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Protistology Molecular Phylogeny of Aphelidium Tribonemae Reveals Its Protistology 10 (3), 97–103 (2016) Protistology Molecular phylogeny of Aphelidium tribonemae reveals its sister relationship with A. aff. melosirae (Aphelida, Opisthosporidia) Sergey A. Karpov1,2, Maria A. Mamkaeva2, David Moreira3 and Purificacion López-García3 1 Zoological Institute, Russian Academy of Sciences, St. Petersburg 199034, Russia 2 St. Petersburg State University, St. Petersburg 199034, Russia 3 Ecologie Systematique Evolution, CNRS, Universite Paris-Sud, AgroParisTech, Universite Paris-Saclay, Orsay 91400, France | Submitted October 5, 2016 | Accepted November 10, 2016 | Summary Aphelids remain poorly known parasitoids of algae but have raised considerable interest due to their phylogenetic position at the base of Holomycota. Together with Cryptomycota and Microsporidia, they have been recently re-classified in the Opisthosporidia, which constitutes the sister group to the fungi within the Holomycota. Molecular environmental studies have revealed a diversity of aphelids, but only four genera have been described: Aphelidium, Amoeboaphelidium, Paraphelidium and Pseudaphelidium. Here, we describe the life cycle of a known representative of Aphelida, Aphelidium tribonemae, and provide the first 18S rRNA gene sequence obtained for this species. Molecular phylogenetic analysis indicates that Aphelidium tribonemae is sister to A. aff. melosirae and both form a monophyletic cluster, which is distantly related to both Paraphelidium with flagellated zoospores, and Amoebaphelidium with amoeboid zoospores. Key words: aphelids, Opisthosporidia, molecular phylogeny, Holomycota Introduction sequences from diverse ecosystems (Karpov et al., 2013, 2014a). The phyla Aphelida, Microsporidia The aphelids are a divergent group of intracel- and Rozellosporidia (Cryptomycota) form the lular parasitoids of green, yellow-green and diatom superphylum Opisthosporidia, the deepest branch algae (Gleason et al., 2014; Karpov et al., 2014a). of the Holomycota lineage, separated from the fungi The four known genera have different ecological (Karpov et al., 2014a; Letcher et al., 2015; Torruella preferences: Aphelidium, Amoeboaphelidium and et al., 2015). Not only does their phylogenetic Paraphelidium occur in freshwater and Pseudaphe- position place them as sister to true fungi, but lidium is found in marine environments. Although also several of their biological peculiarities do not with only these four described genera, the group conform with the classical definition of fungi. is highly diverse, including many environmental The most remarkable of those is that, unlike doi:10.21685/1680-0826-2016-10-3-4 © 2016 The Author(s) Protistology © 2016 Protozoological Society Affiliated with RAS 98 · Sergey A. Karpov et al. osmotrophic fungi, the trophonts of Aphelida and amplifying an excess of host genes, the aphelid 18S Rozellosporidia (but not Microsporidia, which rRNA gene was amplified by polymerase chain are extremely specialized derived parasites) engulf reaction (PCR) with the fungi-like specific primers the host cytoplasm by phagocytosis, like amoebae UF1 (5’-CGAATCGCATGGCCTTG) and AU4 (Gromov, 2000; Karpov et al., 2014a). (5’-RTCTCACTAAGCCATTC) (Kappe et al., Because of great interest in the aphelids, more 1996). PCR was carried out in 25 µl of reaction and more studies have been published in recent buffer, containing 1 µl of DNA, 1.5 mM MgCl2, years. At present, several strains have been studied dNTPs (10 nmol each), 20 pmol of each primer, by modern molecular methods: three strains of and 0.2 U of TaqPlatinum DNA polymerase Amoeboaphelidium: A. protococcarum: X-5 CALU (Invitrogen). PCR reactions consisted of 2 min (Karpov et al., 2013), FD95 (Letcher et al., 2015), denaturation at 94 °C; 35 cycles of a denaturation and A. occidentale FD01 (Letcher et al., 2013), a strain step at 94 °C for 15 s, a 30 s annealing step at 50°C of Aphelidium aff. melosirae P-1 CALU (Karpov et and an extension step at 72 °C for 2 min; and a al., 2014b) and three strains of the recently described final elongation step of 7 min at 72 °C. Negative genus and species Paraphelidium tribonemae (Karpov controls without template DNA were used at et al., 2016). Here, we report the morphological all amplification steps. We cloned the amplified and molecular phylogenetic study of the strain 18S rRNA gene fragments using the Topo TA X-102, which forms a sister branch to Aphelidium Cloning System (Invitrogen, Carlsbad, CA, USA) aff. melosirae and corresponds morphologically to following the manufacturer’s instructions. Clone Aphelidium tribonemae Scherffel 1925. inserts were PCR-amplified using flanking vector primers and inserts of the expected size (1,400 bp) were sequenced bidirectionally with vector primers Material and