Brian Leander
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Dissertations completed in 2010 or later are listed below. Please note that there is a 6-12 month delay to add the latest dissertations.
Dinoflagellates are a diverse group of protists with many unique traits including large genomes packaged into permanently condensed chromosomes, photosynthetic or cryptic plastids acquired vertically or horizontally in serial endosymbioses, and in some taxa, highly complex organelles like nematocysts and the eye-like ocelloid. Because these features promise to expand our understanding of eukaryotic biology, reconstructing how they evolved has become a point of interest. To infer ancestral states, robust and well-supported phylogenies generated from high-coverage transcriptomic datasets are needed. So far, these analyses have relied on transcriptome data from cultured taxa, which are mostly photosynthetic. As half of known dinoflagellate species are non-photosynthetic, current phylogenies fail to reflect the diversity that characterizes this group. Here, I generate single cell transcriptomes from over 150 rare and under-sampled dinoflagellates collected from the environment. Using these data, I explore three major heterotrophic lineages of interest: Abedinium, the Noctilucales, and the complex organelle-bearing members of the Gymnodiniales, the warnowiids. In these investigations I reveal that Abedinium is an independent, deep-branching core dinoflagellate lineage, the unique traits of the Noctilucales are derived rather than ancestral, and the heterotrophic warnowiids retain photosynthetic genes except for photosystem II and RuBisCo, suggesting that this mechanism serves an alternate function in the ocelloid. In the final chapter I generate a comprehensive dinoflagellate phylogeny that better represents the proportion of heterotrophic, athecate, and deep- branching taxa in dinoflagellates. This analysis reveals several new insights, including the early acquisition timing of two histone-like protein (HLP) types, the diversity and punctate distribution of microbial rhodopsins, and the common retention of plastid-derived electron transport genes across heterotrophic dinoflagellates.
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Dinoflagellates are an abundant and diverse group of aquatic eukaryotes, with members that have photosynthetic, heterotrophic, or mixotrophic life strategies, as well as a number of unique cytological features. My thesis focuses on two groups of closely related dinoflagellates: polykrikoids and warnowiids. Both include heterotrophic as well as plastid-bearing members, though the number of times photosynthesis has been lost (or gained) in each group is unclear, and the presence and provenance of plastids in some species (e.g., Nematodinium sp. and Polykrikos lebouriae) have been debated. Polykrikoids and warnowiids also contain some of the most complex subcellular structures described--such as nematocysts and, in warnowiids, eye-like ocelloids. Yet these groups are rare in nature and uncultivated, and as such, the origins of their complex organelles are unclear. For my thesis, I modified existing techniques for use on single-cell environmental isolates, and applied these techniques to wild polykrikoid and warnowiid cells. By exploiting the common splice leader sequence found on dinoflagellate transcripts, I was able to amplify a single-cell transcriptome from Polykrikos lebouriae—a dinoflagellate with aberrant plastids. Coupled with single-cell genomics using multiple displacement amplification (MDA), I demonstrated that Polykrikos lebouriae has retained peridinin-type plastids, while photosynthesis has been lost in multiple other polykrikoid species independently. Using MDA and single-cell transmission electron microscopy, I also determined that the eye-like ocelloid of Nematodinium sp. is made in part from a peridinin plastid, and also from mitochondria. Specifically, single-cell focused ion beam scanning electron microscopy (FIB-SEM) allowed me to demonstrate that a retina-like portion of the ocelloid is a small part of a much larger peridinin-plastid that ramifies throughout the Nematodinium cell. Lastly, I investigated the evolution of nematocysts in Polykrikos spp. and Nematodinium sp. using a combination of transcriptomics, TEM, SEM, and FIB-SEM, and inferred that “nematocysts” in these groups evolved independently from those in cnidarians. Thus, nematocyst-like extrusive organelles appear to have evolved multiple times in eukaryotes. The data presented in this thesis show how extreme subcellular complexity has evolved in dinoflagellates through both endosymbiotic and autogenous origins.
