Metagenomes of Mediterranean Coastal Lagoons

Coastal lagoons, both hypersaline and freshwater, are common, but still understudied ecosystems. We describe, for the first time, using high throughput sequencing, the extant microbiota of two large and representative Mediterranean coastal lagoons, the hypersaline Mar Menor, and the freshwater Albufera de Valencia, both located on the south eastern coast of Spain. We show there are considerable differences in the microbiota of both lagoons, in comparison to other marine and freshwater habitats. Importantly, a novel uncultured sulfur oxidizing Alphaproteobacteria was found to dominate bacterioplankton in the hypersaline Mar Menor. Also, in the latter prokaryotic cyanobacteria were almost exclusively comprised by Synechococcus and no Prochlorococcus was found. Remarkably, the microbial community in the freshwaters of the hypertrophic Albufera was completely in contrast to known freshwater systems, in that there was a near absence of well known and cosmopolitan groups of ultramicrobacteria namely Low GC Actinobacteria and the LD12 lineage of Alphaproteobacteria.

[1]  H. Utermöhl Zur Vervollkommnung der quantitativen Phytoplankton-Methodik , 1958 .

[2]  H. Caspers Das Phytoplankton des Süßwassers. Systematik und Biologie. Hrsg. G. Huber-Pestalozzi. Band XVI, 6. Teil Chlorophyceen (Grünalgen). Ordnung: Tetrasporales. Von B. Fott. Stuttgart: E. Schweizerbart'sche Verlagsbuchhandlung (Nägele u. Obermiller) 1972. DM 56, — , 1974 .

[3]  A. Anton,et al.  Use of cluster analysis in the systematics of the algal genus Cryptomonas , 1981 .

[4]  H. Ettl,et al.  Süsswasserflora von Mitteleuropa , 1985 .

[5]  K. Anagnostidis,et al.  Modern approach to the classification system of cyanophytes. 3 - Oscillatoriales , 1988 .

[6]  A. Lewitus,et al.  Improved separations of phytoplankton pigments using temperature-controlled high performance liquid chromatography , 1994 .

[7]  F. Rodríguez-Valera,et al.  Bacterial diversity in two coastal lagoons deduced from 16S rDNA PCR amplification and partial sequencing , 1995 .

[8]  M. Kawachi,et al.  Functional roles of the haptonema and the spine scales in the feeding process of Chrysochromulina spinifera (Fournier) Pienaar et Norris (Haptophyta = Prymnesiophyta) , 1995 .

[9]  H. Paerl,et al.  Flow scintillation counting of 14 C-labeled microalgal photosynthetic pigments , 1996 .

[10]  T. Zohary,et al.  Bacterial abundance, biomass, and production in relation to phytoplankton biomass in the Levantine Basin of the southeastern Mediterranean Sea , 1996 .

[11]  B. Methé,et al.  Bacterial diversity in Adirondack mountain lakes as revealed by 16S rRNA gene sequences , 1997, Applied and environmental microbiology.

[12]  D. Vaqué,et al.  Dynamics of ciliate abundance, biomass and community composition in an oligotrophic coastal environment (NW Mediterranean) , 1997 .

[13]  Donald M. Anderson,et al.  Physiological ecology of harmful algal blooms , 1998 .

[14]  F. Niell,et al.  SHORT COMMUNICATION Synechococcus and Prochlorococcus-like populations detected by flow cytometry in a eutrophic reservoir in summer , 1999 .

[15]  N. L. Bel’kova,et al.  [Diversity of bacteria at various depths in the southern part of lake Baikal as detected by 16S rRNA sequencing]. , 1999, Mikrobiologiia.

[16]  Rudolf Amann,et al.  Comparative 16S rRNA Analysis of Lake Bacterioplankton Reveals Globally Distributed Phylogenetic Clusters Including an Abundant Group of Actinobacteria , 2000, Applied and Environmental Microbiology.

[17]  R. Kraft,et al.  Novel Genes Coding for Lithotrophic Sulfur Oxidation of Paracoccus pantotrophus GB17 , 2000, Journal of bacteriology.

[18]  J. Antón,et al.  Archaeal Biodiversity in Crystallizer Ponds from a Solar Saltern: Culture versus PCR , 2000, Microbial Ecology.