methods (Beckman Coulter Genomics, Takeley, UK). ISOLATION AND CULTIVATION OF APHELIDIUM TRIBONEMAE MOLECULAR PHYLOGENETIC ANALYSES The strain X-102 of Aphelidium tribonemae was The Aphelidium tribonemae 18S rDNA sequence isolated by M.A. Mamkaeva in 2012 from sample was aligned together with the sequences previously P-2 collected in the vicinity of the Kuty village, used in Karpov et al. (2014b) and Letcher et al. Kingisepp District, Leningrad Province, Russia. (2015) using Mafft (Katoh et al., 2002). The The strain was maintained in culture on Tribonema multiple alignment was then manually trimmed gayanum (strain 20 CALU) as the host. The to eliminate spuriously aligned sites. A total of culture of the host was grown on mineral medium 1,391 unambiguously aligned sites were retained to (KNO3, 2 g/L; KH2PO4, 0.3 g/L; MgSO4, 0.15 reconstruct a phylogenetic tree applying Maximum g/L; EDTA, 10 mg/L; FeSO4, 5 mg/L; NaBO3, 1.4 Likelihood (ML) methods with RAxML 8 (Stama- mg/L; (NH4)6Mo7O2, 4.1 mg/L; CaCl2, 0.6 mg/L; takis, 2014). The best tree was obtained out of 500 ZnSO4, 0.1 mg/L; CuSO4, 50 mg/L, Co(NO3)2, best tree searches applying a GTR+G+I model 20 mg/L) at room temperature in the presence of of nucleotide substitution, taking into account white light. After inoculation with the parasite, the a proportion of invariable sites, and a Gamma- cultures were incubated for 1–2 weeks to reach the shaped distribution of substitution rates with four maximum infection of host cells. Cells were then rate categories. Bootstrap values were calculated harvested and used directly for DNA extraction. with 500 non-parametric replicates with the same Light and DIC microscopy observations of living substitution model. The Aphelidium tribonemae 18S cultures were carried out using a Zeiss Axioplan rRNA sequence has been deposited in GenBank microscope equipped with black and white MRm with accession number KY129663. Axiocam camera. MOLECULAR ANALYSES Results We centrifuged 2 ml of infected Tribonema MOLECULAR PHYLOGENY culture and extracted DNA from pelleted cells with the DNA purification kit PowerSoil (MoBio) We amplified and sequenced a near-full 18S following the manufacturer’s instructions. To avoid rRNA gene from the strain X-102 of Aphelidium Protistology · 99 Rozella sp. JEL347 [AY601707] 98 Rozella allomycis [AY635838] Rozellids 100 Uncultured eukaryote P34.42 [AY642700] (outgroup) Uncultured eukaryote NAMAKO 37 [AB252777] 87 Uncultured eukaryote PS11D8 [GU072454] Uncultured eukaryote TAGIRI 24 [AB191432] Uncultured eukaryote D1P02G09 [EF100212] Aphelids Uncultured eukaryote PFF3AU2004 [DQ244010] 91 Aphelidium tribonemae X-102 89 97 Aphelidium aff. melosirae P-1 [KJ566931] Uncultured eukaryote PRS2 4E 31 [FJ976650] Uncultured eukaryote kor 250804 14 [FJ157335] 72 100 88 Uncultured eukaryote ESS220206.038 [GU067817] 88 Uncultured eukaryote CCW24 [AY230211] 95 Paraphelidium tribonemae X-103 [KX576682] 80 Uncultured eukaryote ESS270706.024 [GU067917] 100 Uncultured eukaryote ESS270706.065 [GU067958] 80 Uncultured eukaryote 051025 T2S1 W T SDP9 128 [FJ350301] 92 Uncultured eukaryote PA2009E13 [HQ191302] Amoeboaphelidium occidentale [JX967274] Amoeboaphelidium protococcarum FD95 [KJ541118] 100 Amoeboaphelidium protococcarum x 5 [JX507298 95 100 Uncultured eukaryote C01 SE1A [FJ592325] 96 Uncultured eukaryote T3P1AeG08 [GQ995416] Uncultured eukaryote kor 110904 24 [FJ157332] Uncultured eukaryote GA089 [HM487005] 83 Uncultured eukaryote CCW48 [AY180024] 60 Uncultured eukaryote T6P2AeG07 [GQ995418] 70 91 Uncultured eukaryote WIM48 [AM114806] 0.02 76 Uncultured eukaryote T4P1AeE08 [GQ995419] 97 Uncultured eukaryote NAMAKO 35 [AB252775] Fig. 1. Molecular phylogeny of Aphelidium tribonemae. Maximum likelihood tree based of aphelid 18S rRNA gene sequences rooted on rozellid representatives. The tree is based on an alignment of 1391 conserved positions. Sequence accession numbers are provided within brackets. Numbers at branches are bootstrap proportions >50 %. tribonemae (CCPP ZIN RAS) maintained in culture 2, I; 3). The cyst germinates and penetrates the host on the xanthophyte alga Tribonema gayanum (strain cell wall with an infection or penetration tube (Fig. 20 CALU). This sequence was only 86% identical 2, I, J). A conspicuous enlarging vacuole pushes to that of the other described Aphelidium species, the contents of the cyst towards the interior of the Aphelidium aff. melosirae (Karpov et al., 2014b), host cell through the penetration tube (Fig. 2, I). clearly indicating that they are two distantly related The parasitoid becomes a trophont, which engulfs Aphelidium species. We reconstructed a maximum the host cytoplasm forming food vacuoles (Fig. 2, likelihood (ML) phylogenetic tree including the L). The parasitoid grows and forms a plasmodium new 18S rDNA sequence
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