Morphology, Phylogeny, and Ecology of the Aphelids (Aphelidea, Opisthokonta) and Proposal for the New Superphylum Opisthosporidia
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REVIEW ARTICLE published: 28 March 2014 doi: 10.3389/fmicb.2014.00112 Morphology, phylogeny, and ecology of the aphelids (Aphelidea, Opisthokonta) and proposal for the new superphylum Opisthosporidia Sergey A. Karpov1,2 *, Maria A. Mamkaeva 2 ,Vladimir V.Aleoshin 3 , Elena Nassonova 2,4 , Osu Lilje 5 and Frank H. Gleason 5 1 Zoological Institute, Russian Academy of Sciences, St. Petersburg, Russian Federation 2 St. Petersburg State University, St. Petersburg, Russian Federation 3 A. N. Belozersky Institute for Physico-Chemical Biology, Lononosov Moscow State University, Moscow, Russian Federation 4 Institute of Cytology, Russian Academy of Sciences, St. Petersburg, Russian Federation 5 School of Biological Sciences F07, University of Sydney, Sydney, NSW, Australia Edited by: The aphelids are a small group of intracellular parasitoids of common species of eukaryotic Télesphore Sime-Ngando, Centre phytoplankton with three known genera Aphelidium, Amoeboaphelidium, and Pseudaphe- National de la Recherche, France lidium, and 10 valid species, which form along with related environmental sequences a Reviewed by: very diversified group. The phyla Microsporidia and Cryptomycota, and the class Aphelidea Sigrid Neuhauser, Natural History Museum London, UK have recently been considered to be a deep branch of the Holomycota lineage forming Jean-François Mangot, University of the so called the ARM-clade which is sister to the fungi. In this review we reorganize Oslo, Norway the taxonomy of ARM-clade, and establish a new superphylum the Opisthosporidia with *Correspondence: three phyla: Aphelida phyl. nov., Cryptomycota and Microsporidia. We discuss here all Sergey A. Karpov, Zoological Institute, aspects of aphelid investigations: history of our knowledge, life cycle peculiarities, the Russian Academy of Sciences, St. Petersburg 199034, Russian morphology (including the ultrastructure), molecular phylogeny, ecology, and provide a Federation taxonomic revision of the phylum supplied with a list of species. We compare the aphelids e-mail: [email protected] with their nearest relatives, the species of Rozella, and improve the diagnosis of the phylum Cryptomycota. Keywords: Opisthosporidia, Aphelida, Cryptomycota, Microsporidia, Rozella, ultrustucture, molecular phylogeny, ecology INTRODUCTION This review focuses on the aphelids and discusses their phy- The aphelids are a small group of intracellular parasitoids of algae, logeny, life cycle, morphology, ecology, and their taxonomy. which are currently placed in the class Aphelidea (Gromov, 2000). Because of their close phylogenetic relationship and life cycle sim- The class Aphelidea includes two freshwater genera, Aphelidium ilarity (in contrast with the fast-evolving Microsporidia), we often and Amoeboaphelidium, and a marine genus, Pseudaphelidium. consider them in comparison with Cryptomycota. Indeed, the Although for a long time members of the class Aphelidea had aphelids have a life cycle similar to that of the Cryptomycota, but uncertain affinities, the phylogenetic position of this class has been are parasitoids of algae, and not of zoosporic fungi and Oomycetes recently clarified by molecular phylogenetic analyses of Amoe- as are the known species of Rozella. boaphelidium protococcarum (Karpov et al., 2013). The aphelids belong to the supergroup Opisthokonta, which includes multicel- APHELID RELATIONSHIPS: HISTORICAL SKETCH lular animals and fungi, and a variety of unicellular organisms, Historical interpretations of the phylogenetic affinities of the aphe- which over the past decade the molecular phylogeny has been lids were thoroughly discussed by Gromov (2000). Therefore, we tied to each of the two following major clades (Paps et al., 2013). only highlight here some of the important points. The research The Metazoa, Choanoflagellata, and Mesomycetozoea now form on aphelids began in the 19th century when the genus Aphelidium the Holozoa (Torruella et al., 2012), whereas nucleariid amoebae, Zopf was first described (Zopf, 1885). 