P.J. Keeling's research while affiliated with University of British Columbia - Vancouver and other places

Publications (989)

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Apicomplexans and related lineages comprise many obligate symbionts of animals; some of which cause notorious diseases such as malaria. They evolved from photosynthetic ancestors and transitioned into a symbiotic lifestyle several times, giving rise to species with diverse non-photosynthetic plastids. Here we sought to reconstruct the evolution of...
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Comparing obligate endosymbionts with their free-living relatives is a powerful approach to investigate the evolution of symbioses, and it has led to the identification of several genomic traits consistently associated with the establishment of symbiosis. ‘ Candidatus Nebulobacter yamunensis’ is an obligate bacterial endosymbiont of the ciliate Eup...
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Molecular phylogenetics of microbial eukaryotes has reshaped the tree of life by establishing broad taxonomic divisions, termed supergroups, that supersede the traditional kingdoms of animals, fungi and plants, and encompass a much greater breadth of eukaryotic diversity¹. The vast majority of newly discovered species fall into a small number of kn...
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Kleptoplasts are distinct among photosynthetic organelles in eukaryotes (i.e, plastids) because they are routinely sequestered from prey algal cells and function only temporarily in the new host cell. Therefore, the hosts of kleptoplasts benefit from photosynthesis without constitutive photoendosymbiosis. Here, we report that the euglenozoan Rapaza...
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Background Microbial symbioses in marine invertebrates are commonplace. However, characterizations of invertebrate microbiomes are vastly outnumbered by those of vertebrates. Protists and fungi run the gamut of symbiosis, yet eukaryotic microbiome sequencing is rarely undertaken, with much of the focus on bacteria. To explore the importance of micr...
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Dinoflagellates are a diverse protist group possessing many unique traits. These include (but are not limited to) expansive genomes packaged into permanently condensed chromosomes, photosynthetic or cryptic plastids acquired vertically or horizontally in serial endosymbioses, and a ruffle-like transverse flagellum attached along its length to the c...
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Animals and fungi have radically distinct morphologies, yet both evolved within the same eukaryotic supergroup: Opisthokonta1,2. Here we reconstructed the trajectory of genetic changes that accompanied the origin of Metazoa and Fungi since the divergence of Opisthokonta with a dataset that includes four novel genomes from crucial positions in the O...
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Microbial predators such as choanoflagellates are key players in ocean food webs. Choanoflagellates, which are the closest unicellular relatives of animals, consume bacteria and also exhibit marked biological transitions triggered by bacterial compounds, yet their native microbiomes remain uncharacterized. Here we report the discovery of a ubiquito...
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New data on the species diversity and morphology of centrohelid heliozoans in freshwater, marine, and soil habitats of Ukraine were obtained. Cell coverings (scales and spicules) were observed using scanning and transmission electron microscopy. Eighteen species from seven genera of centrohelids and unidentifiable Heterophrys-like organisms were re...
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Prokaryotic genomes are usually densely packed with intact and functional genes. However, in certain contexts, such as after recent ecological shifts or extreme population bottlenecks, broken and non-functional gene fragments can quickly accumulate and form a substantial fraction of the genome. Identification of these broken genes, called pseudogen...
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Symbiotic systems vary in the degree to which the partners are bound to each other¹. At one extreme, there are intracellular endosymbionts in mutually obligate relationships with their host, often interpreted as mutualistic. The symbiosis between the betaproteobacterium Polynucleobacter and the ciliate Euplotes (clade B) challenges this view²: alth...
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Gene transfer agents (GTAs) are virus-like structures that package and transfer prokaryotic DNA from donor to recipient prokaryotic cells. Here, we describe widespread GTA gene clusters in the highly reduced genomes of bacterial endosymbionts from microbial eukaryotes (protists). Homologs of the GTA capsid and portal complexes were initially found...
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Animals and microorganisms often establish close ecological relationships. However, much of our knowledge about animal microbiomes comes from two deeply studied groups: vertebrates and arthropods. To understand interactions on a broader scale of diversity, we characterized the bacterial microbiomes of close to 1,000 microscopic marine invertebrates...
