期刊论文详细信息
BMC Microbiology
Evidence for isolated evolution of deep-sea ciliate communities through geological separation and environmental selection
Thorsten Stoeck1  Michail M Yakimov2  Hans-Werner Breiner1  Sabine Filker1  William Orsi3  Virginia Edgcomb3  Alexandra Stock1 
[1] University of Kaiserslautern, School of Biology, Erwin-Schroedinger-Str. 14, D-67663 Kaiserslautern, Germany;Institute for Coastal Marine Environment, IAMC-CNR, Spianata S. Raineri, 86, 98122 Messina, Italy;Department of Geology and Geophysics, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA
关键词: Niche separation;    Environmental filtering;    Species sorting;    Brine;    DHABs;    Deep-sea anoxic basins;    Hypersaline;    Ciliates;   
Others  :  1143564
DOI  :  10.1186/1471-2180-13-150
 received in 2012-11-27, accepted in 2013-05-15,  发布年份 2013
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【 摘 要 】

Background

Deep hypersaline anoxic basins (DHABs) are isolated habitats at the bottom of the eastern Mediterranean Sea, which originate from the ancient dissolution of Messinian evaporites. The different basins have recruited their original biota from the same source, but their geological evolution eventually constituted sharp environmental barriers, restricting genetic exchange between the individual basins. Therefore, DHABs are unique model systems to assess the effect of geological events and environmental conditions on the evolution and diversification of protistan plankton. Here, we examine evidence for isolated evolution of unicellular eukaryote protistan plankton communities driven by geological separation and environmental selection. We specifically focused on ciliated protists as a major component of protistan DHAB plankton by pyrosequencing the hypervariable V4 fragment of the small subunit ribosomal RNA. Geospatial distributions and responses of marine ciliates to differential hydrochemistries suggest strong physical and chemical barriers to dispersal that influence the evolution of this plankton group.

Results

Ciliate communities in the brines of four investigated DHABs are distinctively different from ciliate communities in the interfaces (haloclines) immediately above the brines. While the interface ciliate communities from different sites are relatively similar to each other, the brine ciliate communities are significantly different between sites. We found no distance-decay relationship, and canonical correspondence analyses identified oxygen and sodium as most important hydrochemical parameters explaining the partitioning of diversity between interface and brine ciliate communities. However, none of the analyzed hydrochemical parameters explained the significant differences between brine ciliate communities in different basins.

Conclusions

Our data indicate a frequent genetic exchange in the deep-sea water above the brines. The “isolated island character” of the different brines, that resulted from geological events and contemporary environmental conditions, create selective pressures driving evolutionary processes, and with time, lead to speciation and shape protistan community composition. We conclude that community assembly in DHABs is a mixture of isolated evolution (as evidenced by small changes in V4 primary structure in some taxa) and species sorting (as indicated by the regional absence/presence of individual taxon groups on high levels in taxonomic hierarchy).

【 授权许可】

   
2013 Stock et al.; licensee BioMed Central Ltd.

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【 参考文献 】
  • [1]Ovreas L, Curtis TP: Microbial diversity and ecology. In Biological Diversity: frontiers in measurement and assessment. Edited by Magurran AE, McGill BJ. Oxford: Oxford University Press; 2011:221-236.
  • [2]Alexander E, Stock A, Breiner HW, Behnke A, Bunge J, Yakimov MM, Stoeck T: Microbial eukaryotes in the hypersaline anoxic L'Atalante deep-sea basin. Environ Microbiol 2009, 11:360-381.
  • [3]Edgcomb V, Orsi W, Leslin C, Epstein S, Bunge J, Jeon SO, Yakimov MM, Behnke A, Stoeck T: Protistan community patterns within the brine and halocline of deep hypersaline anoxic basins in the eastern Mediterranean Sea. Extremophiles 2009, 13:151-167.
  • [4]Camerlenghi A: Anoxic basins of the eastern Mediterranean: geological framework. Mar Chem 1990, 31:1-19.
  • [5]La Cono V, Smedile F, Bortoluzzi G, Arcadi E, Maimone G, Messina E, Borghini M, Oliveri E, Mazzola S, L'Haridon S, et al.: Unveiling microbial life in new deep-sea hypersaline Lake Thetis. Part I: Prokaryotes and environmental settings. Environ Microbiol 2011, 13(8):2250-2268.
