Closely related dinoflagellate species in vastly different habitats–an example of a marine–freshwater transition

Phytoplankton are present in a large variety of aquatic environments, ranging from small freshwater ponds to the oceans. Typically, freshwater and marine species are not closely related, indicating an ancient divergence and that salinity poses a strong dispersal barrier. Here we reveal a common recent origin of two dinoflagellates that are well adapted to different habitats. Gymnodinium baicalense inhabits the geologically old freshwater Lake Baikal, which is located in the middle of the Eurasian continent. Gymnodinium corollarium, on the other hand, is a brackish water species from the Baltic Sea. Both species form blooms under ice during the spring. We generated 10 DNA sequences from these species. The partial 28S rRNA gene from G. baicalense and the partial 18S rRNA gene and internal transcribed spacer-2 (ITS2) from G. corollarium were sequenced for the first time. A more detailed description of G. baicalense, which was previously known only from light microscopy observations, is also provided. In the laboratory we demonstrated that G. baicalense is strictly adapted to fresh water, while G. corollarium had a wide salinity tolerance. However, the two species have almost identical morphology, identical SSU rRNA gene sequences, and only small differences in the LSU rRNA gene and ITS2. We infer a common ancestor, which was a species from the Arctic region with a tolerance to a range of salinities. Our data support the scenario that the under-ice phytoplankton community in Lake Baikal has been formed recently, even though the lake is the oldest in the world

Tracing the Origin of Planktonic Protists in an Ancient Lake

Special issue Protist Molecular Ecology in Continental Systems.-- 19 pages, 7 figures, 1 table, supplementary material https://doi.org/10.3390/microorganisms8040543Ancient lakes are among the most interesting models for evolution studies because their biodiversity is the result of a complex combination of migration and speciation. Here, we investigate the origin of single celled planktonic eukaryotes from the oldest lake in the world—Lake Baikal (Russia). By using 18S rDNA metabarcoding, we recovered 1414 Operational Taxonomic Units (OTUs) belonging to protists populating surface waters (1–50 m) and representing pico/nano-sized cells. The recovered communities resembled other lacustrine freshwater assemblages found elsewhere, especially the taxonomically unclassified protists. However, our results suggest that a fraction of Baikal protists could belong to glacial relicts and have close relationships with marine/brackish species. Moreover, our results suggest that rapid radiation may have occurred among some protist taxa, partially mirroring what was already shown for multicellular organisms in Lake Baikal. We found 16% of the OTUs belonging to potential species flocks in Stramenopiles, Alveolata, Opisthokonta, Archaeplastida, Rhizaria, and Hacrobia. Putative flocks predominated in Chrysophytes, which are highly diverse in Lake Baikal. Also, the 18S rDNA of a number of species (7% of the total) differed >10% from other known sequences. These taxa as well as those belonging to the flocks may be endemic to Lake Baikal. Overall, our study points to novel diversity of planktonic protists in Lake Baikal, some of which may have emerged in situ after evolutionary diversificationN.V.A. was supported by a grant of the Russian Science Foundation (18-74-00054). R.L. was supported by a Ramón y Cajal fellowship (RYC-2013-12554, MINECO, Spain). Lake Baikal expedition was supported by the Russian state assignment to N.V.A. (0345-2016-0009). DNA sequencing was supported with research start-up funding to R.L. (RYC-2013-12554, MINECO, Spain)With the funding support of the ‘Severo Ochoa Centre of Excellence’ accreditation (CEX2019-000928-S), of the Spanish Research Agency (AEI

Delineating closely related dinoflagellate lineages using phylotranscriptomics

Recently radiated dinoflagellates Apocalathium aciculiferum (collected in Lake Erken, Sweden), Apocalathium malmogiense (Baltic Sea) and Apocalathium aff. malmogiense (Highway Lake, Antarctica) represent a lineage with an unresolved phylogeny. We determined their phylogenetic relationships using phylotranscriptomics based on 792 amino acid sequences. Our results showed that A. aciculiferum diverged from the other two closely related lineages, consistent with their different morphologies in cell size, relative cell length and presence of spines. We hypothesized that A. aff. malmogiense and A. malmogiense, which inhabit different hemispheres, are evolutionarily more closely related because they diverged from a marine common ancestor, adapting to a wide salinity range, while A. aciculiferum colonized a freshwater habitat, by acquiring adaptations to this environment, in particular, salinity intolerance. We show that phylotranscriptomics can resolve the phylogeny of recently diverged protists. This has broad relevance, given that many phytoplankton species are morphologically very similar, and single genes sometimes lack the information to determine species’ relationships

Recent radiation in a marine and freshwater dinoflagellate species flock.

Processes of rapid radiation among unicellular eukaryotes are much less studied than among multicellular organisms. We have investigated a lineage of cold-water microeukaryotes (protists) that appear to have diverged recently. This lineage stands in stark contrast to known examples of phylogenetically closely related protists, in which genetic difference is typically larger than morphological differences. We found that the group not only consists of the marine-brackish dinoflagellate species Scrippsiella hangoei and the freshwater species Peridinium aciculiferum as discovered previously but also of a whole species flock. The additional species include Peridinium euryceps and Peridinium baicalense, which are restricted to a few lakes, in particular to the ancient Lake Baikal, Russia, and freshwater S. hangoei from Lake Baikal. These species are characterized by relatively large conspicuous morphological differences, which have given rise to the different species descriptions. However, our scanning electron microscopic studies indicate that they belong to a single genus according to traditional morphological characterization of dinoflagellates (thecal plate patterns). Moreover, we found that they have identical SSU (small subunit) rDNA fragments and distinct but very small differences in the DNA markers LSU (large subunit) rDNA, ITS2 (internal transcribed spacer 2) and COB (cytochrome b) gene, which are used to delineate dinoflagellates species. As some of the species co-occur, and all four have small but species-specific sequence differences, we suggest that these taxa are not a case of phenotypic plasticity but originated via recent adaptive radiation. We propose that this is the first clear example among free-living microeukaryotes of recent rapid diversification into several species followed by dispersion to environments with different ecological conditions.The ISME Journal advance online publication, 20 January 2015; doi:10.1038/ismej.2014.267