Iron Limitation Leads to Rusty Algal Viruses

Since Proctor and Fuhrman (1991) first exposed researchers to the significance of marine viruses in microbial energy flow, the importance of viral interactions in the ‘microbial loop’ has become increasingly well understood. The term ‘viral shunt’ was subsequently coined to refer to the redirection of carbon flow away from higher trophic levels by viral lysis to DOM/POM pools (see Suttle, 2007). Marine environments can be, however, chemically heterogeneous systems characterised by areas of micronutrient limitation preventing optimal biological activity – particularly iron (Fe), which exhibits poor solubility in seawater. Research is lacking as to how Fe limitation affects viral shunting, however a recent paper has aimed to remedy this.

Slagter and others (2016) explored the effect of Fe limitation on the infectivity of two dsDNA viruses (MpV and PgV) that infect globally abundant phytoplankton species (the prasinophyte Micromonas pusilla and the haptophyte Phaeocystis globosa respectively). Algal monocultures were cultivated under ecologically realistic Fe-limited or Fe-controlled media, and were later inoculated with viral lysates produced on Fe-limited or Fe-controlled host cultures. Infected cell cultures were monitored for viral infectivity (endpoint dilution assay) and pigment composition (high pressure liquid chromatography (HPLC) followed by spectroscopy). For both viruses, the ‘burst size’ (number of viral progeny lysed cell^‑1) was reduced ~30% under Fe-limitation, however only MpV exhibited reduced infectivity under the same treatment.

Interestingly, when Fe-control lysates were introduced into Fe-limited cell cultures, the acute spike in Fe concentration only partially aided the production of viral progeny and failed to counteract the deleterious effects of Fe-limitation, suggesting that the impaired physiological history of the host was a major factor in suppressing viral activity. This is supported by evidence from the HPLC pigment analysis, which shifted away from the production of photosynthetic primary pigments such as chlorophyll-a to photoprotective stress xanthophylls in both Fe-limited algal species, indicating a reversal from normal metabolic activity.

Overall, this study offered an intriguing insight into the effect of Fe-limitation on viral lysis and has implications in understanding the complexities of viral shunting. Iron is integral to central cellular metabolic pathways, by acting as a cofactor in enzymes involved in photosynthesis, respiration and DNA repair. The authors hypothesise that suppression of host metabolic processes through Fe-limitation would deleteriously affect virus production, which hijacks such machinery. However, I am cautious in accepting this explanation outright as investigations as to the viral particles’ intrinsic requirement for iron is lacking in this investigation. Some bacteriophages, for example, bind Fe atoms to proteinaceous fibrils to aid in host attachment and therefore the authors may be missing a contributory factor outside of host physiology. The ubiquity of the selected algal species makes them good choices for model organisms, however the differential response of the viruses in this study stresses the importance of further study in different algal supergroups and viral taxa. I would be fascinated to see this study repeated in diatoms, some species of which have evolved to survive environmental Fe-limitation by reducing their intracellular Fe-demand (Thalassiosira oceanica has replaced Fe-containing electron transport cytochromes with the copper-based plastocyanin). Would host resistance to Fe-limitation in turn support viral production?  Nevertheless, this study augments our understanding of the chemical complexities of viral shunting and provides researchers with a more thorough understanding of viral carbon flow in marine systems. 

Reviewed paper: Slagter, H. A., Gerringa, L. J., & Brussaard, C. P. (2016). Phytoplankton Virus Production Negatively Affected by Iron Limitation. Frontiers in Marine Science, 3, 156. http://journal.frontiersin.org/article/10.3389/fmars.2016.00156/full 

Further Reading:

Review of marine viruses: Suttle, C. A. (2007). Marine viruses—major players in the global ecosystem.Nature Reviews Microbiology, 5(10), 801-812. http://www.nature.com/nrmicro/journal/v5/n10/abs/nrmicro1750.html

Iron in a bacteriophage: Bartual, S. G., Otero, J. M., Garcia-Doval, C., Llamas-Saiz, A. L., Kahn, R., Fox, G. C., & van Raaij, M. J. (2010). Structure of the bacteriophage T4 long tail fiber receptor-binding tip. Proceedings of the National Academy of Sciences, 107(47), 20287-20292. http://www.pnas.org/content/107/47/20287.short

Plastocyanin in diatoms: Peers, G., & Price, N. M. (2006). Copper-containing plastocyanin used for electron transport by an oceanic diatom. Nature, 441(7091), 341-344.http://www.nature.com/nature/journal/v441/n7091/abs/nature04630.html