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Absence of Co-Phylogeny Indicates Repeated Diatom Capture in Dinophytes Hosting a Tertiary Endosymbiont

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Absence of Co-Phylogeny Indicates Repeated Diatom Capture in Dinophytes Hosting a Tertiary Endosymbiont Org Divers Evol (2018) 18:29–38 https://doi.org/10.1007/s13127-017-0348-0 ORIGINAL ARTICLE Absence of co-phylogeny indicates repeated diatom capture in dinophytes hosting a tertiary endosymbiont Anže Žerdoner Čalasan1 & Juliane Kretschmann1 & Marc Gottschling1 Received: 28 July 2017 /Accepted: 26 October 2017 /Published online: 18 November 2017 # Gesellschaft für Biologische Systematik 2017 Abstract Tertiary endosymbiosis is proven through Keywords Chloroplast . Dinoflagellates . Dinotoms . dinophytes, some of which (i.e. Kryptoperidiniaceae) have Endosymbiosis . Evolution . Mutualism engulfed diatom algae containing a secondary plastid. Chloroplasts are usually inherited together permanently with the host cell, leading to co-phylogeny. We compiled a diatom Introduction sequence data matrix of two nuclear and two chloroplast loci. Almost all endosymbionts of Kryptoperidiniaceae found their As one of the important groups of unicellular eukaryotic life closest relatives in free-living diatoms and not in other forms, Dinophyceae (or Dinoflagellata under zoological no- harboured algae, rejecting co-phylogeny and indicating that menclature) are nothing less but diverse from every single resident diatoms were taken up by dinophytes multiple times point of view (Morden and Sherwood 2002; Pochon et al. independently. Almost intact ultrastructure and insignificant 2012; Gottschling and McLean 2013; Burki 2014). Together genome reduction are supportive for young, if not recent with Ciliata and Apicomplexa (= Sporozoa), Dinophyceae events of diatom capture. With their selective specificity on belong to Alveolata and are a well-supported monophyletic the one hand and extraordinary degree of endosymbiotic flex- group based on molecular data and numerous unique anatom- ibility on the other hand, dinophytes hosting diatoms share ical characteristics (Harper et al. 2005; Medlin and Fensome more traits with lichens or facultatively phototrophic ciliates 2013; Keeling et al. 2014; Janouškovec et al. 2017). Compared than with green algae and land plants. Time estimates indicate to all other eukaryotes, the genome of dinophytes is highly the dinophyte lineages as consistently older than the hosted unusual with respect to structure and regulation (Moreno Díaz diatom lineages, thus also favouring a repeated uptake of en- de la Espina et al. 2005; Wisecaver and Hackett 2011). The dosymbionts. The complex ecological role of dinophytes nucleus contains chromosomes that are permanently condensed employing a variety of organismic interactions may explain throughout cell development (displaying a liquid crystalline their high potential and plasticity in acquiring a great diversity state: Rill et al. 1989) except in the DNA replication stage of plastids. (Dodge 1966; Rizzo 2003). Dinophyte morphology also ex- hibits unique traits such as the coiled transverse flagellum asso- ciated with a transverse groove termed the ‘cingulum’ (Taylor 1980; Fensome et al. 1999; Leander and Keeling 2004; Electronic supplementary material The online version of this article Okamoto and Keeling 2014). (https://doi.org/10.1007/s13127-017-0348-0) contains supplementary Despite the fact that they represent only about a half of all material, which is available to authorized users. dinophyte species (Taylor et al. 2008), photosynthetically ac- tive taxa have gained chloroplasts in numerous advanced * Marc Gottschling [email protected] ways (Gagat et al. 2014; Dorrell and Howe 2015), excluding the most basic primary engulfment (primary endosymbiosis). 1 Department Biologie, Systematische Botanik und Mykologie, The most common and widespread chloroplast type found in GeoBio-Center, Ludwig-Maximilians-Universität München, dinophytes indicates a secondary engulfment event (second- Menzinger Str. 67,, 80 638 Munich, Germany ary endosymbiosis) of a red algae (Dodge 1989; Jeffrey 1989; 30 Žerdoner Čalasan A. et al. Janouškovec et al. 2017). Some dinophyte predators capture Takano et al. 2008) surrounded by a triple-membrane structure additional plastids of their prey and keep them up to several (Horiguchi and Pienaar 1994). weeks in an evolutionary phenomenon known as All Kryptoperidiniaceae constitute a monophyletic group kleptoplastidy (Schnepf and Elbrächter 1999; Stoecker 1999; as a part of the Peridiniales (Pienaar et al. 2007; Takano et al. Gast et al. 2007; Takano et al. 2014). Other dinophytes have 2008; Gottschling and McLean 2013; Janouškovec et al. taken up a different endosymbiont in a more permanent way 2017; Price and Bhattacharya 2017; Kretschmann et al. in and have brought the endosymbiosis even further to a tertiary press), but