  • [6]van der Wielen PW, Bolhuis H, Borin S, Daffonchio D, Corselli C, Giuliano L, D'Auria G, de Lange GJ, Huebner A, Varnavas SP, et al.: The enigma of prokaryotic life in deep hypersaline anoxic basins. Science 2005, 307(5706):121-123.
  • [7]Azam F, Fenchel T, Field J, Gray J, Meyer-Reil L, Thingstad F: The ecological role of water column microbes in the sea. Mar Ecol Prog Ser 1983, 10:257-263.
  • [8]Corliss JO: Biodiversity and biocomplexity of the protists and an overview of their significant roles in maintenance of our biosphere. Acta Protozool 2002, 41(3):199-220.
  • [9]Finlay BJ, Corliss JO, Esteban G, Fenchel T: Biodiversity at the microbial level: the number of free-living ciliates in the biosphere. Ouart Rev Biol 1996, 71:221-237.
  • [10]Lynn DH, Gilron GL: A brief review of approaches using ciliated protists to assess aquatic ecosystem health. J Aquatic Ecosyst Health 1992, 1:263-270.
  • [11]Doherty M, Cosatas BA, McManus GB, Katz LA: Culture independent assessment of planktonic ciliate diversity in coastal northwest Atlantic waters. Aquat Microb Ecol 2007, 48:141-154.
  • [12]Fenchel T, Finlay BJ: The diversity of microbes: resurgence of the phenotype. Phil Trans Roy Soc Lond B Biol Sci 2006, 361(1475):1965-1973.
  • [13]Finlay BJ: Global dispersal of free-living microbial eukaryote species. Science 2002, 296(5570):1061-1063.
  • [14]Foissner W, Chao A, Katz LA: Diversity and geographic distribution of ciliates (Protista: Ciliophora). Biodiv Conserv 2008, 17:345-363.
  • [15]Katz LA, McManus GB, Snoeyenbos-West OLO, Pirog K, Griffin A, Foissner W: Reframing the Microbial 'Everything is Everywhere' Debate: evidence for high gene flow and diversity in ciliate morphospecies. Aquat Microb Ecol 2005, 41:55-65.
  • [16]Stoeck T, Bass D, Nebel M, Christen R, Jones MD, Breiner HW, Richards TA: Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. Mol Ecol 2010, 19:21-31.
  • [17]Weisse T: Distribution and diversity of aquatic protists: an evolutionary and ecological perspective. Biodiv Conserv 2008, 17:243-259.
  • [18]Dunthorn M, Foissner W, Katz LA: Molecular phylogenetic analysis of class Colpodea (phylum Ciliophora) using broad taxon sampling. Mol Phylogenet Evol 2008, 46(1):316-327.
  • [19]Lynn DH: The Ciliated Protozoa. Third edition. New York: Springer; 2008.
  • [20]Christen R: Global sequencing: a review of current molecular data and new methods available to assess microbial diversity. Microb Environ 2008, 23(4):253-268.
  • [21]Epstein S, Lopez-Garcia P: “Missing” protists: a molecular prospective. Biodivers Conserv 2008, online early(17):261-276.
  • [22]Jeon S, Bunge J, Leslin C, Stoeck T, Hong S, Epstein SS: Environmental rRNA inventories miss over half of protistan diversity. BMC Microbiol 2008, 8:222. BioMed Central Full Text
  • [23]Moreira D, Lopez-Garcia P: The molecular ecology of microbial eukaryotes unveils a hidden world. Trends Microbiol 2002, 10(1):31-38.
  • [24]Pedros-Alio C: Ecology. Dipping into the rare biosphere. Science 2007, 315(5809):192-193.
  • [25]Orsi WD, Charvet S, Vdacny P, Bernhard JM, Edgcomb VP: Prevalence of partnerships between bacteria and ciliates in oxygen-depleted marine water columns. Front Microbiol 2012, 3:341.
  • [26]Yetinson T, Shilo M: Seasonal and geographic distribution of luminous bacteria in the eastern mediterranean sea and the gulf of elat. Appl Environ Microbiol 1979, 37(6):1230-1238.
