Publication Date:
2022-05-25
Description:
Submitted in partial fulfillment of the requirements for the degree Doctor of Philosophy at the Massachusetts and the Woods Hole Oceanographic Institution September 2006
Description:
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.
Description:
This thesis could not
have taken its current form without the financial freedom allowed me by Gary Comer’s
generous gift six years ago. Additional financial support was provided by the Carroll
Wilson Award from the MIT Entrepreneurship Society, the Cove Point Foundation, and National Science Foundation grant OCE-0136861.
Keywords:
Ecology
;
Dinoflagellates
Repository Name:
Woods Hole Open Access Server
Type:
Thesis
Format:
application/pdf
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