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Gregarine apicomplexans are a diverse but poorly understood group of single-celled parasites infecting a wide range of invertebrates in marine, freshwater and terrestrial environments. My thesis focuses on marine gregarines. Gregarines from marine hosts are unique because some (archigregarines) have maintained a set of pleisiomorphic characteristics from the ancestor of gregarines and apicomplexans alike. Other lineages of marine gregarines (eugregarines) are thought to have been modified from this archigregarine morphotype, and represent a wide-range of diversity with regard to general morphology, motility, and feeding strategies. My work has broadly applied molecular phylogenetics to novel species of marine gregarines from areas around British Columbia, Canada and Okinawa, Japan, with the goal of placing the evolution of gregarines in a molecular phylogenetic context. I amplified mainly SSU rDNA from a distinct life history stage (trophozoites), and coupled that with morphological data I gathered from light, confocal, as well as electron microscopy. Although my work was unable to resolve deep phylogenetic relationships among gregarines (and apicomplexans), this work did improve our understanding of evolution within gregarines. With the discovery of Veloxidium leptosynaptae from the gut of an echinoderm in Bamfield, British Columbia, and Surculinium glossobalanae from a hemichordate in Okinawa, I was able to show the paraphyly of the archigregarine morphotype, and polyphyly of other gregarine lineages, including some groups of neogregarines and eugregarines in terrestrial and freshwater environments. With the description Polyplicarium, my work uncovered and identified an ambiguous environmental sequence clade and, along with other work on Selenidium, was able to show that SSU rDNA can be reliably isolated from single cells as a method for delimiting closely related or morphologically similar species. In my final data chapter, I conducted an in-depth study on the morphology and molecular phylogenetic relationships between two sister species from the same host, Selenidium terebellae, and a newly discovered species, Selenidium melitzanae. Results from this data gave me the first opportunity to compare character evolution and niche partitioning among closely related gregarines, and provided another example of convergence of the eugregarine morphotype.
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The Euglenida is a diverse group of single celled eukaryotes with modes of nutrition that include phagotrophy, osmotrophy, and phototrophy. Phototrophic members of the group have attracted the most attention from previous researchers, and some species (e.g., Euglena gracilis) have become models in cell biology research. Phagotrophic euglenids, by contrast, are difficult to cultivate and manipulate so are severely underrepresented in culture collections, comparative ultrastructural studies, and molecular phylogenetic studies. Species discovery and the comparative ultrastructure of phagotrophic euglenids within a phylogenetic context were the main aims of this thesis. These data are essential for a comprehensive knowledge of the overall diversity and evolutionary history of euglenids as a whole, as well as for a better understanding of the relationships with their closest euglenozoan relatives, the Kinetoplastida and the Diplonemida. I generated DNA sequences of heat shock protein 90 and small subunit (SSU) rRNA genes from several different species of phagotrophic euglenids in order to evaluate some of the deepest branches in the phylogeny of euglenozoans, especially the phylogenetic position of Petalomonas cantuscygni. This species has a set of morphological features that are intermediate between kinetoplastids and euglenids (e.g., pellicle strips and kinetoplast-like mitochondrial inclusions). I also characterized the ultrastructure, feeding behaviour, and phylogenetic position of Heteronema scaphurum, a phagotrophic euglenid that feeds on green algal prey and is equipped with a distinctive “cytoproct” or cell anus. My explorations in low oxygen marine sediments led me to discover and characterize a novel lineage of euglenozoans, the “Symbiontida”. Members of this group formed intimate symbiotic relationships with at least two distinct types of epibiotic bacteria: rod-shaped epsilon-proteobacteria and spherical-shaped verrucomicrobia. I was able to show, using electron microscopy, that the verrucomicrobial symbionts were capable of evasive sporulation using a conspicuous extrusive apparatus that consisted of a thread tightly wound around a central core of DNA. The highly similar episymbionts reported previously on a group of ciliates led to questions about host transfer and the convergent evolution of extrusive organelles across the tree of eukaryotes.
