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Living at the Limits: Evidence for Microbial Eukaryotes Thriving under Pressure in Deep Anoxic, Hypersaline Habitats

DOI: 10.1155/2014/532687

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Abstract:

The advent of molecular tools in microbial ecology paved the way to exploit the diversity of microbes in extreme environments. Here, we review these tools as applied in one of the most polyextreme habitats known on our planet, namely, deep hypersaline anoxic basins (DHABs), located at ca. 3000–3500?m depth in the Eastern Mediterranean Sea. Molecular gene signatures amplified from environmental DHAB samples identified a high degree of genetic novelty, as well as distinct communities in the DHABs. Canonical correspondence analyses provided strong evidence that salinity, ion composition, and anoxia were the strongest selection factors shaping protistan community structures, largely preventing cross-colonization among the individual basins. Thus, each investigated basin represents a unique habitat (“isolated islands of evolution”), making DHABs ideal model sites to test evolutionary hypotheses. Fluorescence in situ hybridization assays using specifically designed probes revealed that the obtained genetic signatures indeed originated from indigenous polyextremophiles. Electron microscopy imaging revealed unknown ciliates densely covered with prokaryote ectosymbionts, which may enable adaptations of eukaryotes to DHAB conditions. The research reviewed here significantly advanced our knowledge on polyextremophile eukaryotes, which are excellent models for a number of biological research areas, including ecology, diversity, biotechnology, evolutionary research, physiology, and astrobiology. 1. Introduction Ocean bottom surveys in the early 1980s observed abyssal depressions at a depth of more than 3000?m in the Eastern Mediterranean Sea showing unusual reflection profiles and backscatter images [1, 2]. Subsequent hydrochemical analyses of the water trapped in these depressions identified the respective environments as deep hypersaline anoxic basins (DHABs) [1, 3, 4]. With the most recent discovery [5], there are eight known DHABs in the Eastern Mediterranean Sea, distributed in the Strabo Trench (Tyro), the Mediterranean Ridge (Bannock, Kryos, Medee, and Thetis), and the Medriff Corridor (L’Atalante, Discovery, and Urania) ([6], Figure 1). The formation of DHAB brines is reviewed in Cita [7]. They originated by submarine dissolution of Messinian evaporites (late Miocene, ca. 6 MYA) thought to originate primarily from the dissolution of evaporites ~2000–176,000 years ago. Due to the fact that different minerals deposit in different orders depending on evaporation conditions, evaporites may contain different concentrations of halite (NaCl-mineral), kieserite

References

[1]  G. J. de Lange and H. L. Ten Haven, “Recent sapropel formation in the eastern Mediterranean,” Nature, vol. 305, no. 5937, pp. 797–798, 1983.
[2]  A. Camerlenghi, “Anoxic basins of the eastern Mediterranean: geological framework,” Marine Chemistry, vol. 31, no. 1–3, pp. 1–19, 1990.
[3]  D. Jongsma, A. R. Fortuin, W. Huson et al., “Discovery of an anoxic basin within the strabo trench, eastern mediterranean,” Nature, vol. 305, no. 5937, pp. 795–797, 1983.
[4]  M. B. Cita, F. S. Aghib, A. Cambi et al., “Precipitazione attuale di gesso in un bacino anossico profondo, prime osservazioni geologiche, idrologiche, paleontologiche sul Bacino Bannock (Mediterraneo orientale),” Geol, vol. 47, pp. 143–163, 1985.
[5]  V. la Cono, F. Smedile, G. Bortoluzzi et al., “Unveiling microbial life in new deep-sea hypersaline Lake Thetis. Part I: prokaryotes and environmental settings,” Environmental Microbiology, vol. 13, no. 8, pp. 2250–2268, 2011.
[6]  M. M. Yakimov, V. la Cono, V. Z. Slepak et al., “Microbial life in the Lake Medee, the largest deep-sea salt-saturated formation,” Scientific Reports, vol. 3, article 3554, 2013.
