Prorocentrum rivalis sp. nov. (Dinophyceae) and its phylogenetic affinities inferred from analysis of a mixed morphological and LSU rRNA data set

Abstract

A new freshwater epiphytic Prorocentrum species, Prorocentrum rivalis, from the temperate region of the Haute-Vienne, France, is described. This species is the third freshwater species identified among approximately 60 marine Prorocentrum species. This new species is described using scanning electron microscope and phylogenetic analyses by a polyphasic approach (LSU rRNA sequences combined with 9 morphological characters). The phylogenetic analysis attests that P. rivalis is close to other planktonic freshwater species and the freshwater Prorocentrum clade is evolutionarily derived from an epiphytic freshwater prorocentroid ancestor. The unique marine species in the freshwater clade results from an ecophysiological reversion. P. rivalis differs from other epiphytic taxa by its rarity, its temperate distribution and its ecophysiological needs. The phylogeny confirms also that all planktonic Prorocentrum species are evolutionarily derived from epiphytic/benthic ancestors.

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References

  1. Aligizaki K., Nikolaidis G., Katikou P., Baxevanis A.D. & Abatzopoulos T.J. 2009. Potentially toxic ephytic Prorocentrum (Dinophyceae) species in Greek coastal waters. Harmful Algae 8: 299–311.

    Article  CAS  Google Scholar 

  2. Berrendero E., Perona E. & Mateo P. 2008. Genetic and morphological characterization of Rivularia and Calothrix (Nostocales, Cyanobacteria) from running water. Int. J. Syst. Evol. Microbiol. 58: 447–460.

    PubMed  Article  CAS  Google Scholar 

  3. Cameron S.A. & Williams P.H. 2003. Phylogeny of bumble bees in the New World subgenus Fervidobombus (Hymenoptera: Apidae): congruence of molecular and morphological data. Mol. Phylogenet. Evol. 28: 552–563.

    PubMed  Article  CAS  Google Scholar 

  4. Cohen-Fernandez E.J., Meave Del Castillo E., Salgado Ugarte I.H. & Pedroche F.F. 2006. Contribution of external morphology in solving a species complex: The case of Prorocentrum micans, Prorocentrum gracile and Prorocentrum sigmoides (Dinoflagellata) from the Mexican Pacific Coast. Phycological Res. 54: 330–340.

    Article  Google Scholar 

  5. Cortés-Altamirano R. & Sierra-Beltrán A.P. 2003. Morphology and taxonomy of Prorocentrum mexicanum and reinstatement of Prorocentrum rhathymum (Dinophyceae). J. Phycology 39: 221–225.

    Article  Google Scholar 

  6. Croome R.L. & Tyler P.A. 1987. Prorocentrum playfairi and Prorocentrum foveolata, two new Dinoflagellates from Australian freshwaters. Eur. J. Phycology 22: 67–75.

    Article  Google Scholar 

  7. Faust M.A. 1990. Morphologic details of six benthic species of Prorocentrum (Pyrrophyta) from a mangrove island, twin cays, Belize, including two new species. J. Phycology 26: 548–558.

    Article  Google Scholar 

  8. Faust M.A. 1993. Prorocentrum belizeanum, Prorocentrum elegans and Prorocentrum caribbaeum, three new benthic species (Dinophyceae) from a mangrove island Twin Cays, Belize. J. Phycology 29: 100–107.

    Article  Google Scholar 

  9. Faust M.A. 1994. Three new benthic species of Prorocentrum (Dinophyceae) from Carrie Bow Cay, Belize: P. sabulosum sp. nov., P. sculptile sp. nov., and P. arenarium sp. nov. J. Phycology 30: 755–763.

    Article  Google Scholar 

  10. Faust M.A. 2008. Prorocentrum levis, a new benthic species (Dinophyceae) from a mangrove island, Twin Cays, Belize. J. Phycology 44: 232–240.

    Article  CAS  Google Scholar 

  11. Felsenstein J. 1989. PHYLIP — Phylogeny Inference Package (Version 3.2). Cladistics 5: 164–166.

    Google Scholar 

  12. Fukuyo Y. 2004. Biological Character of Red-Tide Organisms, pp. 61–178. In: Okaichi T. (ed), Red Tides, Terra Scientific Publishing Company, Tokyo.