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No abstract available.
In an effort to better understand character evolution in the cytoskeleton (pellicle) of euglenid protists, I used comparative and descriptive methods to investigate the morphological diversity and development of pellicle surface patterns formed by differences in strip length at the anterior and posterior ends of the cell (strip reduction). By observing dividing Euglena gracilis cells with scanning electron microscopy (SEM) and integrating these data with previous evolutionary and developmental research, I showed that these patterns result from the semiconservative duplication and subsequent intermittent growth of pellicle strips during cytoskeletal replication and cytokinesis. Furthermore, simple changes in the developmental timing of this process (heterochrony) resulted in the diversity of posterior strip reduction patterns observed in phototrophic euglenids. This model was then used to interpret the results of two studies describing pellicle surface patterns in other photosynthetic taxa. The first was a morphological description of the complex linear pattern of posterior reduction in the benthic marine phototroph, Euglena obtusa. The second was an investigation of the evolution of bilaterally symmetrical, “clustered” strip reduction patterns in the rigid genus Phacus, examined in the context of maximum likelihood (ML) and Bayesian phylogenetic analyses of combined nuclear small subunit and partial large subunit ribosomal genes (SSU rDNA and LSU rDNA, respectively). These studies, taken together, show that strip length and other pellicle characters (such as pore placement) are strongly influenced by age and perhaps other developmental factors (such as parental strip identity and cell polarity), but the underlying genetics and molecular biology of these factors are completely unknown. Finally, SEM was used for the first time to describe prearticular strip projections, a pellicle character that has been extensively studied using transmission electron microscopy (TEM). The novel character state revealed by this study shows that the diversity of this pellicle character is still poorly understood. The structural complexity of the euglenid pellicle and the developmental and evolutionary processes that resulted in its astonishing diversity could make it an ideal model system for studying cytoskeletal evolution and development once a robust genetic research framework is constructed.
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Master's Student Supervision
Theses completed in 2010 or later are listed below. Please note that there is a 6-12 month delay to add the latest theses.
The Myzozoa is a monophyletic group of primarily single-celled eukaryotes that have adopted diverse modes of nutrition, such as vampire-like predation, photoautotrophy and parasitism. Most myzozoans fall into two major subgroups, dinoflagellates and apicomplexans, but several lineages fall outside of these groups, such as predatory colpodellids and parasitic squirmids. In this study, the 3-dimensional cytoskeletal organization of a squirmid lineage, namely Platyproteum vivax, was investigated with confocal laser scanning microscopy (CLSM). Platyproteum inhabits the intestines of Pacific peanut worms (Phascolosoma agassizii) and has traits that are similar to other distantly related lineages of intestinal parasites within the Myzozoa called ‘gregarine apicomplexans’ (i.e., Selenidium), such as conspicuous feeding stages, called "trophozoites", capable of dynamic undulations via a system of longitudinal microtubules. More detailed characterizations of these traits will refine inferences about convergent evolution in the intestinal parasites of marine invertebrates. For instance, SEM and CLSM micrographs of P. vivax revealed the presence of an inconspicuous flagellar apparatus and a uniform array of longitudinal microtubules organized in bundles (LMBs). Extreme flattening of the trophozoites and a consistent orientation of the anterior end provided a reliable way to distinguish the dorsal and ventral surfaces. CLSM data also revealed a novel system of microtubules oriented in the flattened dorsoventral plane. Most of these ‘dorsoventral microtubule bundles’ (DVMBs) had a punctate distribution in dorsoventral view and were evenly spaced along a curved line spanning the longitudinal axis of the trophozoites. This configuration of microtubules is novel amongst myzozoans and is inferred to function in maintaining the flattened shape and potentially facilitate dynamic undulations via microtubule sliding. Overall, this study revealed novel traits in the trophozoites of Platyproteum, such as a flagellar apparatus and a system of DVMBs, that are consistent with phylogenomic data showing that this lineage of intestinal parasites is only distantly related to Selenidium and other marine gregarine apicomplexans. Therefore, similarities in the trophozoites of Platyproteum and Selenidium, such as relatively large trophozoites capable of dynamic undulations and uniform arrays of superficial microtubules, reflect convergent evolution within the intestines of marine invertebrates.