[7]  M. B. Cita, “Exhumation of Messinian evaporites in the deep-sea and creation of deep anoxic brine-filled collapsed basins,” Sedimentary Geology, vol. 188-189, pp. 357–378, 2006.
[8]  K. J. Hsü, M. B. Cita, and W. B. F. Ryan, “The origin of the Mediterranean evaporites,” Initial Reports of the Deep Sea Drilling Project, vol. 13, no. 1-2, pp. 1203–1231, 1973.
[9]  F. H. Stewart, Marine Evaporites, United States Government Printing Office, Washington, DC, USA, 1963.
[10]  G. J. de Lange, J. J. Middelburg, C. H. van der Weijden et al., “Composition of anoxic hypersaline brines in the Tyro and Bannock Basins, eastern Mediterranean,” Marine Chemistry, vol. 31, no. 1–3, pp. 63–88, 1990.
[11]  V. P. Edgcomb, W. Orsi, H.-W. Breiner et al., “Novel active kinetoplastids associated with hypersaline anoxic basins in the Eastern Mediterranean deep-sea,” Deep-Sea Research I: Oceanographic Research Papers, vol. 58, no. 10, pp. 1040–1048, 2011.
[12]  P. W. J. J. van der Wielen, H. Bolhuis, S. Borin et al., “The enigma of prokaryotic life in deep hypersaline anoxic basins,” Science, vol. 307, no. 5706, pp. 121–123, 2005.
[13]  K. Wallmann, E. Suess, G. H. Westbrook, G. Winckler, and M. B. Cita, “Salty brines on the Mediterranean sea floor,” Nature, vol. 387, no. 6628, pp. 31–32, 1997.
[14]  S. Borin, L. Brusetti, F. Mapelli et al., “Sulfur cycling and methanogenesis primarily drive microbial colonization of the highly sulfidic Urania deep hypersaline basin,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 23, pp. 9151–9156, 2009.
[15]  D. Daffonchio, S. Borin, T. Brusa et al., “Stratified prokaryote network in the oxic-anoxic transition of a deep-sea halocline,” Nature, vol. 440, no. 7081, pp. 203–207, 2006.
[16]  M. M. Yakimov, V. la Cono, R. Denaro et al., “Primary producing prokaryotic communities of brine, interface and seawater above the halocline of deep anoxic lake L'Atalante, Eastern Mediterranean Sea,” ISME Journal, vol. 1, no. 8, pp. 743–755, 2007.
[17]  G. T. Taylor, M. Iabichella, T.-Y. Ho et al., “Chemoautotrophy in the redox transition zone of the Cariaco Basin: a significant midwater source of organic carbon production,” Limnology and Oceanography, vol. 46, no. 1, pp. 148–163, 2001.
[18]  E. Alexander, A. Stock, H.-W. Breiner et al., “Microbial eukaryotes in the hypersaline anoxic L'Atalante deep-sea basin,” Environmental Microbiology, vol. 11, no. 2, pp. 360–381, 2009.
[19]  V. Edgcomb, W. Orsi, C. Leslin et al., “Protistan community patterns within the brine and halocline of deep hypersaline anoxic basins in the eastern Mediterranean Sea,” Extremophiles, vol. 13, no. 1, pp. 151–167, 2009.
[20]  A. Stock, H.-W. Breiner, M. Pachiadaki et al., “Microbial eukaryote life in the new hypersaline deep-sea basin Thetis,” Extremophiles, vol. 16, no. 1, pp. 21–34, 2012.
[21]  D. A. Caron, P. D. Countway, A. C. Jones, D. Y. Kim, and A. Schnetzer, “Marine protistan diversity,” Annual Review of Marine Science, vol. 4, pp. 467–493, 2012.
[22]  S. Epstein and P. López-García, ““Missing” protists: a molecular prospective,” Biodiversity and Conservation, vol. 17, no. 2, pp. 261–276, 2008.