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The microbial communities of sandy beaches are poorly described despite the biogeochemical importance and ubiquity of these ecosystems. Using metabarcoding of the 16S and 18S rRNA genes, we investigated the diversity, microhabitats (with or between sand grains), and intertidal distributions of microorganisms (including meiofauna) from pristine sand...
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Although photosynthesis has been lost many times, complete loss of the plastid organelle is considered to be very rare, since plastids are integrated into host metabolism in many ways. But understanding plastid loss is critical to understanding the evolution of photosynthesis and endosymbiosis more broadly. Plastid loss is a central force underlyin...
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Diplonemids are a group of flagellate protists, that belong to the phylum Euglenozoa alongside euglenids, symbiontids and kinetoplastids. They primarily inhabit marine environments, though are also found in freshwater lakes. Diplonemids have been considered as rare and unimportant eukaryotes for over a century, with only a handful of species descri...
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Stramenopiles are a diverse but relatively well-studied eukaryotic supergroup with considerable genomic information available (Sibbald and Archibald, 2017). Nevertheless, the relationships between major stramenopile subgroups remain unresolved, in part due to a lack of data from small nanoflagellates that make up a lot of the genetic diversity of t...
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The family ‘ Candidatus Midichloriaceae’ constitutes the most diverse but least studied lineage within the important order of intracellular bacteria Rickettsiales . Midichloriaceae endosymbionts are found in many hosts, including terrestrial arthropods, aquatic invertebrates, and protists. Representatives of the family are not documented to be path...
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Gene exchange between viruses and their hosts acts as a key facilitator of horizontal gene transfer and is hypothesized to be a major driver of evolutionary change. Our understanding of this process comes primarily from bacteria and phage co-evolution, but the mode and functional importance of gene transfers between eukaryotes and their viruses rem...
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Protist-bacteria associations are extremely common. Among them, those involving ciliates of the genus Euplotes are emerging as models for symbioses between prokaryotes and eukaryotes, and a great deal of information is available from cultured representatives of this system. Even so, as for most known microbial symbioses, data on natural populations...
Preprint
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Stramenopiles are a diverse but relatively well-studied eukaryotic supergroup with considerable genomic information available (Sibbald and Archibald, 2017). Nevertheless, the relationships between major stramenopile subgroups remain unresolved, in part due to a lack of data from small nanoflagellates that make up a lot of the genetic diversity of t...
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The endosymbiotic origin of plastids from cyanobacteria gave eukaryotes photosynthetic capabilities and launched the diversification of countless forms of algae. These primary plastids are found in members of the eukaryotic supergroup Archaeplastida. All known archaeplastids still retain some form of primary plastids, which are widely assumed to ha...
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Prokaryotic genomes are generally gene dense and encode relatively few pseudogenes, or nonfunctional/inactivated remnants of genes. However, in certain contexts, such as recent ecological shifts or extreme population bottlenecks (such as those experienced by symbionts and pathogens), pseudogenes can quickly accumulate and form a substantial fractio...
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We present the Aquatic Symbiosis Genomics Project, a global collaboration to generate high quality genome sequences for a wide range of eukaryotes and their microbial symbionts. Launched under the Symbiosis in Aquatic Systems Initiative of the Gordon and Betty Moore Foundation, the ASG Project brings together researchers from across the globe who h...
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Heterolobose amoebae are important members of marine, freshwater, and soil microbial communities, but their diversity remains under-explored. We studied the diversity of Vahlkampfiidae to improve our understanding of heterolobosean relationships and their representation in aquatic benthos. Using light and electron microscopy, and molecular phylogen...
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Most of the genetic, cellular, and biochemical diversity of life rests within single-celled organisms — the prokaryotes (bacteria and archaea) and microbial eukaryotes (protists). Very close interactions, or symbioses, between protists and prokaryotes are ubiquitous, ecologically significant, and date back at least two billion years ago to the orig...
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Gregarines are an early-diverging lineage of apicomplexan parasites that hold many clues into the origin and evolution of the group, a remarkable transition from free-living phototrophic algae into obligate parasites of animals.1 Using single-cell transcriptomics targeting understudied lineages to complement available sequencing data, we characteri...