  • [27]Inagaki F, Nunoura T, Nakagawa S, Teske A, Lever M, Lauer A, Suzuki M, Takai K, Delwiche M, Colwell FS, et al.: Biogeographical distribution and diversity of microbes in methane hydrate-bearing deep marine sediments on the Pacific Ocean Margin. Proc Natl Acad Sci U S A 2006, 103(8):2815-2820.
  • [28]Whitaker RJ, Grogan DW, Taylor JW: Geographic barriers isolate endemic populations of hyperthermophilic archaea. Science 2003, 301(5635):976-978.
  • [29]Jones EBG, Pang KL: Tropical aquatic fungi. Biodiv Conserv 2012, 21:2403-2423.
  • [30]Dolan JR: An introduction to the biogeography of aquatic microbes. Aquat Microb Ecol 2005, 41(1):39-48.
  • [31]Martiny JBH, Bohannan BJM, Brown JH, Colwell RK, Fuhrman JA, Green JL, Horner-Devine MC, Kane M, Krumins JA, Kuske CR, et al.: Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 2006, 4(2):102-112.
  • [32]Vyverman W, Verleyen E, Sabbe K, Vanhoutte K, Sterken M, Hodgson DA, Mann DG, Juggins S, Van de Vijver B, Jones V, et al.: Historical processes constrain patterns in global diatom diversity. Ecology 2007, 88(8):1924-1931.
  • [33]Fenchel T, Esteban GF, Finlay BJ: Local versus global diversity of microorganisms: cryptic diversity of ciliated protozoa. Oikos 1997, 80(2):220-225.
  • [34]Stephenson SL, Schnittler M, Novozhilov YK: Myxomycete diversity and distribution from the fossil record to the present. Biodivers Conserv 2008, 17(2):285-301.
  • [35]Wilson DS: Complex interactions in metacommunities, with implications for biodiversity and higher levels of selection. Ecology 1992, 73:1984-2000.
  • [36]Leibold MA, Holyoak M, Moquet N, Amarasekare P, Chase JM, Hoopes MF, Holt RD, Shurin JB, Law R, Tilman D, Loreau M, Gonzalez A: The metacommunity concept: a framework for multi-scale community ecology. Ecol Lett 2004, 7:601-613.
  • [37]Holyoak M, Leibold MA, Holt RD: Metacommunities: Spatial Dynamics and Ecological Communities. Chicago, IL, USA: The University of Chicago Press; 2005.
  • [38]Santangelo G, Lucchesi P: Spatial distribution pattern of ciliated protozoa in a Mediterranean interstitial environment. Aquat Microb Ecol 1995, 9:47-54.
  • [39]Albuquerque L, Taborda M, La Cono V, Yakimov M, da Costa MS: Natrinema salaciae sp. nov., a halophilic archaeon isolated from the deep, hypersaline anoxic Lake Medee in the Eastern Mediterranean Sea. Syst Appl Microbiol 2012, 35(6):368-373.
  • [40]Forster D, Behnke A, Stoeck T: Meta-analyses of environmental sequence data identify anoxia and salinity as parameters shaping ciliate communities. Systematics and Biodiversity 2012, 10(3):277-288.
  • [41]Lozupone CA, Knight R: Global patterns in bacterial diversity. Proc Natl Acad Sci U S A 2007, 104(27):11436-11440.
  • [42]Logares R, Lindstrom ES, Langenheder S, Logue JB, Paterson H, Laybourn-Parry J, Rengefors K, Tranvik L, Bertilsson S: Biogeography of bacterial communities exposed to progressive long-term environmental change. ISME J 2013, 7(5):937-948.
  • [43]Logares R, Brate J, Bertilsson S, Clasen JL, Shalchian-Tabrizi K, Rengefors K: Infrequent marine-freshwater transitions in the microbial world. Trends Microbiol 2009, 17(9):414-422.
  • [44]Oren A, Larimer F, Richardson P, Lapidus A, Csonka LN: How to be moderately halophilic with broad salt tolerance: clues from the genome of Chromohalobacter salexigens. Extremophiles 2005, 9(4):275-279.
  • [45]Ramos-Cormenzana A: Halophilic organisms and their environment. In General and Applied Aspects of Halophilic Microorganisms. Edited by Rodriguez-Valera F. New York: Plenum Press; 1991:15-24.
  • [46]Pedros-Alio C, Calderon-Paz JI, MacLean MH, Medina G, Marrase C, Gasol JM, Guixa-Boixereu N: The microbial food web along salinity gradients. FEMS Microbiol Ecol 2000, 32(2):143-155.