[23]  W. D. Grant, “Life at low water activity,” Philosophical Transactions of the Royal Society B: Biological Sciences, vol. 359, pp. 1249–1267, 2004.
[24]  R. Logares, J. Br?te, S. Bertilsson, J. L. Clasen, K. Shalchian-Tabrizi, and K. Rengefors, “Infrequent marine-freshwater transitions in the microbial world,” Trends in Microbiology, vol. 17, no. 9, pp. 414–422, 2009.
[25]  D. Forster, A. Behnke, and T. Stoeck, “Meta-analyses of environmental sequence data identify anoxia and salinity as parameters shaping ciliate communities,” Systematics and Biodiversity, vol. 10, pp. 277–288, 2012.
[26]  J. Elloumi, J.-F. Carrias, H. Ayadi, T. Sime-Ngando, and A. Boua?n, “Communities structure of the planktonic halophiles in the solar saltern of Sfax, Tunisia,” Estuarine, Coastal and Shelf Science, vol. 81, no. 1, pp. 19–26, 2009.
[27]  J. S. Park and A. G. B. Simpson, “Characterization of halotolerant Bicosoecida and Placididea (Stramenopila) that are distinct from marine forms, and the phylogenetic pattern of salinity preference in heterotrophic stramenopiles,” Environmental Microbiology, vol. 12, no. 5, pp. 1173–1184, 2010.
[28]  M. F. Estep and T. C. Hoering, “Stable hydrogen isotope fractionations during autotrophic and mixotrophic growth of microalgae,” Plant Physiology, vol. 67, no. 3, pp. 474–477, 1981.
[29]  J. Ruinen, “Notizen über Ciliaten aus konzentrierten Salzgew?ssern,” Zoologische Mededelingen, vol. 20, pp. 243–256, 1938.
[30]  F. J. Post, L. J. Borowitzka, M. A. Borowitzka, B. Mackay, and T. Moulton, “The protozoa of a Western Australian hypersaline lagoon,” Hydrobiologia, vol. 105, no. 1, pp. 95–113, 1983.
[31]  D. J. Patterson and A. G. B. Simpson, “Heterotrophic flagellates from coastal marine and hypersaline sediments in Western Australia,” European Journal of Protistology, vol. 32, no. 4, pp. 423–448, 1996.
[32]  J. S. Park, B. C. Cho, and A. G. B. Simpson, “Halocafeteria seosinensis gen. et sp. nov. (Bicosoecida), a halophilic bacterivorous nanoflagellate isolated from a solar saltern,” Extremophiles, vol. 10, no. 6, pp. 493–504, 2006.
[33]  J. Ruinen, “Notizen über Salzflagellaten II. über die Verbreitung der Salzflagellaten,” Archiv für Protistenkunde, vol. 90, pp. 210–258, 1938.
[34]  J. Tucolesco, “Etudes Protozoologiques sur les eaux Roumaines. I. Espèces nouvelles d’Infusoires de la mer Noire et des Bassins salés Paramarins,” Archiv für Protistenkunde, vol. 106, pp. 1–36, 1962.
[35]  G. F. Esteban and B. J. Finlay, “Cryptic Freshwater Ciliates in a Hypersaline Lagoon,” Protist, vol. 154, no. 3-4, pp. 411–418, 2003.
[36]  J. Elloumi, J.-F. Carrias, H. Ayadi, T. Sime-Ngando, M. Boukhris, and A. Boua?n, “Composition and distribution of planktonic ciliates from ponds of different salinity in the solar saltwork of Sfax, Tunisia,” Estuarine, Coastal and Shelf Science, vol. 67, no. 1-2, pp. 21–29, 2006.
[37]  N. Gunde-Cimerman, J. Ramos, and A. Plemenita?, “Halotolerant and halophilic fungi,” Mycological Research, vol. 113, no. 11, pp. 1231–1241, 2009.
