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      Environmental Barcoding Reveals Massive Dinoflagellate Diversity in Marine Environments

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          Abstract

          Background

          Dinoflagellates are an ecologically important group of protists with important functions as primary producers, coral symbionts and in toxic red tides. Although widely studied, the natural diversity of dinoflagellates is not well known. DNA barcoding has been utilized successfully for many protist groups. We used this approach to systematically sample known “species”, as a reference to measure the natural diversity in three marine environments.

          Methodology/Principal Findings

          In this study, we assembled a large cytochrome c oxidase 1 (COI) barcode database from 8 public algal culture collections plus 3 private collections worldwide resulting in 336 individual barcodes linked to specific cultures. We demonstrate that COI can identify to the species level in 15 dinoflagellate genera, generally in agreement with existing species names. Exceptions were found in species belonging to genera that were generally already known to be taxonomically challenging, such as Alexandrium or Symbiodinium. Using this barcode database as a baseline for cultured dinoflagellate diversity, we investigated the natural diversity in three diverse marine environments (Northeast Pacific, Northwest Atlantic, and Caribbean), including an evaluation of single-cell barcoding to identify uncultivated groups. From all three environments, the great majority of barcodes were not represented by any known cultured dinoflagellate, and we also observed an explosion in the diversity of genera that previously contained a modest number of known species, belonging to Kareniaceae. In total, 91.5% of non-identical environmental barcodes represent distinct species, but only 51 out of 603 unique environmental barcodes could be linked to cultured species using a conservative cut-off based on distances between cultured species.

          Conclusions/Significance

          COI barcoding was successful in identifying species from 70% of cultured genera. When applied to environmental samples, it revealed a massive amount of natural diversity in dinoflagellates. This highlights the extent to which we underestimate microbial diversity in the environment.

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          Most cited references47

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          Global dispersal of free-living microbial eukaryote species.

          The abundance of individuals in microbial species is so large that dispersal is rarely (if ever) restricted by geographical barriers. This "ubiquitous" dispersal requires an alternative view of the scale and dynamics of biodiversity at the microbial level, wherein global species number is relatively low and local species richness is always sufficient to drive ecosystem functions.
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            Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton.

            Phylogenetic information from ribosomal RNA genes directly amplified from the environment changed our view of the biosphere, revealing an extraordinary diversity of previously undetected prokaryotic lineages. Using ribosomal RNA genes from marine picoplankton, several new groups of bacteria and archaea have been identified, some of which are abundant. Little is known, however, about the diversity of the smallest planktonic eukaryotes, and available information in general concerns the phytoplankton of the euphotic region. Here we recover eukaryotes in the size fraction 0.2-5 microm from the aphotic zone (250-3,000 m deep) in the Antarctic polar front. The most diverse and relatively abundant were two new groups of alveolate sequences, related to dinoflagellates that are found at all studied depths. These may be important components of the microbial community in the deep ocean. Their phylogenetic position suggests a radiation early in the evolution of alveolates.
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              The use of mean instead of smallest interspecific distances exaggerates the size of the "barcoding gap" and leads to misidentification.

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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2010
                15 November 2010
                : 5
                : 11
                : e13991
                Affiliations
                [1 ]The Biodiversity Research Centre, University of British Columbia, Vancouver, British Columbia, Canada
                [2 ]Department of Geology, State University of New York at Buffalo, Buffalo, New York, United States of America
                [3 ]Provasoli-Guillard National Center for Culture of Marine Phytoplankton, Bigelow Laboratory for Ocean Sciences, West Boothbay Harbor, Maine, United States of America
                [4 ]Culture Collection of Algae and Protozoa, Scottish Association for Marine Science, Scottish Marine Institute, Oban, United Kingdom
                [5 ]Australian National Algae Culture Collection, CSIRO Marine and Atmospheric Research, Hobart, Australia
                [6 ]Forschungsinstitut Senckenberg, Deutsches Zentrum für Marine Biodiversitätsforschung (DZMB), Wilhelmshaven, Germany
                [7 ]Algobank-Caen, Université de Caen Basse-Normandie, Caen, France
                [8 ]National Institute for Environmental Studies, Tsukuba, Japan
                [9 ]School of Biological Sciences, University of Texas at Austin, Austin, Texas, United States of America
                University of Canterbury, New Zealand
                Author notes

                Conceived and designed the experiments: RFS PJK. Performed the experiments: RFS MAC ERJ. Analyzed the data: RFS AH RA MAC FCK IJ MH ERJ PJK. Contributed reagents/materials/analysis tools: AH RA MAC RAA FCK IJ MH BV FK JB PJK. Wrote the paper: RFS PJK. Contributed to manuscript preparation: AH RA MAC FCK RAA IJ MH BV FK JB. Established cultures: MAC MH. Contributed to collective acquisition of cultures: RAA. Contributed to interpretation of results: RAA IJ MH. Contributed to preparation of materials: IJ.

                Article
                10-PONE-RA-19357R1
                10.1371/journal.pone.0013991
                2981561
                21085582
                8b6b1f9f-5612-4933-b0a1-0687e5ba9876
                Stern 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.
                History
                : 29 May 2010
                : 12 October 2010
                Page count
                Pages: 14
                Categories
                Research Article
                Ecology/Marine and Freshwater Ecology
                Microbiology/Environmental Microbiology
                Marine and Aquatic Sciences/Genetics, Genomics, and Barcoding

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