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Fabien Burki

Postdoctoral fellow in Molecular Systematics & Environmental Genomics

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  • Evolutionary Origins of Rhizarian Parasites. Mol. Biol. Evol. 2016 Apr;33(4):980-3. msv340. 10.1093/molbev/msv340.

    abstract

    The SAR group (Stramenopila, Alveolata, Rhizaria) is one of the largest clades in the tree of eukaryotes and includes a great number of parasitic lineages. Rhizarian parasites are obligate and have devastating effects on commercially important plants and animals but despite this fact, our knowledge of their biology and evolution is limited. Here, we present rhizarian transcriptomes from all major parasitic lineages in order to elucidate their evolutionary relationships using a phylogenomic approach. Our results suggest that Ascetosporea, parasites of marine invertebrates, are sister to the novel clade Apofilosa. The phytomyxean plant parasites branch sister to the vampyrellid algal ectoparasites in the novel clade Phytorhiza. They also show that Ascetosporea + Apofilosa + Retaria + Filosa + Phytorhiza form a monophyletic clade, although the branching pattern within this clade is difficult to resolve and appears to be model-dependent. Our study does not support the monophyly of the rhizarian parasitic lineages (Endomyxa), suggesting independent origins for rhizarian animal and plant parasites.

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  • The Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP): illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing. PLoS Biol. 2014 Jun;12(6):e1001889. 10.1371/journal.pbio.1001889. PBIOLOGY-D-14-00511. PMC4068987.

    abstract

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  • Phylogenomics of the intracellular parasite Mikrocytos mackini reveals evidence for a mitosome in rhizaria. Curr. Biol. 2013 Aug;23(16):1541-7. S0960-9822(13)00758-6. 10.1016/j.cub.2013.06.033.

    abstract

    Mikrocytos mackini is an intracellular protistan parasite of oysters whose position in the phylogenetic tree of eukaryotes has been a mystery for many years [1,2]. M. mackini is difficult to isolate, has not been cultured, and has no defining morphological feature. Furthermore, its only phylogenetic marker that has been successfully sequenced to date (the small subunit ribosomal RNA) is highly divergent and has failed to resolve its evolutionary position [2]. M. mackini is also one of the few eukaryotes that lacks mitochondria [1], making both its phylogenetic position and comparative analysis of mitochondrial function particularly important. Here, we have obtained transcriptomic data for M. mackini from enriched isolates and constructed a 119-gene phylogenomic data set. M. mackini proved to be among the fastest-evolving eukaryote lineages known to date, but, nevertheless, our analysis robustly placed it within Rhizaria. Searching the transcriptome for genetic evidence of a mitochondrion-related organelle (MRO) revealed only four mitochondrion-derived genes: IscS, IscU, mtHsp70, and FdxR. Interestingly, all four genes are involved in iron-sulfur cluster formation, a biochemical pathway common to other highly reduced "mitosomes" in unrelated MRO-containing lineages [7]. This is the first evidence of MRO in Rhizaria, and it suggests the parallel evolution of mitochondria to mitosomes in this supergroup.

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  • The revised classification of eukaryotes. J. Eukaryot. Microbiol. 2012 Sep;59(5):429-93. 10.1111/j.1550-7408.2012.00644.x. PMC3483872. NIHMS394066.

    abstract

    This revision of the classification of eukaryotes, which updates that of Adl et al. [J. Eukaryot. Microbiol. 52 (2005) 399], retains an emphasis on the protists and incorporates changes since 2005 that have resolved nodes and branches in phylogenetic trees. Whereas the previous revision was successful in re-introducing name stability to the classification, this revision provides a classification for lineages that were then still unresolved. The supergroups have withstood phylogenetic hypothesis testing with some modifications, but despite some progress, problematic nodes at the base of the eukaryotic tree still remain to be statistically resolved. Looking forward, subsequent transformations to our understanding of the diversity of life will be from the discovery of novel lineages in previously under-sampled areas and from environmental genomic information.

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  • Evolution of Rhizaria: new insights from phylogenomic analysis of uncultivated protists. BMC Evol. Biol. 2010 ;10():377. 1471-2148-10-377. 10.1186/1471-2148-10-377. PMC3014934.

    abstract

    Recent phylogenomic analyses have revolutionized our view of eukaryote evolution by revealing unexpected relationships between and within the eukaryotic supergroups. However, for several groups of uncultivable protists, only the ribosomal RNA genes and a handful of proteins are available, often leading to unresolved evolutionary relationships. A striking example concerns the supergroup Rhizaria, which comprises several groups of uncultivable free-living protists such as radiolarians, foraminiferans and gromiids, as well as the parasitic plasmodiophorids and haplosporids. Thus far, the relationships within this supergroup have been inferred almost exclusively from rRNA, actin, and polyubiquitin genes, and remain poorly resolved. To address this, we have generated large Expressed Sequence Tag (EST) datasets for 5 species of Rhizaria belonging to 3 important groups: Acantharea (Astrolonche sp., Phyllostaurus sp.), Phytomyxea (Spongospora subterranea, Plasmodiophora brassicae) and Gromiida (Gromia sphaerica).