[38]  Y. Lei, K. Xu, J. Ki Choi, H. Pyo Hong, and S. A. Wickham, “Community structure and seasonal dynamics of planktonic ciliates along salinity gradients,” European Journal of Protistology, vol. 45, no. 4, pp. 305–319, 2009.
[39]  A. Oren, “Biodiversity in highly saline environments,” in Physiology and Biochemistry of Extremophiles, C. Gerday and N. Glansdorff, Eds., pp. 223–231, ASM Press, Washington, DC, USA, 2007.
[40]  T. Fenchel and B. J. Finlay, Ecology and Evolution in Anoxic Worlds, Oxford University Press, Oxford, UK, 1995.
[41]  S. Y. Moon-van der Staay, R. de Wachter, and D. Vaulot, “Oceanic 18S rDNA sequences from picoplankton reveal unsuspected eukaryotic diversity,” Nature, vol. 409, no. 6820, pp. 607–610, 2001.
[42]  B. Díez, C. Pedrós-Alió, and R. Massana, “Study of genetic diversity of eukaryotic picoplankton in different oceanic regions by small-subunit rRNA gene cloning and sequencing,” Applied and Environmental Microbiology, vol. 67, no. 7, pp. 2932–2941, 2001.
[43]  P. López-García, F. Rodríguez-Valera, C. Pedrós-Alió, and D. Moreira, “Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton,” Nature, vol. 409, no. 6820, pp. 603–607, 2001.
[44]  S. C. Dawson and N. R. Pace, “Novel kingdom-level eukaryotic diversity in anoxic environments,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 12, pp. 8324–8329, 2002.
[45]  P. López-García, H. Philippe, F. Gail, and D. Moreira, “Autochthonous eukaryotic diversity in hydrothermal sediment and experimental microcolonizers at the Mid-Atlantic Ridge,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 2, pp. 697–702, 2003.
[46]  T. Stoeck and S. Epstein, “Novel eukaryotic lineages inferred from small-subunit rRNA analyses of oxygen-depleted marine environments,” Applied and Environmental Microbiology, vol. 69, no. 5, pp. 2657–2663, 2003.
[47]  K. Romari and D. Vaulot, “Composition and temporal variability of picoeukaryote communities at a coastal site of the English Channel from 18S rDNA sequences,” Limnology and Oceanography, vol. 49, no. 3, pp. 784–798, 2004.
[48]  P. D. Countway, R. J. Gast, P. Savai, and D. A. Caron, “Protistan diversity estimates based on 18S rDNA from seawater incubations in the Western North Atlantic,” Journal of Eukaryotic Microbiology, vol. 52, no. 2, pp. 95–106, 2005.
[49]  A. Behnke, J. Bunge, K. Barger, H.-W. Breiner, V. Alla, and T. Stoeck, “Microeukaryote community patterns along an O2/H2S gradient in a supersulfidic anoxic Fjord (Framvaren, Norway),” Applied and Environmental Microbiology, vol. 72, no. 5, pp. 3626–3636, 2006.
[50]  R. J. Gast, D. M. Moran, D. J. Beaudoin, J. N. Blythe, M. R. Dennett, and D. A. Caron, “Abundance of a novel dinoflagellate phylotype in the Ross Sea, Antarctica,” Journal of Phycology, vol. 42, no. 1, pp. 233–242, 2006.
[51]  C. Lovejoy, R. Massana, and C. Pedrós-Alió, “Diversity and distribution of marine microbial eukaryotes in the arctic ocean and adjacent seas,” Applied and Environmental Microbiology, vol. 72, no. 5, pp. 3085–3095, 2006.
[52]  A. Z. Worden, “Picoeukaryote diversity in coastal waters of the Pacific Ocean,” Aquatic Microbial Ecology, vol. 43, no. 2, pp. 165–175, 2006.
