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Integrative Taxonomy of the Pavlovophyceae (Haptophyta): a Reassessment

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Integrative Taxonomy of the Pavlovophyceae (Haptophyta): a Reassessment Protist, Vol. 162, 738–761, November 2011 http://www.elsevier.de/protis Published online date 28 June 2011 ORIGINAL PAPER Integrative Taxonomy of the Pavlovophyceae (Haptophyta): A Reassessment El Mahdi Bendifa,b,1, Ian Proberta,2, Annie Hervéc, Chantal Billardb, Didier Gouxd, Christophe Lelongb, Jean-Paul Cadoretc, and Benoît Vérona,b,3 aUniversité de Caen Basse-Normandie, Algobank-Caen, IFR 146, 14032 Caen, France bUniversité de Caen Basse-Normandie, UMR 100 PE2 M - IFREMER, 14032 Caen, France cIFREMER, Laboratoire de Physiologie et Biotechnologie des Algues, rue de l’Ile d’Yeu, BP21105, 44311 Nantes, France dUniversité de Caen Basse-Normandie, Centre de Microscopie Appliquée à la Biologie, IFR 146, 14032 Caen, France Submitted October 18, 2010; Accepted March 15, 2011 Monitoring Editor: Barry S. C. Leadbeater. The Pavlovophyceae (Haptophyta) contains four genera (Pavlova, Diacronema, Exanthemachrysis and Rebecca) and only thirteen characterised species, several of which are important in ecological and eco- nomic contexts. We have constructed molecular phylogenies inferred from sequencing of ribosomal gene markers with comprehensive coverage of the described diversity, using type strains when avail- able, together with additional cultured strains. The morphology and ultrastructure of 12 of the described species was also re-examined and the pigment signatures of many culture strains were determined. The molecular analysis revealed that sequences of all described species differed, although those of Pavlova gyrans and P. pinguis were nearly identical, these potentially forming a single cryptic species complex. Four well-delineated genetic clades were identified, one of which included species of both Pavlova and Diacronema. Unique combinations of morphological/ultrastructural characters were iden- tified for each of these clades. The ancestral pigment signature of the Pavlovophyceae consisted of a basic set of pigments plus MV chl cPAV, the latter being entirely absent in the Pavlova + Diacronema clade and supplemented by DV chl cPAV in part of the Exanthemachrysis clade. Based on this com- bination of characters, we propose a taxonomic revision of the class, with transfer of several Pavlova species to an emended Diacronema genus. The evolution of the class is discussed in the context of the phylogenetic reconstruction presented. © 2011 Elsevier GmbH. All rights reserved. Key words: 18S rDNA; Haptophyta; Pavlovophyceae; phylogeny; taxonomy; ultrastructure. Introduction The Haptophyta is a phylum of chlorophyll a + c 1Present address: CNRS-UMPC (Université Paris-06), UMR 7144, Groupe Plancton, Station Biologique de Roscoff, BP74, containing unicellular algae characterised by the 29682 Roscoff cedex, France presence of a unique filamentous appendage, the 2Present address: Roscoff Culture Collection, CNRS-UMPC haptonema, and comprising two distinct classes, (Université Paris-06), FR2424, Station Biologique de Roscoff, the Prymnesiophyceae Hibberd emend. Cavalier- BP74, 29682 Roscoff cedex, France Smith and the Pavlovophyceae (Cavalier-Smith) 3Corresponding author; fax +33 2 31 56 53 46 e-mail [email protected] (B. Véron). Green et Medlin. The erection of a third class of © 2011 Elsevier GmbH. All rights reserved. doi:10.1016/j.protis.2011.05.001 Integrative Taxonomy of the Pavlovophyceae (Haptophyta): A Reassessment 739 haptophytes was recently proposed based exclu- (Green 1980) or modified hairs (Cavalier-Smith sively on molecular data (Shi et al. 2009). The 1994), often form a dense investment on the longer Prymnesiophyceae contains ca. 400 described flagellum together with fine hairs. The process of species including many well known taxa such mitosis in the Pavlovophyceae differs notably from as Phaeocystis, Chrysochromulina, Prymnesium that in the Prymnesiophyceae (Green and Hori and the coccolithophores that can periodically 1988; Hori and Green 1994). The Pavlovophyceae form blooms in coastal and oceanic environ- are also known to synthesise certain specific sterols ments and thereby have a highly visible impact on and conjugates, the pavlovols (Véron et al. 1996; marine ecosystem functioning, global biogeochem- Volkman et al. 1997) and a unique photosynthetic ical cycles and global climate change (Moestrup pigment (Van Lenning et al. 2003). 