Microbial Ecology

, Volume 62, Issue 4, pp 824–837 | Cite as

Taxonomic and Functional Metagenomic Profiling of the Microbial Community in the Anoxic Sediment of a Sub-saline Shallow Lake (Laguna de Carrizo, Central Spain)

  • Manuel FerrerEmail author
  • María-Eugenia Guazzaroni
  • Michael Richter
  • Adela García-Salamanca
  • Pablo Yarza
  • Ana Suárez-Suárez
  • Jennifer Solano
  • María Alcaide
  • Pieter van Dillewijn
  • Maria Antonia Molina-Henares
  • Nieves López-Cortés
  • Yamal Al-Ramahi
  • Carmen Guerrero
  • Alejandro Acosta
  • Laura I. de Eugenio
  • Virginia Martínez
  • Silvia Marques
  • Fernando Rojo
  • Eduardo Santero
  • Olga Genilloud
  • Julian Pérez-Pérez
  • Ramón Rosselló-Móra
  • Juan Luis Ramos
Environmental Microbiology


The phylogenetic and functional structure of the microbial community residing in a Ca2+-rich anoxic sediment of a sub-saline shallow lake (Laguna de Carrizo, initially operated as a gypsum (CaSO4 × 2 H2O) mine) was estimated by analyzing the diversity of 16S rRNA amplicons and a 3.1 Mb of consensus metagenome sequence. The lake has about half the salinity of seawater and possesses an unusual relative concentration of ions, with Ca2+ and SO 4 2- being dominant. The 16S rRNA sequences revealed a diverse community with about 22% of the bacterial rRNAs being less than 94.5% similar to any rRNA currently deposited in GenBank. In addition to this, about 79% of the archaeal rRNA genes were mostly related to uncultured Euryarchaeota of the CCA47 group, which are often associated with marine and oxygen-depleted sites. Sequence analysis of assembled genes revealed that 23% of the open reading frames of the metagenome library had no hits in the database. Among annotated genes, functions related to (thio) sulfate and (thio) sulfonate-reduction and iron-oxidation, sulfur-oxidation, denitrification, synthrophism, and phototrophic sulfur metabolism were found as predominant. Phylogenetic and biochemical analyses indicate that the inherent physical–chemical characteristics of this habitat coupled with adaptation to anthropogenic activities have resulted in a highly efficient community for the assimilation of polysulfides, sulfoxides, and organosulfonates together with nitro-, nitrile-, and cyanide-substituted compounds. We discuss that the relevant microbial composition and metabolic capacities at Laguna de Carrizo, likely developed as an adaptation to thrive in the presence of moderate salinity conditions and potential toxic bio-molecules, in contrast with the properties of previously known anoxic sediments of shallow lakes.


Electronic Supplementary Material Polysulfide Archaeal Community Anoxic Sediment Epsilonproteobacteria 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This research was supported by the Spanish CSD2007-00005 project and FEDER funds. M-E.G. thanks the CSIC for a JAE fellowship. We also thank Prof. Michail M. Yakimov and Dr. Terence J McGenity for assistance in diversity and adaptation analyses.

Supplementary material

248_2011_9903_MOESM1_ESM.pdf (6.8 mb)
ESM 1 (PDF 6927 kb)


  1. 1.
    Baati H, Guermazi S, Amdouni R, Gharsallah N, Sghir A, Ammar E (2008) Prokaryotic diversity of a Tunisian multipond solar saltern. Extremophiles 12:505–518CrossRefPubMedGoogle Scholar
  2. 2.
    Baati H, Guermazi S, Gharsallah N, Sghir A, Ammar E (2010) Novel prokaryotic diversity in sediments of Tunisian multipond solar saltern. Res Microbiol 161:573–582CrossRefPubMedGoogle Scholar
  3. 3.
    Bairoch A, Boeckmann B, Ferro S, Gasteiger E (2004) Swiss-Prot: juggling between evolution and stability. Brief Bioinform 5:39–55CrossRefPubMedGoogle Scholar
  4. 4.