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  • Untangling the phylogeny of amoeboid protists. J. Eukaryot. Microbiol. ;56(1):16-25. JEU379. 10.1111/j.1550-7408.2008.00379.x.

    abstract

    The amoebae and amoeboid protists form a large and diverse assemblage of eukaryotes characterized by various types of pseudopodia. For convenience, the traditional morphology-based classification grouped them together in a macrotaxon named Sarcodina. Molecular phylogenies contributed to the dismantlement of this assemblage, placing the majority of sarcodinids into two new supergroups: Amoebozoa and Rhizaria. In this review, we describe the taxonomic composition of both supergroups and present their small subunit rDNA-based phylogeny. We comment on the advantages and weaknesses of these phylogenies and emphasize the necessity of taxon-rich multigene datasets to resolve phylogenetic relationships within Amoebozoa and Rhizaria. We show the importance of environmental sequencing as a way of increasing taxon sampling in these supergroups. Finally, we highlight the interest of Amoebozoa and Rhizaria for understanding eukaryotic evolution and suggest that resolving their phylogenies will be among the main challenges for future phylogenomic analyses.

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  • Large-scale phylogenomic analyses reveal that two enigmatic protist lineages, telonemia and centroheliozoa, are related to photosynthetic chromalveolates. Genome Biol Evol 2009 ;1():231-8. 10.1093/gbe/evp022. PMC2817417.

    abstract

    Understanding the early evolution and diversification of eukaryotes relies on a fully resolved phylogenetic tree. In recent years, most eukaryotic diversity has been assigned to six putative supergroups, but the evolutionary origin of a few major "orphan" lineages remains elusive. Two ecologically important orphan groups are the heterotrophic Telonemia and Centroheliozoa. Telonemids have been proposed to be related to the photosynthetic cryptomonads or stramenopiles and centrohelids to haptophytes, but molecular phylogenies have failed to provide strong support for any phylogenetic hypothesis. Here, we investigate the origins of Telonema subtilis (a telonemid) and Raphidiophrys contractilis (a centrohelid) by large-scale 454 pyrosequencing of cDNA libraries and including new genomic data from two cryptomonads (Guillardia theta and Plagioselmis nannoplanctica) and a haptophyte (Imantonia rotunda). We demonstrate that 454 sequencing of cDNA libraries is a powerful and fast method of sampling a high proportion of protist genes, which can yield ample information for phylogenomic studies. Our phylogenetic analyses of 127 genes from 72 species indicate that telonemids and centrohelids are members of an emerging major group of eukaryotes also comprising cryptomonads and haptophytes. Furthermore, this group is possibly closely related to the SAR clade comprising stramenopiles (heterokonts), alveolates, and Rhizaria. Our results link two additional heterotrophic lineages to the predominantly photosynthetic chromalveolate supergroup, providing a new framework for interpreting the evolution of eukaryotic cell structures and the diversification of plastids.

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  • Phylogenomics reveals a new 'megagroup' including most photosynthetic eukaryotes. Biol. Lett. 2008 Aug;4(4):366-9. J355M22278421402. 10.1098/rsbl.2008.0224. PMC2610160.

    abstract

    Advances in molecular phylogeny of eukaryotes have suggested a tree composed of a small number of supergroups. Phylogenomics recently established the relationships between some of these large assemblages, yet the deepest nodes are still unresolved. Here, we investigate early evolution among the major eukaryotic supergroups using the broadest multigene dataset to date (65 species, 135 genes). Our analyses provide strong support for the clustering of plants, chromalveolates, rhizarians, haptophytes and cryptomonads, thus linking nearly all photosynthetic lineages and raising the question of a possible unique origin of plastids. At its deepest level, the tree of eukaryotes now receives strong support for two monophyletic megagroups comprising most of the eukaryotic diversity.

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  • Phylogenomics reshuffles the eukaryotic supergroups. PLoS ONE 2007 ;2(8):e790. 10.1371/journal.pone.0000790. PMC1949142.

    abstract

    Resolving the phylogenetic relationships between eukaryotes is an ongoing challenge of evolutionary biology. In recent years, the accumulation of molecular data led to a new evolutionary understanding, in which all eukaryotic diversity has been classified into five or six supergroups. Yet, the composition of these large assemblages and their relationships remain controversial.