[53]  A. Zuendorf, A. Behnke, J. Bunge, K. J.-A. Barger, and T. Stoeck, “Diversity estimates of microeukaryotes below the chemocline of the anoxic Mariager Fjord, Denmark,” FEMS Microbiology Ecology, vol. 58, no. 3, pp. 476–491, 2006.
[54]  A. Stock, K. Jürgens, J. Bunge, and T. Stoeck, “Protistan diversity in suboxic and anoxic waters of the Gotland Deep (Baltic Sea) as revealed by 18SrRNA clone libraries,” Aquatic Microbial Ecology, vol. 55, no. 3, pp. 267–284, 2009.
[55]  M. L. Sogin, H. G. Morrison, J. A. Huber et al., “Microbial diversity in the deep sea and the underexplored ‘rare biosphere’,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 32, pp. 12115–12120, 2006.
[56]  L. F. W. Roesch, R. R. Fulthorpe, A. Riva et al., “Pyrosequencing enumerates and contrasts soil microbial diversity,” ISME Journal, vol. 1, no. 4, pp. 283–290, 2007.
[57]  T. Stoeck, A. Behnke, R. Christen et al., “Massively parallel tag sequencing reveals the complexity of anaerobic marine protistan communities,” BMC Biology, vol. 7, article 1741, p. 72, 2009.
[58]  T. Stoeck, D. Bass, M. Nebel et al., “Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water,” Molecular Ecology, vol. 19, no. 1, pp. 21–31, 2010.
[59]  L. A. Amaral-Zettler, E. A. McCliment, H. W. Ducklow, and S. M. Huse, “A method for studying protistan diversity using massively parallel sequencing of V9 hypervariable regions of small-subunit ribosomal RNA Genes,” PLoS ONE, vol. 4, no. 7, Article ID e6372, 2009.
[60]  A. Chao, R. L. Chazdon, R. K. Colwell, and T.-J. Shen, “Abundance-based similarity indices and their estimation when there are unseen species in samples,” Biometrics, vol. 62, no. 2, pp. 361–371, 2006.
[61]  B. Haegeman, J. Hamelin, J. Moriarty, P. Neal, J. Dushoff, and J. S. Weitz, “Robust estimation of microbial diversity in theory and in practice,” The ISME Journal, vol. 7, no. 6, pp. 1092–1101, 2013.
[62]  T. Stoeck, A. Zuendorf, H.-W. Breiner, and A. Behnke, “A molecular approach to identify active microbes in environmental eukaryote clone libraries,” Microbial Ecology, vol. 53, no. 2, pp. 328–339, 2007.
[63]  F. Not, J. del Campo, V. Balagué, C. de Vargas, and R. Massana, “New insights into the diversity of marine picoeukaryotes,” PLoS ONE, vol. 4, no. 9, Article ID e7143, 2009.
[64]  T. Stoeck, B. Hayward, G. T. Taylor, R. Varela, and S. S. Epstein, “A multiple PCR-primer approach to access the microeukaryotic diversity in environmental samples,” Protist, vol. 157, no. 1, pp. 31–43, 2006.
[65]  A. Jumpponen, “Soil fungal communities underneath willow canopies on a primary successional glacier forefront: rDNA sequence results can be affected by primer selection and chimeric data,” Microbial Ecology, vol. 53, no. 2, pp. 233–246, 2007.
[66]  A. Engelbrektson, V. Kunin, K. C. Wrighton et al., “Experimental factors affecting PCR-based estimates of microbial species richness and evenness,” ISME Journal, vol. 4, no. 5, pp. 642–647, 2010.
[67]  S. Filker, A. Stock, H.-W. Breiner et al., “Environmental selection of protistan plankton communities in hypersaline anoxic deep-sea basins, Eastern Mediterranean Sea,” MicrobiologyOpen, vol. 2, no. 1, pp. 54–63, 2013.
