Molecular and Morphological Investigations into the Evolution and Development of Red Algal Parasites

Jillian Freese, University of Rhode Island

Abstract

Symbiotic relationships occur on a spectrum from mutualistic to parasitic. Parasitism—where one organism benefits greatly and the other is potentially harmed—is the most common type of symbiosis found throughout the tree of life. Most of the well-studied parasites have detrimental impacts on agriculture and human health as the causative agents of disease. However, these pathogens do not represent the diversity of parasitism. Most eukaryotic parasites have a photosynthetic ancestry but lost the ability to carry out photosynthesis at some point in their transition to parasitism. These parasites have undergone significant morphological and genomic changes as a result of their parasitism—evolving mechanisms to enter host cells, genes to evade host defenses, and losing redundant pathways. But parasitic red algae are not like other parasites. Similar to other formerly photosynthetic parasites, they are diminished in size and have reduced or entirely lost pigmentation. However, their mechanism for entering host cells and close relationship to their host makes them unique among parasites. Red algal parasites and their hosts are members of the red algal class Florideophyceae, which is characterized by the presence of pit connections—cytoplasmic connections between cells. The success and diversity of red algal parasites may be due to the pre-existing mechanisms that facilitates their entry into host cells. The majority of red algal parasites are categorized as neoplastic parasites and infect a free-living red algal host within the same genus or a neighboring one. Even the more distantly related archaeplastic parasites infect a host in the same family. This close relationship has enabled direct comparisons between host and parasite to examine the effects of parasitism—overcoming a major challenge to studying parasite evolution. Since their discovery in the mid-19th century, red algal parasite research has mainly been focused on the morphology of reproductively mature parasites and placing them phylogenetically. This dissertation aimed to address the gaps in understanding the evolutionary relationships between red algal parasite and their hosts, parasite development, and the host response to infection. Chapter two focused on unraveling the phylogenetic relationships between members of the red algal parasitic genus Asterocolax and their hosts. Asterocolax is a parasitic genus, housing red algal parasites that infect host species in the Phycodrys group. Morphologically, these parasites are highly similar, but molecular data has shown their repeated independent evolution. Phylogenetically, Asterocolax species, and potentially many other parasites, resolve not within Asterocolax, but within the genera of free-living red algae, often the same genus as their host. Our phylogenetic analysis of the internal transcribed spacer region showed numerous independent evolutionary events from a photosynthetic ancestor. In response, we carried out the first taxonomic revision of an entire genus of parasitic red algae and proposed nomenclatural changes that would better reflect their true phylogenetic position. Chapter three and four used the red algal parasite Choreocolax polysiphoniae and its host, Vertebrata lanosa, as a model system for exploring parasite development and the host response to infection. A combined methodological approach using histology and transcriptomics visualized the morphological features of infection and changes in gene regulation throughout parasite development. Choreocolax polysiphoniae develops internal and external structures simultaneously—the internal cells actively infecting V. lanosa, while the external cells eventually house reproductive structures. Floridean starch is actively transported from infected V. lanosa to external C. polysiphoniae cells and eventually the parasite reproductive structures using saccharide membrane transporters and the endocytosis pathway. This active transfer of metabolites establishes a nutrient gradient that leads to the transfer of saccharides and floridean starch from neighboring uninfected V. lanosa to infected host cells. With decreased photosynthetic and carbohydrate metabolism pathways, infected V. lanosa is dependent upon these nutrients to prevent localized cell death. The use of histology and transcriptomics confirmed the parasitic nature of C. polysiphoniae, the role of V. lanosa in its successful development, and the host response to infection.

Subject Area

Parasitology|Developmental biology|Molecular biology

Recommended Citation

Jillian Freese, "Molecular and Morphological Investigations into the Evolution and Development of Red Algal Parasites" (2019). Dissertations and Master's Theses (Campus Access). Paper AAI27547557.
https://digitalcommons.uri.edu/dissertations/AAI27547557

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