[19]  Erin R. Haramoto,et al.  Harmful algal blooms in the Chesapeake and Coastal Bays of Maryland, USA: Comparison of 1997, 1998, and 1999 events , 2001 .

[20]  C. Friedrich,et al.  The cysteine residue of the SoxY protein as the active site of protein‐bound sulfur oxidation of Paracoccus pantotrophus GB17 , 2001, FEBS letters.

[21]  Frede Thingstad,et al.  Prokaryotic genetic diversity throughout the salinity gradient of a coastal solar saltern. , 2002, Environmental microbiology.

[22]  P. Falkowski The ocean's invisible forest. , 2002, Scientific American.

[23]  Louis Legendre,et al.  Fluxes of carbon in the upper ocean: regulation by food-web control nodes , 2002 .

[24]  F. Hagen,et al.  Typical freshwater bacteria: an analysis of available 16S rRNA gene sequences from plankton of lakes and rivers , 2002 .

[25]  M. Hahn Isolation of Strains Belonging to the Cosmopolitan Polynucleobacter necessarius Cluster from Freshwater Habitats Located in Three Climatic Zones , 2003, Applied and Environmental Microbiology.

[26]  Maria Rosa Miracle,et al.  Which factors determine the abundance and distribution of picocyanobacteria in inland waters? A comparison among different types of lakes and ponds , 2003 .

[27]  T. Kratz,et al.  Temporal Patterns in Bacterial Communities in Three Temperate Lakes of Different Trophic Status , 2003, Microbial Ecology.

[28]  A. G. Humes How many copepods? , 2004, Hydrobiologia.

[29]  D. Canfield,et al.  Use of an alternative method for monitoring total nitrogen concentrations in Florida lakes , 1996, Hydrobiologia.

[30]  O. White,et al.  Environmental Genome Shotgun Sequencing of the Sargasso Sea , 2004, Science.

[31]  Maria Rosa Miracle,et al.  Population dynamics and ecology of subdominant phytoplankton species in a shallow hypertrophic lake (Albufera of Valencia, Spain) , 2004, Hydrobiologia.

[32]  Philip Hugenholtz,et al.  Chthoniobacter flavus gen. nov., sp. nov., the First Pure-Culture Representative of Subdivision Two, Spartobacteria classis nov., of the Phylum Verrucomicrobia , 2004, Applied and Environmental Microbiology.

[33]  S. Romo,et al.  Phytoplankton changes in a shallow Mediterranean lake (Albufera of Valencia, Spain) after sewage diversion , 2003, Hydrobiologia.

[34]  G. Zwart,et al.  Distribution of Typical Freshwater Bacterial Groups Is Associated with pH, Temperature, and Lake Water Retention Time , 2005, Applied and Environmental Microbiology.

[35]  Eric W. Triplett,et al.  Geographic and Environmental Sources of Variation in Lake Bacterial Community Composition , 2005, Applied and Environmental Microbiology.

[36]  M. Noordewier,et al.  Genome Streamlining in a Cosmopolitan Oceanic Bacterium , 2005, Science.

[37]  C. Friedrich,et al.  Prokaryotic sulfur oxidation. , 2005, Current opinion in microbiology.

[38]  C. Stedmon,et al.  Resolving the variability in dissolved organic matter fluorescence in a temperate estuary and its catchment using PARAFAC analysis , 2005 .

[39]  Á. Pérez-Ruzafa,et al.  Spatial and temporal variations of hydrological conditions, nutrients and chlorophyll a in a Mediterranean coastal lagoon (Mar Menor, Spain) , 2005, Hydrobiologia.

[40]  Maureen L. Coleman,et al.  Three Prochlorococcus Cyanophage Genomes: Signature Features and Ecological Interpretations , 2005, PLoS biology.

[41]  E. Delong,et al.  Community Genomics Among Stratified Microbial Assemblages in the Ocean's Interior , 2006, Science.

[42]  Satoru Taguchi,et al.  Detecting the bloom-forming dinoflagellate Alexandrium tamarense using the absorption signature , 2006, Hydrobiologia.

[43]  S. Juggins,et al.  COASTAL DIATOM–ENVIRONMENT RELATIONSHIPS FROM THE GULF OF FINLAND, BALTIC SEA 1 , 2006 .

[44]  J. Soria,et al.  Past, present and future of la Albufera of Valencia Natural Park , 2006, Limnetica.

