Iron-Virus Interactions in the Oceans

Iron is an essential nutrient in the oceans, with the sub-nanomolar concentrations found in open ocean surface waters often insufficient for supporting biological activity. More than 99.9% of dissolved iron is bound to organic ligands, yet identifying the sources of these ligands in seawater remains a major challenge. A significant portion of iron-binding ligands fall into the colloidal fraction, which is operationally defined as the fraction collected between a 0.02 µm and a 0.45 µm filter. Among the organic ligands in this fraction persists an extremely abundant biological candidate: viruses. On average there are 10⁷ viruses per milliliter of seawater, most of which are phages (viruses that infect bacteria). The impact of viruses on ocean biogeochemistry is often evoked purely through the act of lysing hosts and very few studies have considered the geochemical potential of the viral particles themselves. Recent work in non-marine model systems has revealed the presence of iron atoms within the structure of diverse phages infecting Escherichia coli. Combined with the small size and sheer abundance of phages in the oceans, the inclusion of iron in phage structures would translate into a major factor for cycling of this important trace metal. In addition, iron is so critical for growth that bacteria have evolved multiple uptake systems for assimilating iron, such as siderophores. Certain outer membrane proteins serve a dual function in siderophore uptake and as a phage receptor, suggesting that some of the strategies utilized for iron acquisition make bacteria vulnerable to phage infection. Given the constant arms race between bacteria and phages to develop resistance and counter-resistance, respectively, it is not surprising that phage would have evolved to utilize critical regions of surface-exposed proteins which are indispensable for bacterial growth as receptors. The research presented here explores the potential of marine phages to serve as iron-binding ligands and discusses the implications for both trace metal biogeochemistry and marine phage-host interactions.