume approximately 125 ml), were immersed in a 5.25% sodium at 220uC for 5 min, followed by centrifugation (at 16,0006g) for hypochlorite solution (pre-chilled to 4uC for at least 2 h) for 10 s 20 min. The supernatant was decanted and the pellets were dried followed by three rinses with 800 ml of sterile water (4uC, under vacuum for 15 min. Each contained both DNA (represent- 18.2 MV, ,1 ppb total organic carbon, autoclaved). The sections ing the metagenomic portion) and cDNA (representing the were then melted in sterile funnels and meltwater was collected in metatranscriptomic portion). Both were used to assure a sufficient 50 ml aliquots. Each aliquot comprised a ‘‘shell’’ of meltwater mass of nucleic acids for pyrosequencing. corresponding to the outer portion, and sequentially more interior portions of the ice core section. The meltwater was then frozen at Adapter Ligation and Chromatography 220uC. A total of 250 ml of meltwater was used for each sample Pellets from the previous step were rehydrated in 18 mlof (125 ml from each ice core section). The meltwater samples were DEPC-treated water. Then, EcoRI (NotI) adapters were ligated to filtered sequentially through 1.2, 0.45 and 0.22 mm Durapore each end of the cDNA and DNA in the sample in order to provide filters (Millipore, Billerica, MA).
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