    Bodaker I, Sharon I, Suzuki MT, Feingersch R, Shmoish M, Andreishcheva E, Sogin ML, Rosenberg M, Maguire ME, Belkin S, Oren A, Béjà O (2010) Comparative community genomics in the Dead Sea: an increasingly extreme environment. ISME J 4:399–407CrossRefPubMedGoogle Scholar
  5. 5.
    Briée C, Moreira D, López-García P (2007) Archaeal and bacterial community composition of sediment and plankton from a suboxic freshwater pond. Res Microbiol 158:213–227CrossRefPubMedGoogle Scholar
  6. 6.
    Cadillo-Quiroz H, Yashiro E, Yavitt JB, Zinder SH (2008) Characterization of the archaeal community in a minerotrophic fen and terminal restriction fragment length polymorphism-directed isolation of a novel hydrogenotrophic methanogen. Appl Environ Microbiol 74:2059–2068CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Coupland K, Johnson DB (2004) Geochemistry and microbiology of an impounded subterranean acidic water body at Mynydd Parys, Anglesey, Wales. Geobiology 2:77–86CrossRefGoogle Scholar
  8. 8.
    Cummings DE, March AW, Bostick B, Spring S, Caccavo F Jr, Fendorf S, Rosenzweig RF (2000) Evidence for microbial Fe(III) reduction in anoxic, mining-impacted lake sediments (Lake Coeur d'Alene, Idaho). Appl Environ Microbiol 66:154–162CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    De Lange GJ, Middelburg JJ, Van der Weijen CH, Catalano G, Luther GW, Hydes DJ, Woittiez JRW, Klinkhammer GP (1990) Composition of anoxic hypersaline brines in the Tyro and Bannock basins, eastern Mediterranean. Marine Chemistry 31:63–88CrossRefGoogle Scholar
  10. 10.
    Debroas D, Humbert J-F, Enault F, Bronner G, Faubladier M, Cornillot E (2009) Metagenomic approach studying the taxonomic and functional diversity of the bacterial community in a mesotrophic lake (Lac du Bourget–France). Environ Microbiol 11:2412–2424CrossRefPubMedGoogle Scholar
  11. 11.
    Donachie SP, Hou S, Lee KS, Riley CW, Pikina A, Belisle C, Kempe S, Gregory TS, Bossuyt A, Boerema J, Liu J, Freitas TA, Malahoff A, Alam M (2004) The Hawaiian Archipelago: a microbial diversity hotspot. Microb Ecol 48:509–520CrossRefPubMedGoogle Scholar
  12. 12.
    Dong H, Zhang G, Jiang H, Yu B, Chapman LR, Lucas CR, Fields MW (2006) Microbial diversity in sediments of saline Qianghai lake, China: linking geochemical controls to microbial ecology. Microb Ecol 51:65–82CrossRefPubMedGoogle Scholar
  13. 13.
    Edwards RA, Rodriguez-Brito B, Wegley L, Haynes M, Breitbart M, Peterson DM, Saar MO, Alexander S, Alexander EC Jr, Rohwer F (2006) Using pyrosequencing to shed light on deep mine microbial ecology. BMC Genomics 7:57CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Engel AS, Porter ML, Stern LA, Quinlan S, Bennett PC (2004) Bacterial diversity and ecosystem function of filamentous microbial mats from aphotic (cave) sulfidic springs dominated by chemolithoautotrophic "Epsilonproteobacteria". FEMS Microbiol Ecol 51:31–53CrossRefPubMedGoogle Scholar
  15. 15.
    Finn RD, Tate J, Mistry J, Coggill PC, Sammut JS, Hotz HR et al (2008) The Pfam protein families database. Nucleic Acids Res Database Issue 36:D281–D288CrossRefGoogle Scholar
  16. 16.
    Fresquet V, Williams L, Raushel FM (2004) Mechanism of cobyrinic acid a, c-diamide synthetase from Salmonella typhimurium LT2. Biochemistry 43:10619–10627CrossRefPubMedGoogle Scholar
  17. 17.