[45]  J. Velasco,et al.  Nutrient And Particulate Inputs Into The Mar Menor Lagoon (Se Spain) From An Intensive Agricultural Watershed , 2006 .

[46]  Kyun-Woo Lee,et al.  Effects of diets on the growth of the brackish water cyclopoid copepod Paracyclopina nana Smirnov , 2006 .

[47]  M. Wagner,et al.  The Planctomycetes, Verrucomicrobia, Chlamydiae and sister phyla comprise a superphylum with biotechnological and medical relevance. , 2006, Current opinion in biotechnology.

[48]  M. Hahn,et al.  Differences in structure and dynamics of Polynucleobacter communities in a temperate and a subtropical lake, revealed at three phylogenetic levels. , 2006, FEMS microbiology ecology.

[49]  P. Negro,et al.  Picocyanobacteria in Adriatic transitional environments , 2007 .

[50]  A. Cembella,et al.  On the allelochemical potency of the marine dinoflagellate Alexandrium ostenfeldii against heterotrophic and autotrophic protists , 2007 .

[51]  K. McMahon,et al.  Phylogenetic Ecology of the Freshwater Actinobacteria acI Lineage , 2007, Applied and Environmental Microbiology.

[52]  E. Reavie,et al.  A diatom quality index from a diatom-based total phosphorus inference model , 2007 .

[53]  R. Knight,et al.  Global patterns in bacterial diversity , 2007, Proceedings of the National Academy of Sciences.

[54]  H. Kasai,et al.  Coraliomargarita akajimensis gen. nov., sp. nov., a novel member of the phylum 'Verrucomicrobia' isolated from seawater in Japan. , 2007, International journal of systematic and evolutionary microbiology.

[55]  A. Halpern,et al.  The Sorcerer II Global Ocean Sampling Expedition: Northwest Atlantic through Eastern Tropical Pacific , 2007, PLoS biology.

[56]  Alexander F. Auch,et al.  MEGAN analysis of metagenomic data. , 2007, Genome research.

[57]  J. García-Pintado,et al.  Anthropogenic nutrient sources and loads from a Mediterranean catchment into a coastal lagoon: Mar Menor, Spain. , 2007, The Science of the total environment.

[58]  S. Fraga,et al.  Phylogenetic relationships among the Mediterranean Alexandrium (Dinophyceae) species based on sequences of 5.8S gene and Internal Transcript Spacers of the rRNA operon , 2008 .

[59]  R. Wit Microbial diversity in the Bassin d’Arcachon coastal lagoon (SW France) , 2008, Hydrobiologia.

[60]  P. B. Pope,et al.  Metagenomic analysis of a freshwater toxic cyanobacteria bloom. , 2008, FEMS microbiology ecology.

[61]  Susana G. Romo Pérez,et al.  Tendencias del fitoplancton en el lago de la Albufera de Valencia e implicaciones para su ecología, gestión y recuperación , 2008, Limnetica.

[62]  A. Oren Microbial life at high salt concentrations: phylogenetic and metabolic diversity , 2008, Saline systems.

[63]  A. Ventosa,et al.  Prokaryotic diversity in one of the largest hypersaline coastal lagoons in the world , 2008, Extremophiles.

[64]  H. Kasai,et al.  Haloferula rosea gen. nov., sp. nov., Haloferula harenae sp. nov., Haloferula phyci sp. nov., Haloferula helveola sp. nov. and Haloferula sargassicola sp. nov., five marine representatives of the family Verrucomicrobiaceae within the phylum 'Verrucomicrobia'. , 2008, International journal of systematic and evolutionary microbiology.

[65]  O. Béjà,et al.  Comparative analyses of actinobacterial genomic fragments from Lake Kinneret. , 2009, Environmental microbiology.

[66]  J. Humbert,et al.  Metagenomic approach studying the taxonomic and functional diversity of the bacterial community in a mesotrophic lake (Lac du Bourget--France). , 2009, Environmental microbiology.

[67]  J. J. Abellán,et al.  Environmental distribution of prokaryotic taxa , 2010, BMC Microbiology.

[68]  O. Béjà,et al.  Bias in assessments of marine SAR11 biodiversity in environmental fosmid and BAC libraries? , 2009, The ISME Journal.