  • [47]Koch TA, Ekelund F: Strains of the heterotrophic flagellate Bodo designis from different environments vary considerably with respect to salinity preference and SSU rRNA gene composition. Protist 2005, 156(1):97-112.
  • [48]Finlay BJ, Esteban GF, Brown S, Fenchel T, Hoef-Emden K: Multiple cosmopolitan ecotypes within a microbial eukaryote morphospecies. Protist 2006, 157(4):377-390.
  • [49]Embley TM, Finlay BJ, Dyal PL, Hirt RP, Wilkinson M, Williams AG: Multiple Origins of Anaerobic Ciliates with Hydrogenosomes within the Radiation of Aerobic Ciliates. Phil Trans Roy Soc Lond B Biol Sci 1995, 262(1363):87-93.
  • [50]Hjort K, Goldberg AV, Tsaousis AD, Hirt RP, Embley TM: Diversity and reductive evolution of mitochondria among microbial eukaryotes. Phil Trans Roy Soc Lond B Biol Sci 2010, 365(1541):713-727.
  • [51]Boxma B, de Graaf RM, van der Staay GWM, van Alen TA, Ricard G, Gabaldon T, van Hoek AHAM, der Staay SY M-v, Koopman WJH, van Hellemond JJ, et al.: An anaerobic mitochondrion that produces hydrogen. Nature 2005, 434(7029):74-79.
  • [52]Fenchel T, Perry T, Thane A: Anaerobiosis and symbiosis with bacteria in free-living ciliates. J Eukaryot Microbiol 1977, 24:154-163.
  • [53]van Hoek AH, van Alen TA, Sprakel VS, Leunissen JA, Brigge T, Vogels GD, Hackstein JH: Multiple acquisition of methanogenic archaeal symbionts by anaerobic ciliates. Mol Biol Evol 2000, 17(2):251-258.
  • [54]Edgcomb V, Orsi W, Breiner HW, Stock A, Filker S, Yakimov MM, Stoeck T: Novel active kinetoplastids associated with hypersaline anoxic basins in the Eastern Mediterranean deep-sea. Deep-Sea Res I 2011, 58:1040-1048.
  • [55]Stoeck T, Taylor GT, Epstein SS: Novel eukaryotes from the permanently anoxic Cariaco Basin (Caribbean Sea). Appl Environ Microbiol 2003, 69(9):5656-5663.
  • [56]Behnke A, Bunge J, Barger K, Breiner HW, Alla V, Stoeck T: Microeukaryote community patterns along an O2/H2S gradient in a supersulfidic anoxic Fjord (Framvaren, Norway). Appl Environ Microbiol 2006, 72(5):3626-3636.
  • [57]Zuendorf A, Behnke A, Bunge J, Barger K, Stoeck T: Diversity estimates of microeukaryotes below the chemocline of the anoxic Mariager Fjord, Denmark. FEMS Microbiol Ecol 2006, 58:476-491.
  • [58]Stock A, Jurgens K, Bunge J, Stoeck T: Protistan diversity in suboxic and anoxic waters of the Gotland Deep (Baltic Sea) as revealed by 18S rRNA clone libraries. Aquat Microb Ecol 2009, 55(3):267-284.
  • [59]Wylezich C, Jurgens K: Protist diversity in suboxic and sulfidic waters of the Black Sea. Environ Microbiol 2011, 13(11):2939-2956.
  • [60]Casamayor EO, Garcia-Cantizano J, Pedros-Alio C: Carbon dioxide fixation in the dark by photosynthetic bacteria in sulfide-rich stratified lakes with oxic-anoxic interfaces. Limnol Oceanogr 2008, 53(4):1193-1203.
  • [61]Oren A: Thermodynamic limits to microbial life at high salt concentrations. Environ Microbiol 2011, 13(8):1908-1923.
  • [62]Rengefors K, Logares R, Laybourn-Parry J: Polar lakes may act as ecological islands to aquatic protists. Mol Ecol 2012, 21(13):3200-3209.
  • [63]Pernthaler J: Predation on prokaryotes in the water column and its ecological implications. Nat Rev Microbiol 2005, 3(7):537-546.
