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Phylogenomics of the Intracellular Parasite Mikrocytos Mackini Reveals Evidence for a Mitosome in Rhizaria

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Phylogenomics of the Intracellular Parasite Mikrocytos Mackini Reveals Evidence for a Mitosome in Rhizaria Current Biology 23, 1541–1547, August 19, 2013 ª2013 Elsevier Ltd All rights reserved http://dx.doi.org/10.1016/j.cub.2013.06.033 Report Phylogenomics of the Intracellular Parasite Mikrocytos mackini Reveals Evidence for a Mitosome in Rhizaria Fabien Burki,1 Nicolas Corradi,2 Roberto Sierra,3 M. mackini was a basal, highly divergent eukaryote without Jan Pawlowski,3 Gary R. Meyer,4 Cathryn L. Abbott,4 close relatives [2]. This idea was reinforced by the structural and Patrick J. Keeling1,* simplicity of microcells and the fact that no canonical mito- 1Department of Biology, Canadian Institute for Advanced chondrion or related organelle, such as hydrogenosome or Research, University of British Columbia, Vancouver, mitosome, has been observed [1,6]. However, in the last BC V6T 1Z4, Canada 10 years, systematic studies of other ‘‘amitochondriate’’ 2Department of Botany, Canadian Institute for Advanced lineages have repeatedly falsified the hypothesis that these Research, University of Ottawa, Ottawa, ON K1N 6N5, Canada lineages ancestrally lack mitochondria. The current view is 3Department of Genetics and Evolution, University of Geneva, that all extant eukaryotes possess mitochondria or reduced 1211 Geneva, Switzerland mitochondrial-related organelles (MROs), which have inde- 4Department of Fisheries and Oceans, Pacific Biological pendently evolved in several lineages (see [7,8] for reviews). Station, Nanaimo, BC V9R 5K6, Canada To see how M. mackini fits into this picture of mitochondrial evolution, we generated a large transcriptome data set by Illumina sequencing and used it to obtain multiple genes in Summary order to investigate its phylogenetic position and assess what type of MRO, if any, is most likely present. Mikrocytos mackini is an intracellular protistan parasite of M. mackini cells are not easily separated from its Pacific oys- oysters whose position in the phylogenetic tree of eukary- ter host, Crassostrea gigas [9]. Using an enrichment protocol otes has been a mystery for many years [1,2]. M. mackini is and the C. gigas genome to filter host-derived sequences difficult to isolate, has not been cultured, and has no from the transcriptome (see the Supplemental Information defining morphological feature. Furthermore, its only phylo- available online), we identified 15,874 contigs of putative genetic marker that has been successfully sequenced to M. mackini origin. From these, we searched for homologs of date (the small subunit ribosomal RNA) is highly divergent 252 protein-coding genes previously used in a phylogenomic and has failed to resolve its evolutionary position [2]. study [10], which revealed that M. mackini genes are charac- M. mackini is also one of the few eukaryotes that lacks terized by very high rates of evolution. Consequently, single- mitochondria [1], making both its phylogenetic position gene trees were generally poorly resolved; therefore, we and comparative analysis of mitochondrial function particu- applied two conditions in order to assess orthology of the larly important. Here, we have obtained transcriptomic data M. mackini sequences: (1) the sequences must be most for M. mackini from enriched isolates and constructed a closely related to the correct orthologs (bootstrap R 70%), 119-gene phylogenomic data set. M. mackini proved to be and (2) they must show no sign of suspicious relationships among the fastest-evolving eukaryote lineages known to to any other lineages (such as C. gigas or prokaryotes). Overall, date, but, nevertheless, our analysis robustly placed it within this led to the identification of 103 M. mackini orthologous Rhizaria. Searching the transcriptome for genetic evidence sequences, but, because a preliminary analysis showed that of a mitochondrion-related organelle (MRO) revealed only M. mackini might belong to the eukaryotic supergroup Rhizaria four mitochondrion-derived genes: IscS, IscU, mtHsp70, (data not shown), we added an additional 16 genes that had and FdxR. Interestingly, all four genes are involved in iron- fewer than 60% missing positions for Rhizaria as a whole, sulfur cluster formation, a biochemical pathway common leading to a concatenated alignment of 119 genes (Table S1) to other highly reduced ‘‘mitosomes’’ in unrelated MRO- and 23,162 amino acid (aa) positions. containing lineages [7]. This is the first evidence of MRO in To determine the relationship of M. mackini to other Rhizaria, and it suggests the parallel evolution of mitochon- eukaryotes, we first analyzed a broad taxon sampling of 101 dria to mitosomes in this supergroup. operational taxonomic units (OTUs), including representatives of all supergroups and