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

Abstract

Phytoplankton community structure is shaped by both bottomup 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.Phycodnaviridae | NCLDV | prasinophytes | Mamiellophyceae | lateral gene transfer

Demystifying Eukaryote Lateral Gene Transfer (Response to Martin 2017 DOI: 10.1002/bies.201700115)

“…We know of several mechanisms for the introduction of foreign DNA into eukaryotic genomes, and we have direct evidence for some of them occurring on a recent time scale. Eukaryotic genomes are littered with remnants of viruses and transposons that promiscuously hop between diverse eukaryotic host genomes, sometimes mobilizing host DNA in the process . Conjugation between bacteria and eukaryotes in nature is well documented and can be reproduced under laboratory conditions (reviewed in ref.…”

Nutrient stoichiometry shapes microbial coevolution

“…Many phage contain auxiliary metabolic genes that modify a host's resource allocation (Monier et al . ). For example, phage‐encoded genes for phosphorus acquisition ( pstS and phoA ) were upregulated when phosphorus‐starved marine Prochlorococcus was infected by phage P‐SSM2 (Zeng & Chisholm ).…”

Visualization of viral infection dynamics in a unicellular eukaryote and quantification of viral production using VirusFISH

“…We designed probes to detect OtV5, but the alignment of the probes with other Prasinovirus genomes showed that they can very likely label all 11 genome sequenced Ostreococcus spp. viruses (Table S2 and Table S3), except OtV6, which is evolutionarily distinct (Monier et al , 2017). Thus, our technique may help in fostering our knowledge on the role of viruses in the control of the abundance of the cosmopolitan Ostreococcus spp.…”

“…Currently available methods to assess the dynamics between host and viruses during infection are i) the frequency of visibly infected cells (FVIC) (Wommack and Colwell, 2000), ii) Real Time PCR (RT-PCR) (Monier et al , 2017) of viral genes and iii) the plaque assay, for counting plaque forming units (PFU) (Brussaard et al , 2016). Compared with these methods, VirusFISH brings further advantages.…”