The role of viruses in phytoplankton community structure

Phytoplankton are important for marine nutrient cycles and ocean biogeochemistry. The community structure of phytoplankton is determined by top-down processes (e.g. predation) and bottom-up factors (e.g. nutrient availability). Viruses play a role in top-down host mortality of phytoplankton in the viral shunt of oceanic nutrient cycles. However, viruses can also affect bottom-up processes influencing phytoplankton communities through auxiliary metabolic genes (host-derived genes) which allow the hosts function to be altered. This ability to alter host function is thought to increase viral fitness, as well as temporarily increasing the host fitness in some cases.

Nitrogen and phosphorus are essential nutrients for phytoplankton but are often limited. Nutrient limitation results in competition between phytoplankton and has led to the evolution of strategies to maximise nutrient uptake, including nitrogen and phosphorus transporters. As nutrients are also important for virus replication and phytoplankton viral genomes have already been shown to contain phosphorus transporters derived from phytoplankton hosts, Monier et al. hypothesised that nitrogen transporters derived from phytoplankton hosts would also be found in phytoplankton viral genomes.

To investigate this hypothesis, viral amino acid sequence databases were searched for the main nitrogen transporter protein families. Searches identified one nitrogen transporter (vAmt) from the OtV6 viral genome; its presence was confirmed using targeted PCR amplification. OtV6 infects the phytoplankton Ostreococcus tauri; RT-PCR on infected and uninfected cultures confirmed that the vAmt gene was expressed during infection. Evidence was collected for the role of vAmt as an NH⁺₄ transporter based on its sequence and predicted structure and also as a potential transporter of a range of other nitrogen sources. vAmt was confirmed to be functional by comparing the growth of a yeast mutant (NH⁺₄ transporters deleted) with either the vAmt gene or an empty vector added; vAmt addition increased growth and culture density. Comparing NH⁺₄ uptake rates, using methylammonuim as a proxy, of the yeast mutant with either the vAmt gene added or its homolog in O. tauri showed uptake by the viral transporter was higher at low concentrations suggesting that vAmt can alter nitrogen uptake in infected host cells; this was confirmed in experiments using O. tauri. By reconstructing phylogenetic trees, the authors demonstrated that OtV6 acquired vAmt from O. tauri, most likely by host-to-virus horizontal gene transfer.

In summary, the authors showed that the O. tauri virus (OtV6) contains a host derived transporter protein (vAmt) that uptakes nitrogen; expression of vAmt during infection alters the nutrient uptake of the host, indicating that viruses play a role in determining phytoplankton community structure not only by top-down mortality but also by influencing nutrient uptake. However, as their database searches only identified one nitrogen transporter protein in viral amino acid sequences, the extent to which virus influence nitrogen uptake in phytoplankton does not appear to be common. While this may be the case, it may also be a result of the sampling method as only the main nitrogen transporter families were searched for in sequence databases so those belonging to other families would not be identified. Additionally, as not all viral genomes have been sequenced the extent of host-derived nitrogen transporters in viruses may be underestimated. Even if host-derived nitrogen transporters are rare, auxiliary metabolic genes affecting other aspects of hosts function have been identified (including phosphate uptake), so there are potentially numerous ways viruses could influence phytoplankton communities.

Reviewed Paper:

Monier, A., Chambouvet, A., Milner, D. S., Attah, V., Terrado, R., Lovejoy, C., Moreau, H., Santoro, A. E., Derelle, E. & Richards, T. A. (2017). Host-derived viral transporter protein for nitrogen uptake in infected marine phytoplankton. Proceedings of the National Academy of Sciences, 114(36), E7489-E7498.