1994). By contrast, the Pavlovophyceae contains Due to their trophic, economic and phyloge- only 13 described species that inhabit littoral, brack- netic importance, the Pavlovophyceae represent ish water and sometimes freshwater environments, a highly relevant model for genomic studies. and which have consequently not received a great Pavlova lutheri was part of the protist EST program deal of attention in the context of global issues. (http://megasun.bch.umontreal.ca/pepdb/pep.html, The Pavlovophyceae is nevertheless a class Tonon et al. 2005) and the genome size and struc- of interest for a number of reasons, not least ture of two species, P. gyrans and Diacronema sp., because it is seemingly a very common compo- have been estimated using Pulse Field Gel Elec- nent of near coastal phytoplankton communities in trophoresis with a view to the possibility of initiating widespread locations. The Pavlovophyceae synthe- a full genome sequencing project (Nosenko et al. size long chain polyunsaturated fatty acids such 2007). as docosahexaenoic (DHA) and eicosapentaenoic The 13 described species of Pavlovophyceae (EPA) acids and certain species, notably Pavlova are classified in a single subclass, the Pavlovophy- lutheri and P. gyrans, are extensively used as feed- cideae Cavalier-Smith, one order, the Pavlovales stocks in the aquaculture of bivalves, crustaceans Green, and one family, the Pavlovaceae Green, that and fish (Gayral 1980; Green 1975; Meireles et al. is composed of 4 genera: Diacronema (Prauser) 2003; Ponis et al. 2006). The separation of the two Green et Hibberd, Exanthemachrysis Lepailleur, known haptophyte classes is genetically well sup- Pavlova (Butcher) Green and Rebecca Green ported with 6% divergence in 18S rDNA phylogeny (Table 1). Butcher (1952) erected the genus (Edvardsen et al. 2000). Using molecular clocks Pavlova with the description of P.gyrans as the type calibrated with the coccolithophore fossil record, species. Based mostly on TEM ultrastructural stud- the time of divergence of these two classes of the ies of culture strains, new species were sporadically Haptophyta has been estimated at between 805 described until 1992. The last major taxonomic sur- and 1000 million years ago (de Vargas et al. 2007; vey of the class was conducted over a quarter of Liu et al. 2010; Medlin et al. 2008). This deep a century ago (Green 1980), when a determina- divergence provides a model of key interest for evo- tion key was proposed for the three existing genera, lutionary studies on the origin of the Haptophyta Diacronema, Pavlova and Exanthemachrysis. More and the early radiation of eukaryotes. recently, the availability of 18S rDNA sequences for In this context, the Pavlovophyceae are generally a sub-set of pavlovophycean taxa led to the transfer perceived to be representative of the primitive state, of two Pavlova species to the new genus Rebecca with characteristics likely to be related to those of (Edvardsen et al. 2000). In addition, analysis of the ancestral haptophyte. Structural features com- photosynthetic pigment profiles of a selection of mon to all or most members of the Pavlovophyceae species demonstrated that such profiles are phylo- that distinguish them from the Prymnesiophyceae genetically informative (Van Lenning et al. 2003). include the markedly anisokont nature of the In both of these latter studies, however, a com- heterodynamic flagella and the relatively simple plete reinvestigation of the class was not carried arrangement of microtubular and fibrous roots of out. Undescribed species are frequently observed the pavlovophycean flagellar-haptonematal basal in miscellaneous samples (Gayral 1980) and the complex (Green and Hori 1994). This flagel- majority of the main microalgal culture collections lar arrangement results in pavlovophycean cells hold several unidentified Pavlovophyceae strains exhibiting a characteristic swimming movement. In that are likely to include new species. addition, pavlovophycean scales, when present, Using type cultures when still available (11 of the consist of small dense bodies in contrast to the plate 13 described species), we conducted a combined scales of the Prymnesiophyceae. These so-called morphological, pigmentary and molecular genetic ‘knob scales’, considered to be modified scales analysis in order to assess the validity of the current 740 E.M. Bendif et al. Table 1. Actual Pavlovophyceae taxonomy and authorities. Haptophyta Hibberd Cavalier-Smith ex Edvardsen et Eikrem in Edvardsen et al. 2000 Pavlovophyceae Cavalier-Smith ex Green et Medlin in Edvardsen et al. 2000 Pavlovales Green 1976 Pavlovaceae Green 1976 Diacronema (Prauser) Green et Hibberd 1977 Diacronema vlkianum (Prauser) Green et Hibberd 1977 Exanthemachrysis Lepailleur 1970 Exanthemachrysis gayraliae Lepailleur 1970 Pavlova Butcher 1952 Pavlova calceolata van der Veer 1976 Pavlova ennorea van der Veer et Leewis 1977 Pavlova granifera (Mack) Green 1973 Pavlova gyrans (Butcher) Green et Manton 1970 Pavlova lutheri (Droop) Green 1975 Pavlova noctivaga (Kalina 1970) van der Veer et Leewis 1977 Pavlova pinguis Green 1967 Pavlova virescens Billard 1976 Pavlova viridis Tseng, Chen et Zhang 1992 Rebecca Green 2000 Rebecca helicata (van der Veer) Green 2000 Rebecca salina
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