The ecology, life history, and phylogeny of the marine thecate heterotrophic dinoflagellates Protoperidinium and Diplopsalidaceae (Dinophyceae)
Gribble, Kristin E.
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Marine thecate heterotrophic dinoflagellates likely play an important role in the consumption of primary productivity and in the trophic structure of the plankton, yet we know little about these species. This thesis expanded our understanding of the autecology and evolutionary history of the Protoperidinium and diplopsalids. The distributions of Protoperidinium species off the southwestern coast of Ireland were influenced by physical oceanographic conditions coupled with the availability of preferred prey. The distributions of individual Protoperidinium species varied widely from the distribution of total Protoperidinium, indicating differences in ecologies among species. Certain species of Protoperidinium co-occurred with known preferred phytoplankton prey species. Concentrations of other Protoperidinium species were not related to those of any particular phytoplankton species, indicating that these Protoperidinium may rely on phytoplankton or other food sources beyond those already known, may not be species specific selective feeders, or may have become uncoupled from their preferred prey. The description of the sexual and asexual life history of Protoperidinium steidingerae provided the first account of the life history of any Protoperidinium species. Asexual division occurred by eleutheroschisis within a temporary, immotile cyst, yielding two daughter cells. Daughter cells were initially round and half to two-thirds the size of parent cells, then rapidly increased in size, forming horns before separating. Sexual reproduction was constitutive in clonal cultures, indicating that the species may be homothallic. Fusing gametes were isogamous, and resulted in a planozygote with two longitudinal flagella. Hypnozygotes had a mandatory dormancy period of ca. 70 days. Germination resulted in planomeiocytes with two longitudinal flagella. Nuclear cyclosis may occur in the planomeiocyte stage. A high level of morphological diversity among life history stages of P. steidingerae has led to mis-classification and taxonomic inaccuracy of Protoperidinium species identified from field samples. The large subunit ribosomal DNA (LSU rDNA) molecular phylogeny of the heterotrophic dinoflagellates revealed that the genus Protoperidinium appeared to be recently diverged within the dinoflagellates. In maximum parsimony and neighbor joining analysis, Protoperidinium formed a monophyletic group, evolving from diplopsalid dinoflagellates. In maximum likelihood and Bayesian analyses, however, Protoperidinium was polyphyletic, as the lenticular, diplopsalid heterotroph, Diplopsalis lenticula Bergh, was inserted within the Protoperidinium clade basal to Protoperidinium excentricum (Paulsen) Balech, and Preperidinium meunieri (Pavillard) Elbrächter fell within a separate clade as a sister to the Oceanica section and Protoperidinium steidingerae Balech. In all analyses, the Protoperidinium were divided into two major clades, with members in the Oceanica group and subgenus Testeria in one clade, and the Excentrica, Conica, Pellucida, Pyriforme, and Divergens sections in another clade. The LSU rDNA molecular phylogeny supported the historical morphologically determined sections, but not a simple morphology-based model of evolution based on thecal plate shape. LSU rDNA gene sequences are frequently used to infer the phylogeny of organisms. The many copies of the LSU rDNA found in the genome are thought to be kept homogenous by concerted evolution. In Protoperidinium species, however, there was high intragenomic diversity in the D1-D6 region of the LSU rDNA. For each species, the clone library was usually comprised of one highly represented copy and many unique sequences. Sequence differences were primarily characterized by single base pair substitutions, single base pair insertion/deletions (indels), and/or large indels. Phylogenetic analysis of all clones gave strong support for monophyly of the polymorphic copies of each species, and recovered the same species tree as an analysis using just one sequence per species. Analysis of LSU rDNA gene expression in three species by RT-PCR indicated that copies with fewer substitutions and fewer and smaller indels are expressed, and that 50% or more of the copies are pseudogenes. High intraspecific and intraindividual LSU rDNA sequence variability could lead to inaccurate species phylogenies and over-estimation of species diversity in environmental sequencing studies. This thesis has explored the ecology, life history, molecular phylogeny, and intraspecific DNA sequence variability of marine thecate heterotrohic dinoflagellates using a wide range of methodologies, including field sampling, culturing, microscopy, morphological analyses, histological staining, and molecular biology. The work here has broadened our understanding of the Protoperidinium and diplopsalids, providing new insights into the ecological and evolutionary relationships of these heterotrophs with other plankton species.
Submitted in partial fulfillment of the requirements for the degree Doctor of Philosophy at the Massachusetts and the Woods Hole Oceanographic Institution September 2006
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