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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 references 58

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          MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0.

          We announce the release of the fourth version of MEGA software, which expands on the existing facilities for editing DNA sequence data from autosequencers, mining Web-databases, performing automatic and manual sequence alignment, analyzing sequence alignments to estimate evolutionary distances, inferring phylogenetic trees, and testing evolutionary hypotheses. Version 4 includes a unique facility to generate captions, written in figure legend format, in order to provide natural language descriptions of the models and methods used in the analyses. This facility aims to promote a better understanding of the underlying assumptions used in analyses, and of the results generated. Another new feature is the Maximum Composite Likelihood (MCL) method for estimating evolutionary distances between all pairs of sequences simultaneously, with and without incorporating rate variation among sites and substitution pattern heterogeneities among lineages. This MCL method also can be used to estimate transition/transversion bias and nucleotide substitution pattern without knowledge of the phylogenetic tree. This new version is a native 32-bit Windows application with multi-threading and multi-user supports, and it is also available to run in a Linux desktop environment (via the Wine compatibility layer) and on Intel-based Macintosh computers under the Parallels program. The current version of MEGA is available free of charge at (http://www.megasoftware.net).
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            Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation.

            Interactive Tree Of Life (iTOL) is a web-based tool for the display, manipulation and annotation of phylogenetic trees. Trees can be interactively pruned and re-rooted. Various types of data such as genome sizes or protein domain repertoires can be mapped onto the tree. Export to several bitmap and vector graphics formats is supported. iTOL is available at http://itol.embl.de
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              Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species.

              With millions of species and their life-stage transformations, the animal kingdom provides a challenging target for taxonomy. Recent work has suggested that a DNA-based identification system, founded on the mitochondrial gene, cytochrome c oxidase subunit 1 (COI), can aid the resolution of this diversity. While past work has validated the ability of COI sequences to diagnose species in certain taxonomic groups, the present study extends these analyses across the animal kingdom. The results indicate that sequence divergences at COI regularly enable the discrimination of closely allied species in all animal phyla except the Cnidaria. This success in species diagnosis reflects both the high rates of sequence change at COI in most animal groups and constraints on intraspecific mitochondrial DNA divergence arising, at least in part, through selective sweeps mediated via interactions with the nuclear genome.
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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
                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
                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.
                Counts
                Pages: 14
                Categories
                Research Article
                Ecology/Marine and Freshwater Ecology
                Microbiology/Environmental Microbiology
                Marine and Aquatic Sciences/Genetics, Genomics, and Barcoding

                Uncategorized

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