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A wasting disease has devastated sea star populations across the Northeast Pacific coastline. In 2016, three novel Labyrinthulomycetes – saprobic marine protists linked to other wasting diseases – were found living on diseased sea star tissue of Pisaster ochraceus. This raised the question of whether these Labyrinthulomycetes are a causal factor in sea star wasting disease (SSWD). I hypothesized that Labyrinthulomycetes are a causal factor in SSWD because most Labyrinthulomycetes isolated from living tissue are parasitic to their hosts. If Labyrinthulomycetes are a causal factor in the SSWD of P. ochraceus, they could be: H1) parasites – indicated by Labyrinthulomycetes found living specifically on the dermal tissue of P. ochraceus (host-specific); or H2) facultative parasites – indicated by Labyrinthulomycetes isolated from P. ochraceus and nearby decaying organisms (generalists). If Labyrinthulomycetes are not a causal factor in SSWD – simply taking advantage of already decaying organisms (H3) – then their isolation from diseased sea star tissue would be a result from these protists being at the right place at the right time. An environmental survey was conducted of the Labyrinthulomycetes of the Pacific coast of British Columbia to assess this association. I sampled diseased sea star tissue (P. ochraceus) and nearby decaying organisms from the intertidal zones to determine if these Labyrinthulomycetes are host-specific (H1) or generalists (H2 and H3). Identical Labyrinthulomycetes were isolated from a variety of decaying organisms. More specifically, Oblongichytrium porteri – one of the first Labyrinthulomycetes isolated from sea star tissue in 2016 – was found to have a wide abundance at all sampling locations on diseased sea star tissue and a variety of nearby decaying organisms. I conclude that the Labyrinthulomycetes associated with diseased P. ochraceus tissue are generalists, thereby rejecting H1. Further inoculation experiments are needed to determine whether Labyrinthulomycetes are facilitative parasites involved in SSWD (H2), or if they are just taking advantage of the readily available decaying matter (H3).
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Haplozoans are intestinal parasites of a specific group of marine annelids, called maldanids. Haplozoans are dinoflagellates, yet distinctly abnormal. Dinoflagellates are traditionally considered free-living, photoautotrophs, unicellular, and have two flagella. Yet somehow, Haplozoans are parasitic, and possess a mysterious “multicellular” trophont stage, with no flagella. Their life cycle is also largely unknown; while there is a well-observed adult trophont stage, but our understanding of other life stages is speculative at best. The trophont possesses three different types of compartments that create a multicellular appearance: (1) a trophocyte at the anterior of the cell, (2) gonocytes that compose most of the body length, and (3) sporocytes at the posterior. To explore the unique characteristics of Haplozoon, and provide clarity into the life cycle, I collected LM, confocal, and SEM data. The LM and confocal fluorescent data revealed that haplozoans are in fact unicellular. They possess a single plasma membrane and have compartmentalized their cell using amphiesma. New compartments are added behind the most anterior compartment of the cell and become more mature as they are pushed towards the posterior of the cell. This is a striking example of convergent evolution with a group of “strobilized” multicellular parasites, the Cestoda (Platyhelminthes). This pattern of compartmental maturity suggests that the posterior-most compartment of the cell produces the subsequent life history stage. The confocal data demonstrated that haplozoans do possess flagellar basal bodies in the membrane of each compartment, evidence that supports the existence of a hypothetical free-living dinospore stage. A novel finding from fluorescent tubulin staining was the existence of a complex network of microtubules, concentrated in the trophocyte of the cell. These microtubules of the trophocyte, dubbed the microtubular basket, allows the trophocyte to manipulate its shape and provides the dexterity for the suction cup and stylet to function. These haplozoan ultrastructure discoveries provide novel understanding of this enigmatic protist and provide a foundation from which to continue future research.