lineages with no strong affiliation, such Results and Discussion as Collodictyon, Thecamonas,orPicobiliphytes (Figure 1). This data set also contained notoriously fast-evolving taxa, Mikrocytos mackini Is a Derived Rhizarian such as the cryptomonad nucleomorphs, diplomonads, and Few eukaryotes are of a completely unknown evolutionary parabasalians. Phylogenetic analyses using maximum likeli- origin. Despite ultrastructural and molecular studies, the hood (ML) with the site-homogeneous LG model and Bayesian enigmatic microcell parasite Mikrocytos mackini, which is method (BI) with the site-heterogeneous CAT model were the causative agent of the Denman Island disease in oysters, in general agreement with recent phylogenomic analyses is one such orphan lineage [1,2]. Recently, molecular detection [11–16]. More interestingly, both analyses strongly supported has shown that diverse Mikrocytos-like parasites infect a M. mackini branching within Rhizaria (1.0 BI posterior proba- variety of oysters in different regions of the world, but it did bility and 91% ML bootstrap). The extreme rate of evolution not provide clues of M. mackini’s phylogenetic position [3–5]. of M. mackini genes was reflected in its branch length: On the basis of phylogenetic analysis of small subunit (SSU) from a hypothetical root on unikonts (Amoebozoa + opistho- ribosomal DNA (rDNA), it was tentatively proposed that konts), as recently proposed on the basis of mitochondrial and bacterial proteins [17], the distance to M. mackini is twice that of the second longest branch in the ML tree *Correspondence: [email protected] (the diplomonad Spironucleus). Nevertheless, the position of Current Biology Vol 23 No 16 1542 Missing Missing positions (%) genes (%) 0.96/95 Globobulimina turgida* 0.85/64 Nonionellina sp * Bulimina marginata * RHIZARIA Elphidium sp * Foraminifera Ammonia sp * 0.93/65 Reticulomyxa filosa * Retaria Collozoum sp * Spongosphaera streptacantha * Polycystinea Amphilonche elongata * 0.99/77 Phyllostaurus siculus * Acantharea 0.92/- Astrolonche serrata * Mikrocytos mackini 0.99/- Corallomyxa sp 0.98/- Gromia sphaerica Gromia + Corallomyxa 1/91 1/100 Plasmodiophora brassicae Spongospora subterranea Plasmodiophorida 0.91/50 Cercomonas longicauda 0.95/- Guttulinopsis vulgaris * Aulacantha scolymantha Cercozoa 1/99 Bigelowiella natans 1/92 Nannochloropsis gaditana Ectocarpus siliculosus 1/91 Phaeodactylum tricornutum Thalassiosira pseudonana Aureococcus anophagefferens STRAMENOPILES Phytophthora ramorum Saprolegnia parasitica Blastocystis hominis Alexandrium 1/98 Karlodinium micrum 1/52 Oxyrrhis marina Perkinsus marinus Chromera velia Cryptosporidium ALVEOLATES Plasmodium * Toxoplasma gondii Paramecium tetraurelia * Tetrahymena thermophila * Emiliania huxleyi Isochrysis galbana Prymnesium parvum HAPTOPHYTES Pavlova lutheri Raphidiophrys CENTROHELIDS Arabidopsis Populus trichocarpa Oryza sativa Sorghum bicolor Physcomitrella patens Selaginella moellendorffii GREEN Mesostigma viride Chlorella vulgaris PLANTS Coccomyxa sp Volvox carteri Micromonas Ostreococcus Calliarthron tuberculosum 1/97 Chondrus crispus 1/97 RED 1/- Gracilaria changii 1/97 Porphyra yezoensis ALGAE Porphyridium cruentum + Cyanidioschyzon merolae Galdieria sulphuraria NUCLEOMORPHS Guillardia theta-nucleomorph * Hemiselmis andersenii-nucleomorph * Guillardia theta CRYPTOPHYTES Plagioselmis nannoplanctica 1/- Roombia truncata KATABLEPHARIDS Picobiliphyte PICOBILIPHYTES Telonema subtilis TELONEMIDS Cyanophora paradoxa Glaucocystis nostochinearum GLAUCOPHYTES Bodo saltans * Trypanosoma * 1/99 Euglena 0.85/- Naegleria gruberi Sawyeria marylandensis * EXCAVATES Stachyamoeba lipophora 0.98/- Jakoba Seculamonas ecuadoriensis Reclinomonas americana Collodictyon triciliatum DIPHYLLATIA 0.99/62 Malawimonas MALAWIMONAS Giardia * DIPLOMONADS 1/91 Spironucleus * Trichomonas vaginalis * PARABASALIDS Trimastix pyriformis TRIMASTIX Hartmannella vermiformis Acanthamoeba 1/- Dictyostelium discoideum Physarum polycephalum AMOEBOZOA 1/- Entamoeba histolytica * 1/99 Mastigamoeba balamuthi Batrachochytrium dendrobatidis Laccaria bicolor Neurospora crassa Capsaspora owczarzaki OPISTHOKONTS Homo sapiens Nematostella vectensis 1/91 Monosiga brevicolis Thecamonas trahens APUSOZOA Breviata anathema BREVIATA 100 80 60 40200 20 40 60 80 100 0.5 Figure 1. Global Phylogenetic Tree of Eukaryotes A tree inferred with 119 genes and 101 OTUs under the CAT + G4 model, as implemented in PhyloBayes. Two Markov chain Monte Carlo chains were run for 9,000 cycles with a burn-in of 1,000, but convergence was not reached for a few nodes outside of Rhizaria. In comparison to the tree shown here, differences between the chains concerned the relative positions of haptophytes, centrohelids, cryptophytes + katablepharids, picobiliphytes, and telonemids. Values at nodes denote Bayesian posterior probabilities (to the left of the slash) and maximum likelihood
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