    Glissmann K, Chin K-J, Casper P, Conrad R (2004) Methanogenic pathway and archaeal community structure in the sediment of eutrophic Lake Dagow: effect of temperature. Microb Ecol 48:389–399CrossRefGoogle Scholar
  18. 18.
    Good IJ (1953) The population frequencies of species and the estimation of population parameters. Biometrika 40:237–264CrossRefGoogle Scholar
  19. 19.
    Gough HL, Stahl DA (2011) Microbial community structures in anoxic freshwater lake sediment along a metal contamination gradient. ISME J 5:543–558CrossRefPubMedGoogle Scholar
  20. 20.
    Guazzaroni ME, Golyshin PN, Ferrer M (2010) Molecular methods to study complex microbial communities. In: Marco D (ed) Metagenomics: theory, methods and applications. Caister Academic Press, Norfolk, VA, pp 55–77Google Scholar
  21. 21.
    Haaijer SC, Harhangi HR, Meijerink BB, Strous M, Pol A, Smolders AJ, Verwegen K, Jetten MS, Op den Camp HJ (2008) Bacteria associated with iron seeps in a sulfur-rich, neutral pH, freshwater ecosystem. ISME J 2:1231–1242CrossRefPubMedGoogle Scholar
  22. 22.
    Handley KM, Boothman C, Mills RA, Pancost RD, Lloyd JR (2010) Functional diversity of bacteria in a ferruginous hydrothermal sediment. ISME J 4:1193–1205CrossRefPubMedGoogle Scholar
  23. 23.
    Hankeln W, Buttigieg PL, Fink D, Kottmann R, Yilmaz P, Glöckner FO (2010) MetaBar—a tool for consistent contextual data acquisition and standards compliant submission. BMC Bioinformatics 11:358CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Hirayama H, Takai K, Inagaki F, Yamato Y, Suzuki M, Nealson KH, Horikoshi K (2005) Bacterial community shift along a subsurface geothermal water stream in a Japanese gold mine. Extremophiles 9:169–184CrossRefPubMedGoogle Scholar
  25. 25.
    Hunter S, Apweiler R, Attwood TK, Bairoch A, Bateman A, Binns D et al (2009) InterPro: the integrative protein signature database. Nucleic Acids Res Database Issue 37:D224–D228CrossRefGoogle Scholar
  26. 26.
    Huse SM, Huber JA, Morrison HG, Sogin ML, Weich DM (2007) Accuracy and quality of massively parallel DNA pyrosequencing. Genome Biol 8:R143CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Jahnke LL, Orphan VJ, Embaye T, Turk KA, Kubo MD, Summons RE, des Marais DJ (2008) Lipid biomarker and phylogenetic analyses to reveal archaeal biodiversity and distribution in hypersaline microbial mat and underlying sediment. Geobiology 6:394–410CrossRefPubMedGoogle Scholar
  28. 28.
    Jiang H, Dong H, Zhang G, Yu B, Chapman LR, Fields MW (2006) Microbial diversity in water and sediment of Lake Chaka, an athalassohaline lake in northwestern China. Appl Environ Microbiol 72:3832–3845CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Juretschko S, Loy A, Lehner A, Wagner M (2002) The microbial community composition of a nitrifying-denitrifying activated sludge from an industrial sewage treatment plant analyzed by the full-cycle rRNA approach. Syst Appl Microbiol 25:84–99CrossRefPubMedGoogle Scholar
  30. 30.
    Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M et al (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36:D480–D484CrossRefPubMedGoogle Scholar
  31. 31.
    Kappler U (2008) Bacterial sulfite-oxidazing enzymes—enzymes for chemolithotrophs only? In: Dahl C, Friedrich CG (eds) Microbial sulfur metabolism. Springer-Verlag, Berlin 2008:151Google Scholar
  32. 32.
    Kendall MM, Liu Y, Boone DR (2006) Butyrate- and propionate-degrading syntrophs from permanently cold marine sediments in Skan Bay, Alaska, and description of Algorimarina butyrica gen. nov., sp. nov. FEMS Microbiol Lett 262:107–114CrossRefPubMedGoogle Scholar
  33. 33.
