Abstract
BackgroundDinoflagellates 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 FindingsIn 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/SignificanceCOI 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.
Highlights
Assessing biodiversity in the microbial world has always been a difficult problem: are microorganisms inherently more difficult to examine and differentiate by classical methods, but it is not clear if the theoretical taxonomic frameworks, applied to more familiar life forms, even apply to the diversity of microbial life
Most culture collections were heavily biased towards photosynthetic, planktonic and toxic genera such as Alexandrium, Scrippsiella, Karlodinium, and Karenia. Another well represented taxon was Symbiodinium, a diverse genus divided into the so-called clades A–H originally based on small (SSU) ribosomal subunit phylogeny and later incorporated results from other DNA markers that resulted in the subdivision of clades into subclades or types, as reviewed in [47]
Concluding Remarks: natural diversity of microbial life Our results show cultured dinoflagellates that are considered to be different species can be resolved using DNA barcoding, robust taxonomy using other DNA markers, morphology and chemotaxonomic markers such as lipids and pigments is needed to provide a solid basis for DNA barcoding to work [99]
Summary
Assessing biodiversity in the microbial world has always been a difficult problem: are microorganisms inherently more difficult to examine and differentiate by classical methods, but it is not clear if the theoretical taxonomic frameworks, applied to more familiar life forms, even apply to the diversity of microbial life. Even the validity of the species concept is debatable for some protist groups. The protists, there is a persistent debate over how much diversity exists, irrespective of how we divide it up. On one side of the debate it is argued that protist diversity typically consists of a relatively few cosmopolitan species because their small size allows them to live ubiquitously [1,2,3]. Cosmopolitan genera can exist as multiple distinct genetic and even reproductive entities [6,7]. 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
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