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Rhabdocoel flatworms are abundant members of marine meiofaunal communities worldwide,contributing to a reservoir of biodiversity that thrives between grains of sand. However, theyare relatively understudied due to bias in meiofaunal sampling techniques and a lack oftaxonomic expertise. Here, five species of neodalyellid rhabdocoels were discovered fromintertidal habitats in British Columbia and characterised with molecular and morphologicaldata: Baicalellia solaris n. sp., Baicalellia daftpunka n. sp., Tamanawas kalipis n. sp.,Pogaina paranygulgus and Baicalellia pusillus. A molecular phylogenetic analysis usingmaximum likelihood and Bayesian inference on concatenated 18S and 28S rDNA sequencesprovided a framework for revising neodalyellid systematics and for inferring characterevolution within the group. Kleptoplasty, the phenomenon by which one organism stealsplastids from another, was discovered in the “solar panel worms” B. solaris and P.paranygulgus, representing just the second case in metazoans; kleptoplasty has only beendescribed previously in sacoglossan sea slugs. Using a combination of light and electronmicroscopy, I demonstrated that plastids were intracellularly sequestered in the parenchymaltissue. DNA barcoding of partial rbcL sequences demonstrated that the plastids were stolenfrom raphid pennate diatoms, which was consistent with plastid ultrastucture. Measurementsof oxygen consumption demonstrated that kleptoplasts remain functional for at least ten daysafter sequestration in B. solaris cells. Photosynthetic activity was of a similar magnitude to adense chlorophyte culture, indicating that photosynthetically-fixed carbon enhanced survivalin light-treated compared with dark-treated flatworms. Kleptoplasts ultimately lose functionand are digested; therefore, heterotrophy is required to replenish healthy populations ofkleptoplasts within the host tissue. The kleptoplasts might serve as a food store, providingsustenance when seasonal diatom blooms collapse. It cannot be determined whetherkleptoplasty arose once in the common ancestor of Pogaina and Baicalellia or has evolvedtwice convergently.
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Apicomplexans are diverse single-celled eukaryotes that parasitize animals. The most notorious members include those of particular human interest such as the causative agents of malaria, toxoplasmosis, and cryptosporidiosis. While a subset of apicomplexans has been intensively studied from a medical or veterinary perspective, the diversity of remaining groups is underrepresented in existing literature. This lack of data has left the deep relationships among apicomplexan taxa enigmatic and in turn has hindered the revelation of some major evolutionary processes that sparked the apicomplexan radiation. The dearth of understanding surrounding apicomplexan systematics can be addressed in part through the discovery of novel species and the identification of how morphological and molecular characters are distributed across the apicomplexan phylogeny. Some lineages of marine gregarines have retained plesiomorphic characters that offer unique insight into the earliest stages of apicomplexan evolution. The current thesis describes and establishes two novel marine gregarine species isolated from a polychaete hosts (Lumbrineris inflata). Species delimitation and description was based on morphological data acquired using light and electron microscopy and a molecular phylogenetic analysis of 18S small subunit (SSU) rDNA sequences. Paralecudina anankea n. sp. possessed an elongated body, an oval nucleus, and gliding motility. The sister relationship of P. anankea n. sp. with P. polymorpha was robustly supported by molecular phylogenetic analysis (100 MLB, 1.00 BPP) and the SSU rDNA sequences between the two were 12% divergent. In contrast, L. caspera n. sp. was morphologically dissimilar to its closest relative L. longissima and possessed an acorn-shaped body, a distinct mucron, and gliding motility. Molecular phylogenetic analysis recovered L. caspera n. sp. as a sister species to L. longissima with strong support (100 MLB, 1.00 BPP) and their SSU rDNA sequences which were 8% divergent. The generation of additional morphological and molecular traits in gregarines will improve the phylogenetic resolution of the apicomplexan backbone and improve inferences about the evolutionary transition from photosynthetic ancestors to obligate parasites.
