The Ferrojan Horse Hypothesis: Iron-Virus Interactions in the Ocean

Abstract

Iron is an essential nutrient and the sub-nanomolar concentrations of iron in open ocean surface waters are often insufficient to support optimal biological activity. More than 99.9% of dissolved iron in these waters is bound to organic ligands, yet determining the identity of these ligands in seawater remains a major challenge. Among the potential dissolved organic ligands in the colloidal fraction captured between a 0.02 and a 0.2 µm filter persists an extremely abundant biological candidate: viruses, most of which are phages (viruses that infect bacteria). Recent work in non-marine model systems has revealed the presence of iron ions within the tails of diverse phages infecting Escherichia coli. Based on these findings and the presence of conserved protein motifs in marine phages, here we present several lines of evidence to support the hypothesis that phages are organic iron-binding ligands in the oceans. With average concentrations of 10 7 phages per milliliter surface seawater, we predict that phages could contain up to 0.7 pM iron, a value equivalent to as much as 70% of the colloidal fraction of organically complexed dissolved iron in the surface ocean. Additionally, the production and uptake of siderophores, a strategy that bacteria have developed for assimilating iron, renders cells vulnerable to phage infection due to the dual function of these cell surface receptors. Iron ions present in phage tails enable phages to exploit their bacterial host's iron-uptake mechanism via the "Ferrojan Horse Hypothesis" proposed herein, where the apparent gift of iron leads to cell lysis. Finally, if host iron stores are recycled during the assembly of progeny phages, as much as 14% of the cellular iron released into the water column upon lysis would already be incorporated into new phage tails. The potential role of phages as iron-binding ligands has significant implications for both oceanic trace metal biogeochemistry and marine phage-host interactions.

Vibrio Population Dynamics in Mid-Atlantic Surface Waters during Saharan Dust Events

“…This larger biomass is believed to be a liability, especially during bloom conditions, when they are preferentially preyed upon by eukaryotic protists and subject to viral lysis Yooseph et al, 2010). The interplay between addition of iron from dust deposition, bacterial iron uptake and viral infection is interesting in light of the recent proposed Ferrojan Hypothesis (Bonnain et al, 2016). This hypothesis suggests that viruses can adsorb free iron and then utilize bacterial iron-uptake receptors for infection in the manner of a Trojan Horse.…”

Toward a Regional Classification to Provide a More Inclusive Examination of the Ocean Biogeochemistry of Iron-Binding Ligands

“…Recent studies have suggested that polysaccharides, EPS as well as viruses could represent a significant pool of colloidal iron binding ligands (Benner, 2011;Hassler et al, 2011a;Bonnain et al, 2016). Indeed, iron associated with the tails of phages might mimic Fesiderophore complexes thus providing an efficient way to infect heterotrophic bacteria (Bonnain et al, 2016).…”

Phytoplankton Virus Production Negatively Affected by Iron Limitation

“…For example, non-marine tailed bacteriophages have been found to contain iron ions in the tail proteins that can utilize the siderophore-bound iron receptors on the host cell membrane for attachment of the phage and subsequent infection of the bacterial host (Bartual et al, 2010). It is likely that similar interactions also exists for marine bacteriophages (Bonnain et al, 2016). Still open questions are whether such phages will obtain fewer iron ions in their tail under Fe-deprivation, and if this will negatively affect their infectivity.…”

“…Still open questions are whether such phages will obtain fewer iron ions in their tail under Fe-deprivation, and if this will negatively affect their infectivity. Furthermore, the recently proposed "Ferrojan Horse Hypothesis" by Bonnain et al (2016) posits that introduction of phageattached Fe may aid the host. More study is needed to test this theory and its potential interference with siderophore-specific uptake mechanisms and effect on Fe cycling.…”