Genomic and functional characterization of giant viruses infecting mixotrophic nanoflagellates

Abstract

Phago-mixotrophy is a common metabolic strategy among phytoplankton in the oligotrophic ocean. This lifestyle strategy combines photosynthesis (autotrophy) and predation (heterotrophy), allowing mixotrophs to supplement their nutritional needs by consuming prey. Many giant viruses appear to exploit phagotrophic behavior as a mechanism for entry into the host cell to initiate an infection, which may explain why giant viruses appear to be the most successful type of phytoplankton-infecting virus in the oligotrophic ocean. Despite the ecological importance of mixotrophs and giant viruses, there is limited research on how nutrient conditions influence giant virus-mixotroph interactions. For my dissertation research, I leveraged a collection of novel virus-mixotroph systems isolated from the oligotrophic waters of the North Pacific Subtropical Gyre to investigate how host metabolism influences viral infection dynamics and giant virus evolution. Many mixotrophic algae exhibit trophic plasticity, shifting between auto- and mixotrophy based on dissolved nutrient availability, and therefore I hypothesized that mixotrophic hosts grown under prey-derived nutrient conditions would have increased susceptibility to viral infection. However, results showed that species-specific survival outcomes emerged when provoking autotrophic or phagotrophic host physiologies. Furthermore, this functional comparison revealed that one strain of virus was able to inflict a higher degree of host mortality across a suite of mixotrophs and environmental conditions, so I compared the giant virus genomes and identified an expanded set of virulence factors linked to gene duplications and insertions of mobile genetic elements. Lastly, I characterized the genome of a giant virus infecting an obligate mixotrophic chrysophyte. The giant virus encoded genes that appear to have been acquired from common marine proteo- and cyanobacteria. This genetic exchange suggested that the intracellular environment of the mixotrophic host may facilitate the transfer of genes from prey organism to viral pathogen. Together, these studies showed that metabolic plasticity can alter a mixotrophic host’s fitness and resistance to viral infection as well as provided insight into the mechanisms of giant virus virulence and gene acquisition.