[68]  A. Stock, V. Edgcomb, W. Orsi et al., “Evidence for isolated evolution of deep-sea ciliate communities through geological separation and environmental selection,” BMC Microbiology, vol. 13, article 150, 2013.
[69]  A. Behnke, K. J. Barger, J. Bunge, and T. Stoeck, “Spatio-temporal variations in protistan communities along an O2/H2S gradient in the anoxic Framvaren Fjord (Norway),” FEMS Microbiology Ecology, vol. 72, no. 1, pp. 89–102, 2010.
[70]  V. Edgcomb, W. Orsi, J. Bunge et al., “Protistan microbial observatory in the Cariaco Basin, Caribbean. I. Pyrosequencing vs Sanger insights into species richness,” ISME Journal, vol. 5, no. 8, pp. 1344–1356, 2011.
[71]  W. Orsi, V. Edgcomb, S. Jeon et al., “Protistan microbial observatory in the Cariaco Basin, Caribbean. II. Habitat specialization,” ISME Journal, vol. 5, no. 8, pp. 1357–1373, 2011.
[72]  C. E. Lee and M. A. Bell, “Causes and consequences of recent freshwater invasions by saltwater animals,” Trends in Ecology and Evolution, vol. 14, no. 7, pp. 284–288, 1999.
[73]  E. O. Casamayor, X. Triado-Margarit, and C. Castaneda, “Microbial biodiversity in saline shallow lakes of the Monegros Desert, Spain,” FEMS Microbiology Ecology, vol. 85, no. 3, pp. 503–518, 2013.
[74]  A. Oren, “The bioenergetic basis for the decrease in metabolic diversity at increasing salt concentrations: implications for the functioning of salt lake ecosystems,” Hydrobiologia, vol. 466, pp. 61–72, 2001.
[75]  A. Oren, Halophilic Microorganisms and Their Environments, vol. 5, Kluwer Academic, Dordrecht, The Netherlands, 2002.
[76]  T. Stoeck, G. T. Taylor, and S. S. Epstein, “Novel eukaryotes from the permanently anoxic Cariaco Basin (Caribbean Sea),” Applied and Environmental Microbiology, vol. 69, no. 9, pp. 5656–5663, 2003.
[77]  W. Orsi, Y. C. Song, S. Hallam, and V. Edgcomb, “Effect of oxygen minimum zone formation on communities of marine protists,” ISME Journal, vol. 6, no. 8, pp. 1586–1601, 2012.
[78]  M. Müller, M. Mentel, J. J. van Hellemond et al., “Biochemistry and evolution of anaerobic energy metabolism in eukaryotes,” MicroBiology and Molecular Biology Reviews, vol. 76, no. 2, pp. 444–495, 2012.
[79]  J. E. Hallsworth, M. M. Yakimov, P. N. Golyshin et al., “Limits of life in MgCl2-containing environments: chaotropicity defines the window,” Environmental Microbiology, vol. 9, no. 3, pp. 801–813, 2007.
[80]  H. J. Kunte, H. Trüper, and H. Stan-Lotter, “Halophilic microorganisms,” in Astrobiology the Quest for the Conditions of Life, G. Horneck and C. Baumstark-Khan, Eds., pp. 185–200, Springer, Berlin, Germany, 2002.
[81]  B. W. Catlin and L. S. Cunningham, “Studies of extracellular and intracellular bacterial deoxyribonucleic acids,” Journal of General Microbiology, vol. 19, no. 3, pp. 522–539, 1958.
[82]  S. Borin, E. Crotti, F. Mapelli, I. Tamagnini, C. Corselli, and D. Daffonchio, “DNA is preserved and maintains transforming potential after contact with brines of the deep anoxic hypersaline lakes of the Eastern Mediterranean Sea,” Saline Systems, vol. 4, no. 1, article 10, 2008.
[83]  R. Amann, B. M. Fuchs, and S. Behrens, “The identification of microorganisms by fluorescence in situ hybridisation,” Current Opinion in Biotechnology, vol. 12, no. 3, pp. 231–236, 2001.