  • [64]Yoon HS, Price DC, Stepanauskas R, Rajah VD, Sieracki ME, Wilson WH, Yang EC, Duffy S, Bhattacharya D: Single-cell genomics reveals organismal interactions in uncultivated marine protists. Science 2011, 332(6030):714-717.
  • [65]Coolen MJ: 7000 years of Emiliania huxleyi viruses in the Black Sea. Science 2011, 333(6041):451-452.
  • [66]Miki T, Jacquet S: Complex interactions in the microbial world: underexplored key links between viruses, bacteria and protozoan grazers in aquatic environments. Aquat Microb Ecol 2008, 51(2):195-208.
  • [67]Verity PG: Feeding in planktonic protozoans, evidence for non-random acquisition of prey. J Protozool 1991, 38:69-76.
  • [68]Yakimov MM, Giuliano L, Cappello S, Denaro R, Golyshin PN: Microbial community of a hydrothermal mud vent underneath the deep-sea anoxic brine lake Urania (eastern Mediterranean). Orig Life Evol Biosph 2007, 37(2):177-188.
  • [69]Yakimov MM, La Cono V, Denaro R, D'Auria G, Decembrini F, Timmis KN, Golyshin PN, Giuliano L: Primary producing prokaryotic communities of brine, interface and seawater above the halocline of deep anoxic lake L'Atalante, Eastern Mediterranean Sea. ISME J 2007, 1(8):743-755.
  • [70]Beardsley C, Pernthaler J, Wosniok W, Amann R: Are Readily Culturable Bacteria in Coastal North Sea Waters Suppressed by Selective Grazing Mortality? Appl Environ Microbiol 2003, 69(5):2624-2630.
  • [71]Matz C, Boenigk J, Arndt H, Jurgens K: Role of bacterial phenotypic traits in selective feeding of the heterotrophic nanoflagellate Spumella sp. Aquat Microb Ecol 2002, 27(2):137-148.
  • [72]Gonzalez JM, Sherr EB, Sherr BF: Size-Selective Grazing on Bacteria by Natural Assemblages of Estuarine Flagellates and Ciliates. Appl Environ Microbiol 1990, 56(3):583-589.
  • [73]Simek K, Vrba J, Hartman P: Size-Selective Feeding by Cyclidium Sp on Bacterioplankton and Various Sizes of Cultured Bacteria. FEMS Microbiol Ecol 1994, 14(2):157-167.
  • [74]James JW: The founder effect and response to artificial selection. Genet Res 1970, 16(3):241-250.
  • [75]Masel J: Genetic drift. Curr Biol 2011, 21(20):R837-R838.
  • [76]Fisher RA: The genetical theory of natural selection. Oxford: The Clarendon Press; 1930.
  • [77]De Meester L, Gómez A, Okamura B, Schwenk K: The Monopolization Hypothesis and the dispersal–gene flow paradox in aquatic organisms. Acta Oecol 2002, 23:121-135.
  • [78]Urban MC, Leibold MA, Amarasekare P, De Meester L, Gomulkiewicz R, Hochberg ME, Klausmeier CA, Loeuille N, de Mazancourt C, Norberg J, et al.: The evolutionary ecology of metacommunities. Trends Ecol Evol 2008, 23(6):311-317.
  • [79]Brate J, Logares R, Berney C, Ree DK, Klaveness D, Jakobsen KS, Shalchian-Tabrizi K: Freshwater Perkinsea and marine-freshwater colonizations revealed by pyrosequencing and phylogeny of environmental rDNA. ISME J 2010, 4(9):1144-1153.
  • [80]Foissner W: Biogeography and dispersal of micro-organisms: A review emphasizing protists. Acta Protozool 2006, 45(2):111-136.
  • [81]Garcia-Castellanos D, Estrada F, Jimenez-Munt I, Gorini C, Fernandez M, Verges J, De Vicente R: Catastrophic flood of the Mediterranean after the Messinian salinity crisis. Nature 2009, 462(7274):778-U796.
  • [82]Whittaker RH: Classification of natural communities. Bot Rev 1962, 28:1-239.
  • [83]Lebrija-Trejos E, Perez-Garcia EA, Meave JA, Bongers F, Poorter L: Functional traits and environmental filtering drive community assembly in a species-rich tropical system. Ecology 2010, 91(2):386-398.