[69]  R. Amann,et al.  Substrate incorporation patterns of bacterioplankton populations in stratified and mixed waters of a humic lake. , 2009, Environmental microbiology.

[70]  Martin Hartmann,et al.  Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities , 2009, Applied and Environmental Microbiology.

[71]  P. Negro,et al.  Structural dynamics of bacterioplankton assemblages in the Lagoon of Venice , 2009 .

[72]  K. McMahon,et al.  Evidence for structuring of bacterial community composition by organic carbon source in temperate lakes. , 2009, Environmental microbiology.

[73]  K. Šimek,et al.  Limnohabitans australis sp. nov., isolated from a freshwater pond, and emended description of the genus Limnohabitans , 2010, International journal of systematic and evolutionary microbiology.

[74]  Michael Shmoish,et al.  Microbial community genomics in eastern Mediterranean Sea surface waters , 2010, The ISME Journal.

[75]  E. Stackebrandt,et al.  Polynucleobacter cosmopolitanus sp. nov., free-living planktonic bacteria inhabiting freshwater lakes and rivers. , 2010, International journal of systematic and evolutionary microbiology.

[76]  K. Šimek,et al.  Limnohabitans curvus gen. nov., sp. nov., a planktonic bacterium isolated from a freshwater lake. , 2010, International journal of systematic and evolutionary microbiology.

[77]  S. Langenheder,et al.  Ubiquity of Polynucleobacter necessarius ssp. asymbioticus in lentic freshwater habitats of a heterogeneous 2000 km area. , 2010, Environmental microbiology.

[78]  E. Ammar,et al.  Novel prokaryotic diversity in sediments of Tunisian multipond solar saltern. , 2010, Research in microbiology.

[79]  F. Rodríguez-Valera,et al.  Metagenome of the Mediterranean deep chlorophyll maximum studied by direct and fosmid library 454 pyrosequencing , 2010, The ISME Journal.

[80]  R. Amann,et al.  Bacterioplankton diversity and community composition in the Southern Lagoon of Venice. , 2010, Systematic and applied microbiology.

[81]  Itai Sharon,et al.  Comparative community genomics in the Dead Sea: an increasingly extreme environment , 2010, The ISME Journal.

[82]  Rohit Ghai,et al.  Metagenomics of the Water Column in the Pristine Upper Course of the Amazon River , 2011, PloS one.

[83]  Katherine D. McMahon,et al.  A Guide to the Natural History of Freshwater Lake Bacteria , 2011, Microbiology and Molecular Reviews.

[84]  M. Hartmann,et al.  Metaxa: a software tool for automated detection and discrimination among ribosomal small subunit (12S/16S/18S) sequences of archaea, bacteria, eukaryotes, mitochondria, and chloroplasts in metagenomes and environmental sequencing datasets , 2011, Antonie van Leeuwenhoek.

[85]  Purificación López-García,et al.  Comparative metagenomics of bathypelagic plankton and bottom sediment from the Sea of Marmara , 2010, The ISME Journal.

[86]  W. Inskeep,et al.  Yellowstone Lake: high-energy geochemistry and rich bacterial diversity. , 2011, Environmental microbiology.

[87]  R. Stepanauskas,et al.  New Abundant Microbial Groups in Aquatic Hypersaline Environments , 2011, Scientific reports.

[88]  M. Denis,et al.  Characterization of heterotrophic prokaryote subgroups in the Sfax coastal solar salterns by combining flow cytometry cell sorting and phylogenetic analysis , 2011, Extremophiles.

[89]  Konstantinos T. Konstantinidis,et al.  Metagenomic Insights into the Evolution, Function, and Complexity of the Planktonic Microbial Community of Lake Lanier, a Temperate Freshwater Ecosystem , 2011, Applied and Environmental Microbiology.

[90]  F. Rodríguez-Valera,et al.  Breaking a paradigm: cosmopolitan and abundant freshwater actinobacteria are low GC. , 2012, Environmental microbiology reports.

[91]  J. Banfield,et al.  De novo metagenomic assembly reveals abundant novel major lineage of Archaea in hypersaline microbial communities , 2011, The ISME Journal.

[92]  Marina Montresor,et al.  The globally distributed genus Alexandrium: multifaceted roles in marine ecosystems and impacts on human health. , 2012, Harmful algae.