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Review
. 2014 Mar 28:5:112.
doi: 10.3389/fmicb.2014.00112. eCollection 2014.

Morphology, phylogeny, and ecology of the aphelids (Aphelidea, Opisthokonta) and proposal for the new superphylum Opisthosporidia

Sergey A Karpov  1 , Maria A Mamkaeva  2 , Vladimir V Aleoshin  3 , Elena Nassonova  4 , Osu Lilje  5 , Frank H Gleason  5
Affiliations
Review

Morphology, phylogeny, and ecology of the aphelids (Aphelidea, Opisthokonta) and proposal for the new superphylum Opisthosporidia

Sergey A Karpov et al. Front Microbiol. .

Abstract

The aphelids are a small group of intracellular parasitoids of common species of eukaryotic phytoplankton with three known genera Aphelidium, Amoeboaphelidium, and Pseudaphelidium, and 10 valid species, which form along with related environmental sequences a very diversified group. The phyla Microsporidia and Cryptomycota, and the class Aphelidea have recently been considered to be a deep branch of the Holomycota lineage forming the so called the ARM-clade which is sister to the fungi. In this review we reorganize the taxonomy of ARM-clade, and establish a new superphylum the Opisthosporidia with three phyla: Aphelida phyl. nov., Cryptomycota and Microsporidia. We discuss here all aspects of aphelid investigations: history of our knowledge, life cycle peculiarities, the morphology (including the ultrastructure), molecular phylogeny, ecology, and provide a taxonomic revision of the phylum supplied with a list of species. We compare the aphelids with their nearest relatives, the species of Rozella, and improve the diagnosis of the phylum Cryptomycota.

Keywords: Aphelida; Cryptomycota; Microsporidia; Opisthosporidia; Rozella; ecology; molecular phylogeny; ultrustucture.

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Figures

FIGURE 1
FIGURE 1
Position of Amoeboaphelidium protococcarum on the tree inferred from rDNA analyses by Bayesian and ML methods (after: Karpov et al., 2013). PhyloBayes tree topology was calculated from an alignment of 144 sequences and 4,384 nucleotide characters. Node support values are given as follows: Bayesian posterior probabilities (PhyloBayes/MrBayes) followed by bootstrap values (RAxML). We used the GTR + CAT model without partition by genes for PhyloBayes calculations and the same model with partition by genes for RAxML calculations. The GTR + I + Γ12 model was used for MrBayes calculations. Filled circles indicate that all support values are above 98%; empty circles indicate that at least one support value is above 98%. Shown in gray are support values for clades not included in the consensus trees. Symbols in the inset indicate habitats for environmental sequences. Scale bar indicates substitutions per site.
FIGURE 2
FIGURE 2
Generalized life cycle of aphelids. Aphelidium (Aph), Amoeboaphelidium (Am) and Pseudaphelidium (Ps), distinguished by zoospore structure and development. (A) Zoospore encystment (c) on the host surface, (B) propagule penetration into the host, (C) trophic amoeba with nucleus (blue) and residual body (red) engulfs host cytoplasm, (D) multinuclear plasmodium (yellow) totally replaced the host, contains several nuclei (blue) and central vacuole with residual body (red), (E) plasmodium divides producing uninuclear cells, (F) mature zoospores released from the empty host cell, (G) precursory stage to the resting spore with nuclei in the center, (H) resting spore with ejected residual body. Dotted line shows conceivable way from resting spore to divided plasmodium. Colors: green, host (alga) cytoplasm; yellow, parasitoid cytoplasm; blue, nucleus; red, residual body.
FIGURE 3
FIGURE 3
Main stages of the life cycle of Aphelidium sp. parasitizing on Tribonema gayanum CALU- 20. Living cells observed under DIC. (A) Zoospore (zo) before attachment to the host (ho) and cysts (cy) on the surface of Tribonema filament. Insert – multiple infection at lower magnification. (B) Plasmodium with central vacuole (cv) and residual body (rb). (C) multicellular stage of parasitoid with rb at the periphery (arrows show separate cells). (D) mature zoospores with flagella and residual body in the empty host cell. (E) Free-swimming zoospore at high magnification. Scale bar: A–D, 10 μm, insertion in A, 15 μm, E, 8 μm.
FIGURE 4
FIGURE 4
Amoeboid zoospores of Amoeboaphelidium protococcarum. Living cells observed using phase contrast. (A–C) Strain x-1 CALU, (D–G) strain x-5 CALU. (H) Amoeba of Amoeboaphelidium protococcarum strain x-5 CALU on ultrathin longitudinal section. (D–H) After: Karpov et al. (2013). f and black arrows, filopodia often producing by broad anterior pseudopodium (ps, white arrow), m, mitochondrium, n, nucleus, arrowheads show pseudocilium. Scale bars: A–C, 3 μm; D–G, 2 μm; H, 1 μm.
FIGURE 5
FIGURE 5
Phylogenetic and taxonomic summary of early diverged groups of Holomycota.
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