    Google Scholar 

  13. Giribet G. 2010. A new dimension in combining data? The use of morphology and phylogenomic data in metazoan systematics. Acta Zool. 91: 11–19.

    Article  Google Scholar 

  14. Grzebyk D., Sako Y. & Berland B. 1998. Phylogenetic analysis of nine species of Prorocentrum (Dinophyceae) inferred from 18S ribosomal DNA sequences, morphological comparisons and description of Prorocentrum panamensis, sp. nov. J. Phycology 34: 1055–1068.

    Article  CAS  Google Scholar 

  15. Helbling E.W., Buma A.G.J., van de Poll W., Fernández Zenoff M.V. & Villafańe V.E. 2008. UVR-induced photosynthetic inhibition dominates over DNA damage in marine dinoflagellates exposed to fluctuating solar radiation regimes. J. Exp. Mar. Biol. Ecol. 365: 96–102.

    Article  CAS  Google Scholar 

  16. Hernández-Becerril D.U., Cortés Altamirano R. & Alonso R.R. 2000. The dinoflagellate genus Prorocentrum along the coasts of the Mexican Pacific. Hydrobiologia 418: 111–121.

    Article  Google Scholar 

  17. Hoppenrath M. & Leander B.S. 2008. Morphology and molecular phylogeny of a new-marine sand-dwelling Prorocentrum species, P. tsawwassenense (Dinophyceae, Prorocentrales), from British Columbia, Canada. J. Phycology 44: 451–466.

    Article  Google Scholar 

  18. Kearney M. 2002. Fragmentary taxa, missing data, and ambiguity: Mistaken assumptions and conclusions. Systemat. Biol. 51: 369–381.

    Article  Google Scholar 

  19. Krakhmalnyy A.F. 2005. Prorocentrum dentatum — New for the Black Sea species of Dinoflagellata. Vestnik Zoologii 39: 61–64.

    Google Scholar 

  20. Litaker R.W., Tester P.A., Colorni A., Levy M.G. & Noga E.J. 1999. The phylogenetic relationship of Pfiesteria piscicida, Cryptoperidiniopsoid sp., Amyloodinium ocellatum and a Pfiesteria-like dinoflagellate to other dinoflagellates and apicomplexans. J. Phycology 35: 1379–1389.

    Article  Google Scholar 

  21. Lu D. & Goebel J. 2001. Five red tide species in genus Prorocentrum including the description of Prorocentrum donghaiense Lu sp. nov. from the East China Sea. Chin. J. Oceanol. Limnol. 19: 337–344.

    Article  Google Scholar 

  22. Lu D., Goebel J., Qi Y., Zou J., Han X., Gao Y. & Li Y. 2005. Morphological and genetic study of Prorocentrum donghaiense Lu from the East China Sea, and comparison with some related Prorocentrum species. Harmful Algae 4: 493–505.

    Article  CAS  Google Scholar 

  23. Luria S.M. & Kinney J.A. 1970. Underwater vision. Science 167: 1454–1461.

    PubMed  Article  CAS  Google Scholar 

  24. Morton S.L. 1998. Morphology and toxicology of Prorocentrum faustiae sp. nov., a toxic species of non-planktonic Dinoflagellate from Heron Island, Australia. Botanica Marina 41: 565–569.

    Article  Google Scholar 

  25. Morton S.L., Faust M.A., Fairey E.A. & Moeller P.D.R. 2002. Morphology and toxicology of Prorocentrum arabianum sp. nov., (Dinophyceae) a toxic planktonic dinoflagellate from the Gulf of Oman, Arabian Sea. Harmful Algae 1: 393–400.

    CAS  Google Scholar 

  26. Murray S., Flř Jřrgensen M., Ho S.Y.W., Patterson D.J. & Jermiin L.S. 2005. Improving the analysis of dinoflagellate phylogeny based on rDNA. Protist 156: 269–286.

    PubMed  Article  CAS  Google Scholar 

  27. Murray S., Ip C.L.C, Moore R., Nagahama Y. & Fukuyo Y. 2009. Are Prorocentroid Dinoflagellates monophyletic ? A study of 25 species based on nuclear and mitochondrial genes. Protist 160: 245–264.