[84]  W. Ludwig, O. Strunk, R. Westram et al., “ARB: a software environment for sequence data,” Nucleic Acids Research, vol. 32, no. 4, pp. 1363–1371, 2004.
[85]  J. Pernthaler, F. O. Gl?ckner, W. Sch?nhuber, and R. Amann, “Fluorescence in situ hybridization (FISH) with rRNA-targeted oligonucleotide probes,” in Methods in Microbiology, J. H. Paul, Ed., vol. 30, pp. 207–226, Academic Press, San Diego, Calif, USA, 2001.
[86]  A. G. B. Simpson, J. Luke?, and A. J. Roger, “The evolutionary history of kinetoplastids and their kinetoplasts,” Molecular Biology and Evolution, vol. 19, no. 12, pp. 2071–2083, 2002.
[87]  S. von der Heyden, E. E. Chao, K. Vickerman, and T. Cavalier-Smith, “Ribosomal RNA phylogeny of bodonid and diplonemid flagellates and the evolution of euglenozoa,” Journal of Eukaryotic Microbiology, vol. 51, no. 4, pp. 402–416, 2004.
[88]  W. Orsi, V. Edgcomb, J. Faria et al., “Class Cariacotrichea, a novel ciliate taxon from the anoxic Cariaco Basin, Venezuela,” International Journal of Systematic and Evolutionary Microbiology, vol. 62, part 6, pp. 1425–1433, 2012.
[89]  W. Orsi, S. Charvet, P. Vd'a?ny, J. M. Bernhard, and V. P. Edgcomb, “Prevalence of partnerships between bacteria and ciliates in oxygen-depleted marine water columns,” Frontiers in Microbiology, vol. 3, article 341, 2012.
[90]  S. Filker, M. Kaiser, R. Rosseló-Móra, M. Dunthorn, G. Lax, and T. Stoeck, ““Candidatus Haloectosymbiotes riaformosensis” (Halobacteriaceae), an archaeal ectosymbiont of the hypersaline ciliate Platynematum salinarum,” Systematic and Applied Microbiology, 2014.
[91]  W. Foissner, J.-H. Jung, S. Filker, J. Rudolph, and T. Stoeck, “Morphology, ontogenesis and molecular phylogeny of Platynematum salinarum nov. spec., a new scuticociliate (Ciliophora, Scuticociliatia) from a solar saltern,” European Journal of Protistology, vol. 50, no. 2, pp. 174–184, 2013.
[92]  A. Antunes, D. K. Ngugi, and U. Stingl, “Microbiology of the Red Sea (and other) deep-sea anoxic brine lakes,” Environmental Microbiology Reports, vol. 3, no. 4, pp. 416–433, 2011.
[93]  R. F. Shokes, P. K. Trabant, B. J. Presley, and D. F. Reid, “Anoxic, hypersaline basin in the northern Gulf of Mexico,” Science, vol. 196, no. 4297, pp. 1443–1446, 1977.
[94]  B. J. Finlay, “Global dispersal of free-living microbial eukaryote species,” Science, vol. 296, no. 5570, pp. 1061–1063, 2002.
[95]  J. G. Caporaso, J. Kuczynski, J. Stombaugh et al., “QIIME allows analysis of high-throughput community sequencing data,” Nature Methods, vol. 7, no. 5, pp. 335–336, 2010.
[96]  M. S. Cline, M. Smoot, E. Cerami et al., “Integration of biological networks and gene expression data using Cytoscape,” Nature protocols, vol. 2, no. 10, pp. 2366–2382, 2007.
[97]  M. E. Nebel, S. Wild, M. Holzhauser et al., “Jaguc-a software package for environmental diversity analyses,” Journal of Bioinformatics and Computational Biology, vol. 9, no. 6, pp. 749–773, 2011.

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