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The endosymbiotic origin of plastids from cyanobacteria gave eukaryotes photosynthetic capabilities and launched the diversification of countless forms of algae. These primary plastids are found in members of the eukaryotic supergroup Archaeplastida, and are widely assumed to have a single origin. Here, we used single-cell genomics from natural sam...
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All organisms host a diversity of associated viruses, bacteria, and protists, collectively defined as the holobiont. While scientific advancements have enhanced the understanding of the functional roles played by various components of the holobiont, there is a growing need to integrate multiple types of molecular data into spatially and temporally...
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Cristamonadea is a large class of parabasalian protists that reside in the hindguts of wood-feeding insects, where they play an essential role in the digestion of lignocellulose. This group of symbionts boasts an impressive array of complex morphological characteristics, many of which have evolved multiple times independently. However, their divers...
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Gene exchange between viruses and their hosts acts as a key facilitator of horizontal gene transfer and is thought to be a major driver of evolutionary change 1–3. Our understanding of this process comes primarily from bacteria and phage co-evolution4, but the mode and functional significance of gene transfers between eukaryotes and their viruses r...
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Corals (Metazoa; Cnidaria; Anthozoa) have recently been shown to play host to a widespread and diverse group of intracellular symbionts of the phylum Apicomplexa. These symbionts, colloquially called ‘corallicolids’, are mostly known through molecular analyses, and no formal taxonomy has been proposed. Another apicomplexan, Gemmocystis cylindrus (d...
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Snow and ice present challenging substrates for cellular growth, yet microbial snow communities not only exist, but are diverse and ecologically impactful. These communities are dominated by green algae, but additional organisms, such as fungi, are also abundant and may be important for nutrient cycling, syntrophic interactions, and community struc...
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Kinetoplastids are heterotrophic flagellated protists, including important parasites of humans and animals (trypanosomatids), and ecologically important free-living bacterial consumers (bodonids). Phylogenies have shown that the earliest-branching kinetoplastids are all parasites or obligate endosymbionts, whose highly-derived state makes reconstru...
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Euglenids are a well-known group of single-celled eukaryotes, with phototrophic, osmotrophic and phagotrophic members. Phagotrophs represent most of the phylogenetic diversity of euglenids, and gave rise to the phototrophs and osmotrophs, but their evolutionary relationships are poorly understood. Symbiontids, in contrast, are anaerobes that are al...
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Recent progress in understanding the early evolution of eukaryotes was tied to morphological identification of flagellates and heliozoans from natural samples, isolation of their culture and genomic and ultrastructural investigations. These protists are the smallest and least studied microbial eukaryotes but play an important role in the functionin...
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Large eukaryotes support diverse communities of microbes on their surface-epibiota-that profoundly influence their biology. Alternate factors known to structure complex patterns of microbial diversity-host evolutionary history and ecology, environmental conditions and stochasticity-do not act independently and it is challenging to disentangle their...
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Corals (Metazoa; Cnidaria; Anthozoa) have recently been shown to play host to a widespread and diverse group of intracellular symbionts of the phylum Apicomplexa. These symbionts, colloquially called ‘corallicolids’, are mostly known through molecular analyses, and no formal taxonomy has been proposed. Another apicomplexan, Gemmocystis cylindrus (d...
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The phylum Apicomplexa consists largely of obligate animal parasites that include the causative agents of human diseases such as malaria. Apicomplexans have also emerged as models to study the evolution of non-photosynthetic plastids, as they contain a relict chloroplast known as the apicoplast. The apicoplast offers important clues into how apicom...
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Dinoflagellates possess many cellular characteristics with unresolved evolutionary histories. These include nuclei with greatly expanded genomes and chromatin packaged using histone-like proteins and dinoflagellate-viral nucleoproteins instead of histones, highly reduced mitochondrial genomes with extensive RNA editing, a mix of photosynthetic and...