    Kendall MM, Wardlaw GD, Tang CF, Bonin AS, Liu Y, Valentine DL (2007) Diversity of Archaea in marine sediments from Skan Bay, Alaska, including cultivated methanogens, and description of Methanogenium boonei sp. nov. Appl Environ Microbiol 73:407–414CrossRefPubMedGoogle Scholar
  34. 34.
    Kobayashi M, Shimizu S (2000) Nitrile hydrolases. Curr Opin Chem Biol 4:95–102CrossRefPubMedGoogle Scholar
  35. 35.
    Konstantinidis K, DeLong EF (2008) Genomic patterns of recombination, clonal divergence and environment in marine microbial populations. ISME J 2:1052–1065CrossRefPubMedGoogle Scholar
  36. 36.
    Konstantinidis KT, Braff J, Karl DM, DeLong EF (2009) Comparative metagenomic analysis of a microbial community residing at a depth of 4,000 meters at station ALOHA in the North Pacific subtropical gyre. Appl Environ Microbiol 75:5345–5355CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    La Cono V, Smedile F, Bortoluzzi G, Arcadi E, Maimone G, Borghini M, Oliveri E, Mazzola S, L’Haridon S, Genovese L, Ferrer M, Giuliano L, Golyshin PN, Yakimov V (2011) Unveiling microbial life in new deep-sea hypersaline Lake Thetis. Part 1: Prokaryotes and environmental settings. Environ Microbiol. doi: 10.1111/j.1462-2920.2011.02478.x
  38. 38.
    Lau MC, Aitchison JC, Pointing SB (2009) Bacterial community composition in thermophilic microbial mats from five hot springs in central Tibet. Extremophiles 13:139–149CrossRefPubMedGoogle Scholar
  39. 39.
    Lauro FM, Demaere MZ, Yau S, Brown MV, Ng C, Wilkins D, Raftery MJ, Gibson JA, Andrews-Pfannkoch C, Lewis M, Hoffman JM, Thomas T, Cavicchioli R (2011) An integrative study of a meromictic lake ecosystem in Antarctica. ISME J 5:879–895CrossRefPubMedGoogle Scholar
  40. 40.
    Lee BW, Van Lanen SG, Iwata-Reuyl D (2007) Mechanistic studies of Bacillus subtilis QueF, the nitrile oxidoreductase involved in queuosine biosynthesis. Biochemistry 46:12844–12854CrossRefPubMedGoogle Scholar
  41. 41.
    Lehours AC, Bardot C, Thenot A, Debroas D, Fonty G (2005) Anaerobic microbial communities in Lake Pavin, a unique meromictic lake in France. Appl Environ Microbiol 71:7389–7400CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Lehours AC, Evans P, Bardot C, Joblin K, Gérard F (2007) Phylogenetic diversity of Archaea and bacteria in the anoxic zone of a meromictic lake (Lake Pavin, France). Appl Environ Microbiol 73:2016–2019CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Ley RE, Harris JK, Wilcox J, Spear JR, Miller SR, Bebout BM, Maresca JA, Bryant DA, Sogin ML, Pace NR (2006) Unexpected diversity and complexity of the Guerrero Negro hypersaline microbial mat. Appl Environ Microbiol 72:3685–3695CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Llirós M, Casamayor EO, Borrego C (2008) High archaeal richness in the water column of a freshwater sulfurous karstic lake along an interannual study. FEMS Microbiol Ecol 66:331–342CrossRefPubMedGoogle Scholar
  45. 45.
    López-López A, Yarza P, Richter M, Suárez-Suárez A, Antón J, Niemann H, Rosselló-Móra R (2011) Extremely halophilic microbial communities in anaerobic sediments from a solar saltern. Environ Microbiol Rep 2:258–271CrossRefGoogle Scholar
  46. 46.
    Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar BA et al (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    MacLeod FA, Guiot SR, Costerton JW (1990) Layered structure of bacterial aggregates produced in an upflow anaerobic sludge bed and filter reactor. Appl Environ Microbiol 56:1598–1607PubMedPubMedCentralGoogle Scholar
  48. 48.