    PubMed  Article  CAS  Google Scholar 

  28. Murray S., Nagahama Y. & Fukuyo Y. 2007. Phylogenetic study of benthic, spine-bearing prorocentroids, including Prorocentrum fukuyoi sp. nov. Phycological Res. 55: 91–102.

    Article  CAS  Google Scholar 

  29. Noesis. 2005. Visilog6-Viewer. Version 6.404.

  30. Noesis, Crolles. Norell M.A. & Wheeler W.C. 2003. Missing entry replacement data analysis: A replacement approach to dealing with missing data in paleontological and total evidence data sets. J. Vertebr. Pal. 23: 275–283.

    Article  Google Scholar 

  31. Rengefors K., Laybourn-Parry J., Logares R., Marshall W.A. & Hansen G. 2008. Marine-derived dinoflagellates in Antarctic saline lakes: Community composition and annual dynamics. J. Phycology 44: 592–604.

    Article  CAS  Google Scholar 

  32. Saldarriaga J.F., Taylor F.J.R., Cavalier-Smith T., Menden-Deuer S. & Keeling P.J. 2004. Molecular data and the evolutionary history of dinoflagellates. Eur. J. Protist. 40: 85–111.

    Article  Google Scholar 

  33. Springer M.S., Teeling E.C., Madsen O., Stanhope M.J. & de Jong W.W. 2001. Integrated fossil and molecular data reconstruct bat echolocation. PNAS 98: 6241–6246.

    PubMed  Article  CAS  Google Scholar 

  34. Steidinger K.A. & Tangen K. 1996. Dinoflagellates, pp. 387–598. In: Tomas C.R. (ed), Identifying Marine Diatoms and Dinoflagellates, Academic Press, New York.

    Chapter  Google Scholar 

  35. Ten-Hage L., Turquet J., Quod J.P., Puiseux-Dao S. & Couté A. 2000. Prorocentrum borbonicum sp. nov. (Dinophyceae), a new toxic benthic dinoflagellate from the southwestern Indian Ocean. Phycologia 39: 296–301.

    Article  Google Scholar 

  36. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F. & Higgins D.G. 1997. The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl. Acids Res. 24: 4876–4882.

    Article  Google Scholar 

  37. Varga J., Frisvard J.C. & Samson R.A. 2007. Polyphasic taxonomy of Aspergillus section Candidi based on molecular, morphological and physiological data. Stud. Mycol. 59: 75–88.

    PubMed  Article  CAS  Google Scholar 

  38. Wenzel J.W. & Siddall M.E. 1999. Noise. Cladistics 15: 51–64.

    Article  Google Scholar 

  39. Wiens J.J. 1998. Does adding characters with missing data increase or decrease phylogenetic accuracy? Systemat. Biol. 47: 625–640.

    Article  CAS  Google Scholar 

  40. Wiens J.J. 2003. Missing data, incomplete taxa, and phylogenetic accuracy. Systemat. Biol. 52: 528–538.

    Article  Google Scholar 

  41. Wiens J.J. 2005. Can incomplete taxa rescue phylogenetic analyses from long-branch attraction? Systemat. Biol. 54: 731–742.

    Article  Google Scholar 

  42. Wiens J.J. 2006. Missing data and the design of phylogenetic analyses. J. Biomed. Inform. 39: 34–42.

    PubMed  Article  CAS  Google Scholar 

  43. Yli-Mattila T., Paavanen-Huhtala S., Bulat S.A., Alekhina I.A. & Nirenberg H.I. 2002. Molecular, morphological and phylogenetic analysis of the Fusarium avenaceum/F. arthrosporioides/F. tricinctum species complex — A polyphasic approach. Mycol. Res. 106: 655–669.

    Article  CAS  Google Scholar 

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Delmail, D., Labrousse, P., Crassous, P. et al. Prorocentrum rivalis sp. nov. (Dinophyceae) and its phylogenetic affinities inferred from analysis of a mixed morphological and LSU rRNA data set. Biologia 66, 418–424 (2011). https://doi.org/10.2478/s11756-011-0029-y

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Key words

  • Prorocentrum rivalis
  • epiphytic microalgae
  • LSU
  • phylogeny
  • polyphasic approach
  • SEM