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The origin of animals is one of the most intensely studied evolutionary events, and our understanding of this transition was greatly advanced by analyses of unicellular relatives of animals, which have shown many “animal-specific” genes actually arose in protistan ancestors long before the emergence of animals [1, 2, 3]. These genes have complex di...
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Phagocytosis is a fundamental process in marine ecosystems by which prey organisms are consumed and their biomass incorporated in food webs or remineralized. However, studies searching for the genes underlying this key ecological process in free-living phagocytizing protists are still scarce, in part due to the lack of appropriate ecological models...
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Recent progress in understanding the early evolution of eukaryotes was tied to morphological identification of flagellates and heliozoans in the natural samples, isolation of their cultures and genomic and ultrastructural investigations. These protists are the smallest and least studied microbial eukaryotes but play an important role in functioning...
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Chlorarachniophytes are marine unicellular algae that acquired a complex plastid through an endosymbiosis with a green alga. As such, they have attracted attention especially from evolutionary biologists as a model for studying organellogenesis. A transient transformation system by particle bombardment was previously established for an amoeboid spe...
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Background: The origin of animals from their unicellular ancestor was one of the most important events in evolutionary history, but the nature and the order of events leading up to the emergence of multicellular animals are still highly uncertain. The diversity and biology of unicellular relatives of animals have strongly informed our understandin...
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The membrane-associated progesterone receptor (MAPR) family consists of heme-binding proteins containing a cytochrome b5 (cytb5) domain characterized by the presence of a MAPR-specific interhelical insert region (MIHIR) between helices 3 and 4 of the canonical cytb5-domain fold. Animals possess three MAPR genes (PGRMC-like, Neuferricin and Neudesin...
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Alveolates are a major supergroup of eukaryotes encompassing more than ten thousand free-living and parasitic species, including medically, ecologically, and economically important apicomplexans, dinoflagellates, and ciliates. These three groups are among the most widespread eukaryotes on Earth, and their environmental success can be linked to uniq...
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Background: The Euglenozoa are a protist group with an especially rich history of evolutionary diversity. They include diplonemids, representing arguably the most species-rich clade of marine planktonic eukaryotes; trypanosomatids, which are notorious parasites of medical and veterinary importance; and free-living euglenids. These different lifest...
Preprint
Alveolates are a major supergroup of eukaryotes encompassing more than ten thousand free-living and parasitic species, including medically, ecologically, and economically important apicomplexans, dinoflagellates, and ciliates. These three groups are among the most widespread eukaryotes on Earth, and their environmental success can be linked to uniq...
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Genome evolution in bacterial endosymbionts is notoriously extreme: the combined effects of strong genetic drift and unique selective pressures result in highly reduced genomes with distinctive adaptations to hosts [1-4]. These processes are mostly known from animal endosymbionts, where nutritional endosymbioses represent the best-studied systems....
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Marine sediments are one of the largest carbon reservoir on Earth, yet the microbial communities, especially the eukaryotes, that drive these ecosystems are poorly characterised. Here, we report implementation of a sampling system that enables injection of reagents into sediments at depth, allowing for preservation of RNA in situ. Using the RNA tem...
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Most eukaryotic microbial diversity is uncultivated, under-studied and lacks nuclear genome data. Mitochondrial genome sampling is more comprehensive, but many phylogenetically important groups remain unsampled. Here, using a single-cell sorting approach combining tubulin-specific labelling with photopigment exclusion, we sorted flagellated heterot...
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Microbial eukaryotes (protists) are structurally, developmentally and behaviourally more complex than their prokaryotic cousins. This complexity makes it more difficult to translate genomic and metagenomic data into accurate functional inferences about systems ranging all the way from molecular and cellular levels to global ecological networks. Thi...
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Awareness of the roles host‐associated microbes play in host biology has escalated in recent years. However, microbiome studies have focused essentially on bacteria, and overall, we know little about the role of host‐associated eukaryotes outside of the field of parasitology. Despite that, eukaryotes and microeukaryotes in particular are known to b...