    Mallet C, Basset M, Fonty G, Desvilettes C, Bourdier G, Debroas D (2004) Microbial population dynamics in the sediments of a eutrophic lake (Aydat, France) and characterization of some heterotrophic bacterial isolates. Microb Ecol 48:66–77CrossRefPubMedGoogle Scholar
  49. 49.
    Markert S, Arnd C, Felback H, Becher D, Sievert SM et al (2007) Physiological proteomics of the uncultured endosymbiont of Riftia pachyptila. Science 315:247–250CrossRefPubMedGoogle Scholar
  50. 50.
    Meyer F, Goesmann A, McHardy AC, Bartels D, Bekel T, Clausen J et al (2003) GenDB—an open source genome annotation system for prokaryote genomes. Nucleic Acids Res 31:2187–2195CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Meyer F, Paarmann D, D'Souza M, Olson R, Glass EM, Kubal M, Paczian T, Rodriguez A, Stevens R, Wilke A, Wilkening J, Edwards RA (2008) The metagenomics RAST server - a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 9:386CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Needleman SB, Wunsch CD (1970) A general method applicable to the search for similarities in the amino acid sequences of two proteins. J Mol Biol 48:443–453CrossRefPubMedGoogle Scholar
  53. 53.
    Nelson DM, Ohene-Adjei S, Hu FS, Cann IK, Mackie RI (2007) Bacterial diversity and distribution in the holocene sediments of a northern temperate lake. Microb Ecol 54:252–263CrossRefPubMedGoogle Scholar
  54. 54.
    Nelson KA, Moin NS, Bernhard AE (2009) Archaeal diversity and the prevalence of Crenarchaeota in salt marsh sediments. Appl Environ Microbiol 75:4211–4215CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Nercessian O, Noyes E, Kalyuzhnaya MG, Lidstrom ME, Chistoserdova L (2005) Bacterial populations active in metabolism of C1 compounds in the sediment of Lake Washington, a freshwater lake. Appl Environ Microbiol 71:6885–6899CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Noguchi H, Park J, Takagi T (2006) MetaGene: prokaryotic gene finding from environmental genome shotgun sequences. Nucleic Acids Res 34:D5623–D5630CrossRefGoogle Scholar
  57. 57.
    Omoregie EO, Mastalerz V, de Lange G, Straub KL, Kappler A, Røy H, Stadnitskaia A, Foucher JP, Boetius A (2008) Biogeochemistry and community composition of iron- and sulfur-precipitating microbial mats at the Chefren mud volcano (Nile Deep Sea Fan, Eastern Mediterranean). Appl Environ Microbiol 74:3198–3215CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Pflüger K, de Lorenzo V (2007) Growth-dependent phosphorylation of the PtsN (EIINtr) protein of Pseudomonas putida. J Biol Chem 282:18206–18211CrossRefPubMedGoogle Scholar
  59. 59.
    Porat I, Vishnivetskaya TA, Mosher JJ, Brandt CC, Yang ZK, Brooks SC, Liang L, Drake MM, Podar M, Brown SD, Palumbo AV (2010) Characterization of archaeal community in contaminated and uncontaminated surface stream sediments. Microb Ecol 60:784–795CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glöckner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Quast C (2006) MicHanThi—Design and Implementation of a System for the Prediction of Gene Functions in Genome Annotation Projects. Universität Bremen, Diploma workGoogle Scholar
  62. 62.
    Richter M, Lombardot T, Kostadinov I, Kottmann R, Peplies J, Duhaime MB, Glöckner FO (2008) JCoast—a biologist-centric software tool for data mining and comparison of prokaryotic (meta)genomes. BMC Bioinformatics 9:177CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Rivière D, Desvignes V, Pelletier E, Chaussonnerie S, Guermazi S, Weissenbach J, Li T, Camacho P, Sghir A (2009) Towards the definition of a core of microorganisms involved in anaerobic digestion of sludge. ISME J 3:700–714CrossRefPubMedGoogle Scholar
  64. 64.
    Robertson CE, Spear JR, Harris JK, Pace NR (2009) Diversity and stratification of Archaea in a hypersaline microbial mat. Appl Environ Microbiol 75:1801–1810CrossRefPubMedGoogle Scholar
  65. 65.