40 years later in 1925, Amoe- fungi, rozellids (Cryptomycota), aphelids, and microsporidia form boaphelidium Scherffel was described, and both these organisms the Holomycota (Liu et al., 2009; Lara et al., 2010; Jones et al., were treated as the Cienkowski’s “Monadinea” group, comprised 2011a; Karpov et al., 2013; Letcher et al., 2013). Recent molecu- of the extremely divergent “fungal animals” – organisms with a lar phylogeny analyses show that the class Aphelidea is sister to fungal-like life cycle, but having an amoeboid trophic stage (ref. both Microsporidia and Cryptomycota (Karpov et al., 2013). This in Gromov, 2000). In the 1950–1960s, the aphelids were included strongly argues in favor of the re-classification of Aphelidea at the in the order Proteomyxida or subclass Proteomyxidia within the phylum rank. All the three phyla form a separate branch sister to class Rhizopoda (Hall, 1953; Honigberg et al., 1964; Kudo, 1966). classical (“true”) fungi, which include Dikarya (Ascomycota and However, subsequently these protists were completely forgotten in Basidiomycota), paraphyletic Zygomycota, and Chytridiomycota classifications in later years (Levine et al., 1980; Karpov, 1990; Page sensu lato (Voigt et al., 2013). and Siemensma, 1991; Cavalier-Smith, 1993, 1996/1997). This is www.frontiersin.org March 2014 | Volume 5 | Article 112 | 1 Karpov et al. Morphology, phylogeny, ecology, and taxonomy of aphelids difficult to understand because during the 1960s and 1970s a num- LIFE CYCLES ber of articles were written on Aphelidium and Amoeboaphelidium The complex life cycles of Aphelidium, Amoeboaphelidium, and by Schnepf et al. (1971) and Gromov et al. (ref. in Gromov, 2000). Pseudaphelidium appear to be very similar to each other (Figure 2) By the end of the last century we knew much more about the life and superficially similar to those of many species of Chytrid- cycles, ultrastructure and biological peculiarities of several species iomycota with endobiotic development in their algal host cells of aphelids. Gromov (2000) reviewed this material and established (Gromov, 2000). a new class Aphelidea for Aphelidium Zopf, 1885, Amoeboaphelid- As an example, the Aphelidium opisthokont zoospore attaches ium Scherffel, 1925, and Pseudaphelidium Schweikert et Schnepf, to the host algae and encysts while losing its flagellum (Figure 3A). 1996. A cyst germinates and penetrates the host cell wall with an infec- Until recently, the relationship between the aphelids and fungi tion tube. The posterior vacuole appears in the cyst, enlarges, was unclear. Cavalier-Smith (1998) suggested that the genus and then pushes the contents of the cyst into the interior of Aphelidium belongs to the opisthokonts because of their pos- the host cell through the infection tube (Figures 2 and 3A). teriorly directed uniflagellate zoospores and flat mitochondrial The parasitoid becomes the intracellular phagotrophic amoeba cristae. Gromov (2000) placed the class Aphelidea in the phy- which engulfs the host cytoplasm with pseudopodia and trans- lum Rhizopoda sensu lato on the basis of the amoeboid nature of ports the food into a central digestive vacuole. The parasitoid the trophozoite stage, despite an unpublished 18S rRNA partial grows forming an endobiotic plasmodium with residual body sequence of Amoeboaphelidium protococcarum which suggested a while it totally consumes the cytoplasm of the host cell (Figures 2 relationship with Choanozoa (Pinevich et al., 1997). Later Kar- and 3B). A multinucleate plasmodium is formed with a large cen- pov (Adl et al., 2005) transferred the class Aphelidea into the tral vacuole and a residual excretory body. The parasitoid does not phylum Mezomycetozoea based on the preliminary 18S rRNA form its own sporangium wall; rather it uses the host cell walls molecular phylogeny of Aphelidium. In addition to these classi- as the sporangium wall (Figure 3C). The mature plasmodium fications based on the 18S rRNA marker, aphelids were placed then divides into a number of uninucleated cells (Figures 2 and within Ichthyosporea based on their parasitic nature (Shalchian- 3C,D). After maturation, the uniflagellated zoospores of Aphe- Tabrizi et al., 2008), and then, based on their morphology and lidium are released from the empty host cell through the hole lifestyle, as a “new” order Aphelidida, class Rozellidea, in the made previously by the infection tube and infect other algae new subphylum Paramycia Cavalier-Smith (2013) of the phylum (Figures 2 and 3D,E). Choanozoa Cavalier-Smith, 1981 (Cavalier-Smith, 2013). The cre- All known aphelids can produce multiple infections (Figures 2 ation of a “new”Aphelidida order was unjustified, since that order and 3). In the case of Amoeboaphelidium, several amoebae grow had already been established by Gromov (2000) earlier. separately in the infected alga but later fuse into a multinucleate Previous classifications attempts based on 18S rRNA par- cell, forming a single plasmodium in each infected cell (Gromov tial gene sequences were affected by the limited resolution of and Mamkaeva, 1968). this marker for the eukaryotic tree. Only recently the molec- Sometimes giant multinucleate amoebae are released along ular phylogeny of Amoeboaphelidium protococcarum (strain x- with the uninucleate amoebae from the sporangium (Gromov and 5 CALU), based on five genes (RPB1, RPB2, 18S, 28S, and Mamkaeva, 1968). The origin of these giant amoebae is not clear, 5.8S rRNA), unambiguously showed that the aphelids branch but they might result from the incomplete