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  • Analysis of expressed sequence tags from a naked foraminiferan Reticulomyxa filosa. Genome 2006 Aug;49(8):882-7. g06-048. 10.1139/g06-048.

    abstract

    Foraminifers are a major component of modern marine ecosystems and one of the most important oceanic producers of calcium carbonate. They are a key phylogenetic group among amoeboid protists, but our knowledge of their genome is still mostly limited to a few conserved genes. Here, we report the first study of expressed genes by means of expressed sequence tag (EST) from the freshwater naked foraminiferan Reticulomyxa filosa. Cluster analysis of 1630 valid ESTs enabled the identification of 178 groups of related sequences and 871 singlets. Approximately 50% of the putative unique 1059 ESTs could be annotated using Blast searches against the protein database SwissProt + TrEMBL. The EST database described here is the first step towards gene discovery in Foraminifera and should provide the basis for new insights into the genomic and transcriptomic characteristics of these interesting but poorly understood protists.

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  • Monophyly of Rhizaria and multigene phylogeny of unicellular bikonts. Mol. Biol. Evol. 2006 Oct;23(10):1922-30. msl055. 10.1093/molbev/msl055.

    abstract

    Reconstructing a global phylogeny of eukaryotes is an ongoing challenge of molecular phylogenetics. The availability of genomic data from a broad range of eukaryotic phyla helped in resolving the eukaryotic tree into a topology with a rather small number of large assemblages, but the relationships between these "supergroups" are yet to be confirmed. Rhizaria is the most recently recognized "supergroup," but, in spite of this important position within the tree of life, their representatives are still missing in global phylogenies of eukaryotes. Here, we report the first large-scale analysis of eukaryote phylogeny including data for 2 rhizarian species, the foraminiferan Reticulomyxa filosa and the chlorarachniophyte Bigelowiella natans. Our results confirm the monophyly of Rhizaria (Foraminifera + Cercozoa), with very high bootstrap supports in all analyses. The overall topology of our trees is in agreement with the current view of eukaryote phylogeny with basal division into "unikonts" (Opisthokonts and Ameobozoa) and "bikonts" (Plantae, alveolates, stramenopiles, and excavates). As expected, Rhizaria branch among bikonts; however, their phylogenetic position is uncertain. Depending on the data set and the type of analysis, Rhizaria branch as sister group to either stramenopiles or excavates. Overall, the relationships between the major groups of unicellular bikonts are poorly resolved, despite the use of 85 proteins and the largest taxonomic sampling for this part of the tree available to date. This may be due to an acceleration of evolutionary rates in some bikont phyla or be related to their rapid diversification in the early evolution of eukaryotes.

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  • Phylogenetic position of Gromia oviformis Dujardin inferred from nuclear-encoded small subunit ribosomal DNA. Protist 2002 Sep;153(3):251-60.

    abstract

    Gromia oviformis Dujardin is a common marine protist characterised by a large, globular test and filose pseudopodia. First considered a foraminifer, Gromia was later placed within the Filosea and recently included among amoebae of uncertain affinities. In order to clarify the phylogenetic position of this genus, we sequenced the complete small-subunit ribosomal DNA gene of G. oviformis collected at five different geographic localities. The high divergence of obtained sequences suggests that G. oviformis is a species complex composed of several genetically distinct sibling species. Sequence analyses show Gromia to be a member of the Cercozoa, a heterogeneous assemblage which includes filose amoebae, the amoeboflagellate cercomonads, the chlorarachniophytes and the plasmodiophorid plant pathogens. Contrary to traditional classification, Gromia is not closely related to other testate filose amoebae (the Euglyphida), but seems to branch early among the Cercozoa. Our analyses also show a close relationship between the Cercozoa and the Acantharea. Because the Cercozoa are related to the Foraminifera based on other molecular data, we propose that most protists possessing filopodia, reticulopodia and axopodia have a common origin.

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Taking advantage of the actual dynamic in phylogenomic, the main aim of my thesis is the use of genomic data to study important questions in eukaryotic evolution. Among eukaryotes, I am particularly interested in Rhizaria which represent a big part of the diversity but are nevertheless missing in most of global phylogenies.

Our current project is to extend our taxa sampling with species specifically chosen for their good micropaleontological records. We are inferring a molecular time-scale for the eukaryotic tree, at the interface between phylogenomics and micropaleontology.