  • [84]Humphreys WF, Watts CHS, Cooper SJB, Leijs R: Groundwater estuaries of salt lakes: buried pools of endemic biodiversity on the western plateau, Australia (vol 626, pg 79, 2009). Hydrobiologia 2009, 632(1):377.
  • [85]Juan C, Guzik MT, Jaume D, Cooper SJ: Evolution in caves: Darwin's 'wrecks of ancient life' in the molecular era. Mol Ecol 2010, 19(18):3865-3880.
  • [86]Leijs R, van Nes EH, Watts CH, Cooper SJB, Humphreys WF, Hogendoorn K: Evolution of Blind Beetles in Isolated Aquifers: a Test of Alternative Modes of Speciation. PLoS One 2012, 7(3):e34260.
  • [87]Leys R, Watts CH, Cooper SJ, Humphreys WF: Evolution of subterranean diving beetles (Coleoptera: Dytiscidae: Hydroporini, Bidessini) in the arid zone of Australia. Evolution 2003, 57(12):2819-2834.
  • [88]Degens ET, Ross AT: Hot Brines and Recent Heavy Metal Deposits in the Red Sea. A Geochemical and Geophysical Account. Berlin/Heidelberg/New York: Springer; 1969.
  • [89]Shokes RF, Trabant PK, Presley BJ, Reid DF: Anoxic, hypersaline basin in the northern gulf of Mexico. Science 1977, 196(4297):1443-1446.
  • [90]Nebel ME, Wild S, Holzhauser M, Huttenberger L, Reitzig R, Sperber M, Stoeck T: JAGUC–a software package for environmental diversity analyses. J Bioinform Comput Biol 2011, 9(6):749-773.
  • [91]Behnke A, Engel M, Christen R, Nebel M, Klein RR, Stoeck T: Depicting more accurate pictures of protistan community complexity using pyrosequencing of hypervariable SSU rRNA gene regions. Environ Microbiol 2011, 13(2):340-349.
  • [92]Dunthorn M, Klier J, Bunge J, Stoeck T: Comparing the Hyper-Variable V4 and V9 Regions of the Small Subunit rDNA for Assessment of Ciliate Environmental Diversity. J Eukaryot Microbiol 2012, 59(2):185-187.
  • [93]Kunin V, Engelbrektson A, Ochman H, Hugenholtz P: Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environ Microbiol 2010, 12(1):118-123.
  • [94]Whittaker RH: Evolution and measurements of species diversity. Taxon 1972, 21:213-251.
  • [95]Team RC: R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2012. http://www.R-project.org/ webcite
  • [96]Shannon CE: A mathematical theory of communication. The Bell System Technical Journal 1948, 27:379-423. 623–656
  • [97]Chao A, Lee SM, Jeng SL: Estimating population size for capture-recapture data when capture probabilities vary by time and individual animal. Biometrics 1992, 48(1):201-216.
  • [98]Colwell RK: EstimateS: Statistical estimation of species richness and shared species from samples. Version 8.2. User's Guide and application. 2009. http://viceroy.eeb.uconn.edu/estimates webcite
  • [99]Bray RJ, Curtis JT: An ordination of the upland forest communities of southern Wisconsin. Ecol Monogr 1957, 27:325-349.
  • [100]Magurran AE: Measuring biological diversity. Oxford: Blackwell Publishing; 2004.
  • [101]Sinnott RW: Virtues of the Haversine. Sky Telescope 1984, 68:1-159.
  • [102]Grant A, Ogilvie LA: Terminal restriction fragment length polymorphism data analysis. Appl Environ Microbiol 2003, 69(10):6342. author reply 6342–6343
  • [103]Edgcomb V, Leadbeater ER, Bourland W, Beaudoin D, Bernhard JM: Structured multiple endosymbiosis of bacteria and archaea in a ciliate from marine sediments: a survival mechanism in low oxygen, sulfidic sediments? Front Microb Physiol Metabol 2011, 2:55.
  • [104]Stoeck T, Fowle WH, Epstein SS: Methodology of protistan discovery: from rRNA detection to quality scanning electron microscope images. Appl Environ Microbiol 2003, 69(11):6856-6863.
  • [105]Lara E, Berney C, Harms H, Chatzinotas A: Cultivation-independent analysis reveals a shift in ciliate 18S rRNA gene diversity in a polycyclic aromatic hydrocarbon-polluted soil. FEMS Microbiol Ecol 2007, 62(3):365-373.
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