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The diversity and biology of unicellular relatives of animals has strongly informed our understanding of the transition from single-celled organisms to the multicellular Metazoa. Here we analyse the cellular structures and complex life cycles of the novel unicellular holozoans Pigoraptor and Syssomonas (Opisthokonta). Both lineages are characterize...
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Apicomplexans are a group of microbial eukaryotes that contain some of the most well-studied parasites, including the causing agents of toxoplasmosis and malaria, and emergent diseases like cryptosporidiosis or babesiosis. Decades of research have illuminated the pathogenic mechanisms, molecular biology, and genomics of model apicomplexans, but we...
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Giant viruses are remarkable for their large genomes, often rivaling those of small bacteria, and for having genes thought exclusive to cellular life. Most isolated to date infect nonmarine protists, leaving their strategies and prevalence in marine environments largely unknown. Using eukaryotic single-cell metagenomics in the Pacific, we discovere...
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Lower termites harbor in their hindgut complex microbial communities that are involved in the digestion of cellulose. Among these are protists, which are usually associated with specific bacterial symbionts found on their surface or inside their cells. While these form the foundations of a classic system in symbiosis research, we still know little...
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Whether mitochondria and plastids originated by endosymbiosis is no longer questioned, but we still do not understand the actual process of integration. Other, younger endosymbiotic systems are, however, relatively common. Traditionally, it was not clear whether these systems could be directly and informatively compared to organelles because they a...
Preprint
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Background The membrane-associated progesterone receptor (MAPR) family consists of heme-binding proteins containing a cytochrome b 5 (cytb 5 ) domain characterized by the presence of a MAPR-specific interhelical insert region (MIHIR) between helices 3 and 4 of the canonical cytb5-domain fold. Animals possess three MAPR families (PGRMC-like, Neuferr...
Article
Plastid endosymbiosis has been a major force in the evolution of eukaryotic cellular complexity, but how endosymbionts are integrated is still poorly understood at a mechanistic level. Dinoflagellates, an ecologically important protist lineage, represent a unique model to study this process because dinoflagellate plastids have repeatedly been reduc...
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Developing a detailed understanding of how all known forms of life are related to one another in the tree of life has been a major preoccupation of biology since the idea of tree-like evolution first took hold. Since most life is microbial, our intuitive use of morphological comparisons to infer relatedness only goes so far, and molecular sequence...
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Rhodophyta (red algae) is one of three lineages of Archaeplastida¹, a supergroup that is united by the primary endosymbiotic origin of plastids in eukaryotes2,3. Red algae are a diverse and species-rich group, members of which are typically photoautotrophic, but are united by a number of highly derived characteristics: they have relatively small in...
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The apicomplexans are a group of obligate animal pathogens that include Plasmodium (malaria), Toxoplasma (toxoplasmosis), and Cryptosporidium (cryptosporidiosis) [1]. They are an extremely diverse and specious group but are nevertheless united by a distinctive suite of cytoskeletal and secretory structures related to infection, called the apical co...
Preprint
Full-text available
Genome evolution in bacterial endosymbionts is notoriously extreme: the combined effects of strong genetic drift and unique selective pressures result in highly reduced genomes with distinctive adaptations to hosts. These processes are mostly known from animal endosymbionts, where nutritional endosymbioses represent the best-studied systems. Howeve...
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Endosymbioses between bacteria and eukaryotes are enormously important in ecology and evolution, and as such are intensely studied. Despite this, the range of investigated hosts is narrow in the context of the whole eukaryotic tree of life: most of the information pertains to animal hosts, while most of the diversity is found in unicellular protist...
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To date, sea slugs have been considered the only animals known to sequester functional algal plastids into their own cells, via a process called “kleptoplasty.” We report here, however, that endosymbionts in the marine flatworms Baicalellia solaris and Pogaina paranygulgus are isolated plastids stolen from diatoms. Ultrastructural data show that kl...
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The application of metabarcoding to study animal‐associated microeukaryotes has been restricted because the universal barcode used to study microeukaryotic ecology and distribution in the environment, the Small Subunit of the Ribosomal RNA gene (18S rRNA), is also present in the host. As a result, when host‐associated microbial eukaryotes are analy...