Aggregation/dispersion transitions of T4 phage triggered by environmental ion availability

Abstract

BackgroundBacteriophage survives in at least two extremes of ionic environments: bacterial host (high ionic-cytosol) and that of soil (low ionic-environmental water). The impact of ionic composition in the micro- and macro-environments has not so far been addressed in phage biology.ResultsHere, we discovered a novel mechanism of aggregation/disaggregation transitions by phage virions. When normal sodium levels in phage media (150 mM) were lowered to 10 mM, advanced imaging by scanning electron microscopy, atomic force microscopy and dynamic light scattering all revealed formation of viral packages, each containing 20–100 virions. When ionic strength was returned from low to high, the aggregated state of phage reversed to a dispersed state, and the change in ionic strength did not substantially affect infectivity of the phage. By providing the direct evidence, that lowering of the sodium ion below the threshold of 20 mM causes rapid aggregation of phage while returning Na+ concentration to the values above this threshold causes dispersion of phage, we identified a biophysical mechanism of phage aggregation.ConclusionsOur results implicate operation of group behavior in phage and suggest a new kind of quorum sensing among its virions that is mediated by ions. Loss of ionic strength may act as a trigger in an evolutionary mechanism to improve the survival of bacteriophage by stimulating aggregation of phage when outside a bacterial host. Reversal of phage aggregation is also a promising breakthrough in biotechnological applications, since we demonstrated here the ability to retain viable virion aggregates on standard micro-filters.

The Removal of Endo- and Enterotoxins From Bacteriophage Preparations

“…This is probably due to reversible aggregation of fHoEco02 in the low-salt chromatography buffer, leading to underestimation in the phage titer. The phenomenon of aggregation of T4 phage in low-salt conditions was recently described by Szermer-Olearnik et al (2017). Interestingly, the same effect was not observed in the second purification strategy (1-octanol–ultrafiltration–chromatography–ultrafiltration), perhaps indicating that the residual octanol in the phage sample prevented the aggregation.…”

Nanoencapsulation of Bacteriophages in Liposomes Prepared Using Microfluidic Hydrodynamic Flow Focusing

“…Other studies have reported phage aggregation and formation of cluster rosettes (Serwer et al, 2007 ; Bourdin et al, 2014 ). Methods for dispersion of phage aggregates may help in this regard (Szermer-Olearnik et al, 2017 ).…”

Social Bacteriophages

“…In phages, collective spread can take place when multiple copies of the phage genomes are jointly encapsidated (polyphage), as shown in the filamentous coliphage f1 [43]. Also, changes in pH, temperature, or ionic strength in the environment can favor virion aggregation [44], as has been observed in the coliphages ØX174 [45], MS2 [46], and T4 [47]. Yet, the evolutionary implications of collective spread have been poorly studied in phages.…”