Cryptic speciation in Protoceratium reticulatum (Dinophyceae): Evidence from morphological, molecular and ecophysiological data

Type Article
Date 2019-09
Language English
Author(s) Wang Na1, Mertens KennethORCID2, Krock Bernd3, Luo Zhaohe1, Derrien AmelieORCID2, Pospelova Vera4, Liang Yubo5, Bilien GwenaelORCID2, Smith Kirsty F.6, de Schepper Stijn7, Wietkamp Stephan3, Tillmann Urban3, Gu Haifeng1
Affiliation(s) 1 : Third Institute of Oceanography, Ministry of Natural Resources, Xiamen 361005, China
2 : Ifremer, LER BO, Station de Biologie Marine, Place de la Croix, BP40537, F-29185 Concarneau CEDEX, France
3 : Alfred Wegener Institute for Polar and Marine Research, Am Handelshafen 12, D-27570 Bremerhaven, Germany
4 : School of Earth and Ocean Sciences, University of Victoria, OEASB A405, P. O. Box 1700 16 STN CSC, Victoria, British Columbia, V8W 2Y2, Canada
5 : National Marine Environmental Monitoring Center, Ministry of Ecology and Environment, Dalian, 116023, China
6 : Cawthron Institute, 98 Halifax Street East, Private Bag 2, Nelson 7042, New Zealand
7 : NORCE Climate, NORCE Norwegian Research Centre AS, Bjerknes Centre for Climate Research, Jahnebakken 5, 5007 Bergen, Norway
Source Harmful Algae (1568-9883) (Elsevier BV), 2019-09 , Vol. 88 , P. 101610 (15p.)
DOI 10.1016/j.hal.2019.05.003
WOS© Times Cited 25
Keyword(s) Biogeography, Intraspecific variability, Cysts, Growth, ITS rDNA sequences, Ribotype, Yessotoxin

The cosmopolitan, potentially toxic dinoflagellate Protoceratium reticulatum possesses a fossilizable cyst stage which is an important paleoenvironmental indicator. Slight differences in the internal transcribed spacer ribosomal DNA (ITS rDNA) sequences of P. reticulatum have been reported, and both the motile stage and cyst morphology of P. reticulatum display phenotypic plasticity, but how these morpho-molecular variations are related with ecophysiological preferences is unknown. Here, 55 single cysts or cells were isolated from localities in the Northern (Arctic to subtropics) and Southern Hemispheres (Chile and New Zealand), and in total 34 strains were established. Cysts and/or cells were examined with light microscopy and/or scanning electron microscopy. Large subunit ribosomal DNA (LSU rDNA) and/or ITS rDNA sequences were obtained for all strains/isolates. All strains/isolates of P. reticulatum shared identical LSU sequences except for one strain from the Mediterranean Sea that differs in one position, however ITS rDNA sequences displayed differences at eight positions. Molecular phylogeny was inferred using maximum likelihood and Bayesian inference based on ITS rDNA sequences. The results showed that P. reticulatum comprises at least three ribotypes (designated as A, B, and C). Ribotype A included strains from the Arctic and temperate areas, ribotype B included strains from temperate regions only, and ribotype C included strains from the subtropical and temperate areas. The average ratios of process length to cyst diameter of P. reticulatum ranged from 15% in ribotype A, 22% in ribotype B and 17% in ribotype C but cyst size could overlap. Theca morphology was indistinguishable among ribotypes. The ITS-2 secondary structures of ribotype A displayed one CBC (compensatory change on two sides of a helix pairing) compared to ribotypes B and C. Growth response of one strain from each ribotype to various temperatures was examined. The strains of ribotypes A, B and C exhibited optimum growth at 15 °C, 20 °C and 20–25 °C, respectively, thus corresponding to cold, moderate and warm ecotypes. The profiles of yessotoxins (YTXs) were examined for 25 strains using liquid chromatography coupled with tandem mass spectrometry (LC–MS/MS). The parent compound yessotoxin (YTX) was produced by strains of ribotypes A and B, but not by ribotype C strains, which only produced the structural variant homoyessotoxin (homoYTX). Our results support the notion that there is significant intra-specific variability in Protoceratium reticulatum and the biogeography of the different ribotypes is consistent with specific ecological preferences.

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Wang Na, Mertens Kenneth, Krock Bernd, Luo Zhaohe, Derrien Amelie, Pospelova Vera, Liang Yubo, Bilien Gwenael, Smith Kirsty F., de Schepper Stijn, Wietkamp Stephan, Tillmann Urban, Gu Haifeng (2019). Cryptic speciation in Protoceratium reticulatum (Dinophyceae): Evidence from morphological, molecular and ecophysiological data. Harmful Algae, 88, 101610 (15p.). Publisher's official version : , Open Access version :