    Röling WF, Couto de Brito IR, Swanell RPJ, Head IM (2004) Response of archaeal communities in beach sediments to spilled oil and bioremediation. Appl Environ Microbiol 70:2614–2620CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Sahl JW, Schmidt R, Swanner ED, Mandernack KW, Templeton AS, Kieft TL, Smith RL, Sanford WE, Callaghan RL, Mitton JB, Spear JR (2008) Subsurface microbial diversity in deep-granitic-fracture water in Colorado. Appl Environ Microbiol 74:143–152CrossRefPubMedGoogle Scholar
  67. 67.
    Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71:1501–1506CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Schwarz JI, Lueders T, Eckert W, Conrad R (2007) Identification of acetate-utilizing Bacteria and Archaea in methanogenic profundal sediments of Lake Kinneret (Israel) by stable isotope probing of rRNA. Environ Microbiol 9:223–237CrossRefPubMedGoogle Scholar
  69. 69.
    Schwarz JIK, Eckert W, Conrad R (2007) Community structure of Archaea and Bacteria in a profundal lake sediment Lake Kinneret (Israel). Sys Appl Microbiol 30:239–254CrossRefGoogle Scholar
  70. 70.
    Siegel De Ea (1999) Microscopía óptica y caracterización de minerales. Departamento Ingeniería en Minas, Facultad de Ciencias Físicas y Matemáticas. Universidad de Chile, Santiago, p 98Google Scholar
  71. 71.
    Slot JC, Hibbett DS (2007) Horizontal transfer of a nitrate assimilation gene cluster and ecological transitions in fungi: a phylogenetic study. PLoS One 10:e1097CrossRefGoogle Scholar
  72. 72.
    Sorokin DY, Rusanov II, Pimenov NV, Tourova TP, Abbas B, Muyzer G (2010) Sulfidogenesis under extremely haloalkaline conditions in soda lakes of Kulunda Steppe (Altai, Russia). FEMS Microbiol Ecol 73:278–290PubMedGoogle Scholar
  73. 73.
    Swan BK, Ehrhardt CJ, Reifel KM, Moreno LI, Valentine DL (2010) Archaeal and bacterial communities respond differently to environmental gradients in anoxic sediments of a California hypersaline lake, the Salton Sea. Appl Environ Microbiol 76:757–768CrossRefPubMedGoogle Scholar
  74. 74.
    Tamaki H, Sekiguchi Y, Hanada S, Nakamura K, Nomura N, Matsumura M, Kamagata Y (2005) Comparative analysis of bacterial diversity in freshwater sediment of a shallow eutrophic lake by molecular and improved cultivation-based techniques. Appl Environ Microbiol 71:2162–2169CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Tamames J, Mira A (2010) Horizontal gene transfer in prokaryotic microbial communities. In: Marco D (ed) Metagenomics: theory, methods and applications. Caister Academic Press, Norfolk, VA, pp 39–53Google Scholar
  76. 76.
    Tang X, Gao G, Qin B, Zhu L, Chao J, Wang J, Yang G (2009) Characterization of bacterial communities associated with organic aggregates in a large, shallow, eutrophic freshwater lake (Lake Taihu, China). Microb Ecol 58:307–322CrossRefPubMedGoogle Scholar
  77. 77.
    Tatusov RL, Natale DA, Garkavtsev IV, Tatusova TA, Shankavaram UT, Rao BS et al (2001) The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res 29:22–28CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Teske A, Sorensen KB (2008) Uncultured archaea in deep marine subsurface sediments: have we caught them all? ISME J 2:3–18CrossRefPubMedGoogle Scholar
  79. 79.
    Thomsen TR, Finster K, Ramsing NB (2001) Biogeochemical and molecular signatures of anaerobic methane oxidation in a marine sediment. Appl Environ Microbiol 67:1646–1656CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Tsiamis G, Katsaveli K, Ntougias S, Kyrpides N, Andersen G, Piceno Y, Bourtzis K (2008) Prokaryotic community profiles at different operational stages of a Greek solar saltern. Res Microbiol 159:609–627CrossRefPubMedGoogle Scholar
  81. 81.