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Dicyemids are enigmatic parasites found only within the excretory systems of benthic cephalopods. Over the past century, dicyemids have been considered to be either complex protozoa, “mesozoa” that are ambiguously intermediate between protozoa and metazoa, or reduced metazoans. The phylogenetic position and overall diversity of dicyemids is poorly understood. Current species identification criteria are unconvincing because they are based solely on morphological traits. I set out to test current morphological species concepts with DNA barcodes from dicyemids collected from Pacific Northwest cephalopods. Variation within sequences of the small subunit (18S) rRNA gene was explored because this marker (1) is known to be fast-evolving in parasitic eukaryotes, (2) is one of the few molecular markers to have been previously sequenced in some dicyemids, and (3) has been used successfully as a barcode in other groups of parasites. Three host species of cephalopods were collected in this study, each hosting multiple historical morphospecies of dicyemid parasites. Thirty-four individual dicyemids encompassing eight morphospecies were isolated and their 18S rDNA sequenced. Molecular phylogenetic analyses of these data were incongruent with current morphology-based species concepts. The 18S rDNA sequences suggest that each host species of cephalopod harbors only one species of dicyemid with a great deal of morphological variation. However, the 18S rDNA sequences should eventually be tested with other rapidly evolving molecular markers. Attempts were made to sequence the mitochondrial cytochrome oxidase I (COI) gene, the mitochondrial 16S rRNA gene, and both Internal Transcribed Spacers (ITS) of the nuclear rRNA operon. With so little of the dicyemid genome known, I was unable to establish reliable primer pairs for these genes within the time constraints of my MSc thesis. Nonetheless, this study has shown that DNA barcoding is a powerful tool for the delimitation of dicyemid species. Understanding the diversity of parasite species is particularly problematic because they tend to be devoid of consistent (informative) morphological traits while simultaneously rich in morphological variation associated with developmental stages and environmental conditions. The addition of DNA barcodes to dicyemid diversity will simplify and improve species boundaries in a lineage that is difficult to define in every aspect.
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Scyphozoan jellyfish are a major group of large, bloom-forming marine animals that can disrupt ecological stability and interfere with marine-oriented industries. The widespread geographical distributions and high degrees of morphological plasticity within many species make understanding the overall diversity of scyphozoans difficult. Molecular phylogenetic approaches have the potential to offer powerful insights into many aspects of scyphozoan biology, such as species identification, evolutionary history, and phylogeography that will improve our ability to monitor and manage the roles these animals play in marine ecosystems. We established datasets of 16S rDNA and cytochrome c oxidase subunit I (COI) sequences of several different species of scyphozoans in order to better understand phylogenetic, phylogeographical, and taxonomic patterns within the group. Phylogenetic analysis of 16S rDNA sequences resolved closely related taxa but was too variable to resolve deeper relationships with robust statistical support. Combining this marker with a more conserved dataset of nuclear 18S rDNA sequences resulted in a phylogenetic tree with clades that had higher statistical support than in trees inferred from each marker alone. 16S rDNA sequences also showed phylogeographical patterns in Cyanea, distinguishing clearly between a Northeastern Pacific (NEP) clade and a Northwestern Atlantic clade (NWA) (9.71 - 9.93% mean genetic difference MGD), as well as two Atlantic subclades (NWA1, NWA2) (1.79% MGD). Distances within clades ranged from 0.05 - 0.2%. Therefore, 16S rDNA sequences were able to delimit different (putative) species that reflected distinct geographical distributions. In addition, comparative analyses of morphological features and COI sequences from Northeast Pacific isolates of Cyanea demonstrated that C. ferrugenia is a valid lion’s mane species found in the Northeast Pacific Ocean.
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