their endosymbionts originate from at least three level by engulfing organisms such as diatoms, which already different diatom lineages. The currently accepted scenario de- possessed secondarily gained chloroplasts (Keeling 2004, scribes the single acquisition of a Nitzschia Hassall-related 2010; Hehenberger et al. 2014). organism (present today in Durinskia Carty & El.R.Cox, An example for a chloroplast replacement at a second- Galeidinium Tam. & T.Horig. and Kryptoperidinium ary level of endosymbiosis is Lepidodinium M.Watan., Er.Lindem.: Tamura et al. 2005; Pienaar et al. 2007; Zhang S.Suda, I.Inouye et al. (Gymnodiniaceae s.str.) enclosing et al. 2011a) that has been replaced by either Cyclotella a green alga (Kamikawa et al. 2015). Tertiary endosym- (Kütz.) Bréb.-related (in freshwater Unruhdinium biosis, primarily found in dinophytes, is even more com- Gottschling: Takano et al. 2008; Zhang et al. 2011b;You plex from the symbiont’s point of view. Tertiary plastids et al. 2015)orbyChaetoceros Ehrenb.-related symbionts (in are present in, for example, species of Dinophysis Ehrenb. Blixaea Gottschling: Horiguchi and Takano 2006)intwofur- (Dinophysaceae) possessing cryptomonad-derived sym- ther evolutionary steps. The phenomenon of monophyletic bionts separated from the host by two membranes hosts and polyphyletic symbionts has thus been explained (Schnepf and Elbrächter 1988; Garcia-Cuetos et al. by ‘serial replacement’ (Horiguchi and Takano 2006; 2010). Taxa such as Karenia Gert Hansen & Moestrup Takano et al. 2008) of an already engulfed diatom. However, and Karlodinium J.Larsen (Brachidiniaceae) possess chlo- this idea has been developed based on single-locus analyses roplasts that have originated from haptophyte algae with a rather limited diatom taxon sample. (Hansen et al. 2003;Gastetal.2007). Endosymbiont While preparing a similar study of our own, we took inter- reduction is severe in this group, and the three- est in the study of Yamada et al. (2017). The study advocates membrane layer as part of the chloroplast is the only serial replacement, considering a few diatom acquisition structure left of the engulfed organism. An ancestral events, after which endosymbionts are established, maintained peridinin chloroplast may have co-existed with the newly and inherited. Subsequently, endosymbionts are in permanent gained chloroplast of haptophyte origin but has been lost association with the host cell and should thus find their closest eventually (Nosenko et al. 2006;Patronetal.2006; relatives among other endosymbionts. Co-phylogenetic struc- Takano et al. 2014). However, there is no ultrastructural tures should therefore be present between separately derived evidence that Brachidiniaceae have ever possessed two tress of diatoms and their hosting dinophytes. This hypothesis different functional chloroplasts. is not explicitly phrased in Yamada et al. (2017), although it is Based on ultrastructural analyses of those dinophytes the necessary conceptual basis to understand the origin of harbouring diatoms (Kryptoperidiniaceae, commonly referred dinophytes harbouring tertiary endosymbionts and the dy- to as ‘dinotoms’: Imanian et al. 2010), the endosymbiont namics of this (endo)symbiont/host association. Our data pro- keeps not only its photosynthesis machinery but also the func- vide evidence for a repeated acquisition of endosymbiotic tional nucleus with protein encoding genes, a substantial diatoms through their evolutionary history and for the rejec- amount of cytosol and mitochondria (McEwan and Keeling tion of overall co-phylogeny. Tertiary endosymbiosis present 2004; Imanian and Keeling 2007; Imanian et al. 2012; Takano in Kryptoperidiniaceae may have happened recently in com- et al. 2008). However, numerous studies also show a loss of parison to many other algal groups, in which severe reduction motility, cell wall and mitotic division (Dodge 1971; Tomas has taken place leaving behind only the chloroplasts and their and Cox 1973). Despite this major autonomy and minimal membranes. reduction, the resident diatom is present in the host cell in all stages of development, which indicates synchrony of life his- tory between both host and endosymbiont (Figueroa et al. Materials and methods 2009). Moreover, diatom mitochondria seem to be almost un- affected by endosymbiosis, retaining nearly all of their char- From the dinophyte endosymbionts of Durinskia oculata acteristics and functions (Imanian and Keeling 2007;Imanian (F.Stein) Gert Hansen & Flaim and Kryptoperidinium sp., et al. 2012). Engulfed diatoms due to tertiary endosymbiosis we sequenced the nucleomorph small subunit (SSU) and replace the ancestral peridinin chloroplast, whose remnants Internal Transcribed Spacers (ITS) and plastid rbcLlocias are considered to be a unique form of an eyespot (Dodge previously described (Kretschmann et al. in press). In order 1983; Horiguchi
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