Host-derived viral transporter protein for nitrogen uptake in infected marine phytoplankton

This is the author's accepted manuscriptFinal version available from NAS via the DOI in this recordPhytoplankton community structure is shaped by both bottom–up factors, such as nutrient availability, and top–down processes, such as predation. Here we show that marine viruses can blur these distinctions, being able to amend how host cells acquire nutrients from their environment while also predating and lysing their algal hosts. Viral genomes often encode genes derived from their host. These genes may allow the virus to manipulate host metabolism to improve viral fitness. We identify in the genome of a phytoplankton virus, which infects the small green alga Ostreococcus tauri, a host-derived ammonium transporter. This gene is transcribed during infection and when expressed in yeast mutants the viral protein is located to the plasma membrane and rescues growth when cultured with ammonium as the sole nitrogen source. We also show that viral infection alters the nature of nitrogen compound uptake of host cells, by both increasing substrate affinity and allowing the host to access diverse nitrogen sources. This is important because the availability of nitrogen often limits phytoplankton growth. Collectively, these data show that a virus can acquire genes encoding nutrient transporters from a host genome and that expression of the viral gene can alter the nutrient uptake behavior of host cells. These results have implications for understanding how viruses manipulate the physiology and ecology of phytoplankton, influence marine nutrient cycles, and act as vectors for horizontal gene transfer.A.M. and T.A.R. are funded by the Royal Society, through Newton and University Research fellowships, respectively. This work is supported in part by research grants from The Gordon and Betty Moore Foundation (GBMF5514), Leverhulme Trust (PLP-2014-147), and the University of Exeter. The University of Exeter OmniLog facility is supported by a Wellcome Trust Institutional Strategic Support Award WT105618MA. Phylogenetic reconstructions were computed on the Data Intensive Academic Grid (National Science Foundation, MRI-R2 Project DBI-0959894)