    Vieites JM, Guazzaroni ME, Beloqui A, Golyshin PN, Ferrer M (2010) Molecular methods to study complex microbial communities. Methods Mol Biol 668:1–37CrossRefPubMedGoogle Scholar
  82. 82.
    Wang J, Vollrath S, Behrends T, Bodelier PL, Muyzer G, Meima-Franke M, Den Oudsten F, Van Cappellen P, Laanbroek HJ (2011) Distribution and diversity of Gallionella-like neutrophilic iron oxidizers in a tidal freshwater marsh. Appl Environ Microbiol 77:2337–2344CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Wu X, Xi W, Ye W, Yang H (2007) Bacterial community composition of a shallow hypertrophic freshwater lake in China, revealed by 16S rRNA gene sequences. FEMS Microbiol Ecol 61:85–96CrossRefPubMedGoogle Scholar
  84. 84.
    Yarza P, Richter M, Peplies J, Euzéby J, Amann R, Schleifer K-H et al (2008) The All-Species Living Tree Project: a 16S rRNA-based phylogenetic tree of all sequenced type strains. Syst Appl Microbiol 31:241–250CrossRefPubMedGoogle Scholar
  85. 85.
    Ye W, Liu X, Lin S, Tan J, Pan J, Li D, Yang H (2009) The vertical distribution of bacterial and archaeal communities in the water and sediment of Lake Taihu. FEMS Microbiol Ecol 70:107–120CrossRefPubMedGoogle Scholar
  86. 86.
    Zaballos M, López-López A, Øvreås L, Galán-Bartual S, D'Auria G, Alba-Casado J et al (2006) Comparison of prokaryotic diversity at offshore oceanic locations reveals a different microbiota in the Mediterranean Sea. FEMS Microbiol Ecol 56:389–405CrossRefPubMedGoogle Scholar
  87. 87.
    Zellner G, Stackebrandt E, Messner P, Tindall BJ, Conway de Macario E, Kneifel H, Sleytr UB, Winter J (1989) Methanocorpusculaceae fam. nov., represented by Methanocorpusculum parvum, Methanocorpusculum sinense spec. nov. and Methanocorpusculum bavaricum spec. nov. Arch Microbiol 151:381–390CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Manuel Ferrer
    • 1
    Email author
  • María-Eugenia Guazzaroni
    • 1
  • Michael Richter
    • 2
  • Adela García-Salamanca
    • 3
  • Pablo Yarza
    • 2
  • Ana Suárez-Suárez
    • 2
  • Jennifer Solano
    • 4
  • María Alcaide
    • 1
  • Pieter van Dillewijn
    • 3
  • Maria Antonia Molina-Henares
    • 3
  • Nieves López-Cortés
    • 1
  • Yamal Al-Ramahi
    • 1
  • Carmen Guerrero
    • 5
  • Alejandro Acosta
    • 3
  • Laura I. de Eugenio
    • 6
  • Virginia Martínez
    • 6
  • Silvia Marques
    • 3
  • Fernando Rojo
    • 7
  • Eduardo Santero
    • 8
  • Olga Genilloud
    • 9
  • Julian Pérez-Pérez
    • 10
  • Ramón Rosselló-Móra
    • 2
  • Juan Luis Ramos
    • 3
  1. 1.CSIC, Institute of CatalysisMadridSpain
  2. 2.IMEDEA (CSIC-UIB)EsporlesSpain
  3. 3.CSIC, Estación Experimental del ZaidínGranadaSpain
  4. 4.Bio-Illiberis R&DArmillaSpain
  5. 5.Facultad de CienciasUniversidad Autónoma de MadridMadridSpain
  6. 6.CSIC, Centro de Investigaciones BiológicasMadridSpain
  7. 7.CSIC, Centro Nacional de BiotecnologíaMadridSpain
  8. 8.Universidad Pablo de OlavideSevillaSpain
  9. 9.Fundación MedinaArmillaSpain
  10. 10.SecugenMadridSpain

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