Investigations on phytoplankton - giant virus interactions and dynamics

Abstract

Marine viruses have a profound impact on phytoplankton ecology and diversity. They are ubiquitous source of mortality, driving carbon and nutrient remineralization, and carbon sequestration to the deep ocean. They are also agents of evolutionary changes and genetic diversification through horizontal gene transfer. Despite recent appreciation of the ecological role of marine viruses, there is still limited knowledge of host-virus microscale interactions and environmental dynamics for most marine viruses. Progress on these fronts is hampered by the limited number and diversity of virus isolates and challenges in ecological monitoring. We leveraged existing cultures of host-virus systems, including a green alga and a dinoflagellate, to investigate various aspects of the virus particles (virions) as well as the phytoplankton-virus interactions during infection. Here, we focused on giant viruses belonging to the Nucleocytoplasmic Large DNA Viruses (NCLDVs), formally classified as Phylum Nucleocytoviricota. We focused on giant viruses because of their diversity, which exceeds that of marine prokaryotes, and their immense coding capacity compared to other viral taxa. Because they code for unusually large number and diverse types of metabolic genes, giant viruses could have a significant influence on plankton metabolism and, consequently, on global biogeochemical cycles. We documented the ultrastructural changes in the green alga Tetraselmis when infected by the virus, TetV-1. We analyzed the temporal gene program of TetV-1 as well as the host transcriptional response leading to an improved mechanistic understanding of the infection process. We also conducted a genomic and structural analysis of a novel giant virus with a micron-length tail, PelV-1, that infects the dinoflagellate Pelagodinium. PelV-1 is a pleiomorphic virus that enters the cell through a phagocytosis-like mechanism and a tail that potentially develops independently of the host. Interestingly, PelV-1 encodes for numerous auxiliary metabolic genes, including light-harvesting complex, rhodopsin, tail-fiber proteins, and carbohydrate and lipid metabolism genes. We further expanded our investigations from lab-based model systems to a natural ecological setting, examining the associations of giant viruses to harmful algal bloom event, a fish kill, and monsoon seasons. We uncovered 82 giant virus metagenome-assembled genomes belonging to thirteen NCLDV families in a tropical coastal environment. We found evidence of associations between several phytoplankton-giant virus pairs and found a strong seasonal influence on phytoplankton-giant virus community structure. Overall, this dissertation highlights the diverse mechanisms and microscale interactions that ultimately influence ocean-scale processes, specifically advancing our understanding of phytoplankton-giant virus interactions and dynamics.