Date Awarded

Summer 2020

Document Type

Dissertation

Degree Name

Doctor of Philosophy (Ph.D.)

Department

Virginia Institute of Marine Science

Advisor

Andrew R Wargo

Committee Member

George B McManus

Committee Member

Kimberly S Reece

Committee Member

Jeffrey D Shields

Committee Member

Deborah K Steinberg

Abstract

Ciliates are basal eukaryotes from Phylum Ciliophora that were first described 400 years ago, but their origins date back 800 million years. Such early origins have allowed contemporary ciliates to be remarkably diverse in both their species numbers and ecological adaptations. Peritrichia, a subclass of ciliates, represents an ideal model to study ciliate diversity, as its members display complex phylogenetic relationships and can be epibionts colonizing the body surface of other organisms. Epibiotic relationships are ecologically and evolutionarily important due to the extensive adaptations in epibiont biology to the life cycles of hosts. These relationships are also important for host population dynamics, as peritrich epibionts can cause myriad detrimental effects on their hosts. The overall goal of this dissertation is to investigate peritrich ciliate distribution and ecology in Chesapeake Bay, as well as to examine epibiotic relationships with its copepod hosts in a multidisciplinary approach combining extensive sampling and molecular analyses. Zoothamnium intermedium, a peritrich epibiont, was used as an evolutionary and ecological model, as this species aggregates several of the obstacles found in the study of ciliates and several groups of basal eukaryotes. The ecological importance of ciliates is introduced in Chapter 1. Key points of their diversity and life history are presented to introduce the topics that will be discussed throughout this dissertation. Chapter 2 examines qualitative data on the seasonality and host preference of Z. intermedium along with relationships to water quality parameters in the York River, Virginia, USA. Results from plankton sampling showed that colonization by Z. intermedium was specific to Acartia tonsa and Centropages hamatus. Host identifiction was confirmed by analysis of the host mitochondrial cytochrome oxidase I gene. Analysis of the small subunit rDNA (SSU rDNA) sequences from the epibiont revealed identical sequences from specimens obtained from the two hosts. Both host species are calanoid copepods but are distributed differently in the water column. Colonization of hosts was uneven across all seasons, and was strongly correlated with dissolved oxygen, salinity, water temperature, and total suspended solids. The different life histories of the two copepod hosts species, coupled with the fact that a high number of free-living (non-epibiont) peritrichs were found in the settlement traps, led us to question the diversity of Z. intermedium and other peritrichs in water bodies of Chesapeake Bay. In Chapter 3, we broadened the molecular analysis to incorporate sequences from both epibiotic and free-living peritrich species. By using the same methods of sample collection from Chapter 2, we found new species of calanoid copepod host, different than the ones previously described for Z. intermedium in the York River. Eurytemora affinis and Undinula vulgaris, both calanoid copepods were also found as hosts for morphologically similar Z. intermedium. The diversity of the Z. intermedium sequences, however, did not follow an obvious distribution. SSU rDNA phylogenetic analysis showed a deep separation between sequences obtained from different A. tonsa populations, which has a cryptic species complex in Chesapeake Bay. Genus Zoothamnium was the most diverse peritrich genus in our samples, followed by genus Pseudovorticella. Such finding might not be aleatory, as previous studies have hypothesized that Zoothamnium and Pseudovorticella species are more common in brackish and marine waters as a result of their more recent invasion from freshwater habitats. Such results underscore the importance of a multidisciplinary approach in the understanding of ciliate-host relationships. Knowledge of species ecology and distribution aids molecular analysis in the best choice of genes to study ciliates with different life histories. In Chapter 4, the focus shifts to host microbiome and potential interactions with Z. intermedium. The microbiome of both colonized and uncolonized A. tonsa was analyzed by high throughput sequencing of bacterial 16S ribosomal RNA (16S rRNA). While dominant bacterial taxa and alpha diversity values were similar between colonized and uncolonized copepods, one ASV (Amplicon Sequence Variant), belonging to family Neisseriaceae, was present only in colonized hosts. The beta diversity analysis was also different, showing a significant separation of the 16S community structure, with different clusters of colonized and uncolonized copepods. Finally, Chapter 5 summarizes all research and main findings of the research conducted in the previous chapters and concludes by discussing such findings as a comprehensive unit. The results obtained in this dissertation provide new knowledge on the evolutionary and ecological diversity of peritrich ciliates, while emphasizing the need for a holistic view of microbial relationships to investigate aquatic ecosystems.

DOI

https://doi.org/10.25773/ncwd-yr51

Rights

© The Author

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