Geobacter-associated prophages confer beneficial effect on dissimilatory reduction of Fe(III) oxides

Abstract

The dissimilatory reduction of Fe(III) oxides driven by Fe(III)-reducing bacteria (FRB) is an important biogeochemical process that influences not only iron cycling but also the biogeochemical cycles of carbon, trace metals, nutrients and contaminants. Phages have central roles in modulating the population and activity of FRB, but the mechanism for phage-involved Fe(III) oxide reduction is still unclear. This work used a common FRB, Geobacter soli, to explore the roles and underlying mechanisms of FRB-harboring prophages in the dissimilatory reduction of Fe(III) oxides. Bioinformatic analysis predicted 185 phage-related genes in the G. soli genome, comprising functional prophages that were verified to be induced to form tailed phage particles. Ferrihydrite reduction was facilitated as prophage induction was stimulated and declined as prophage induction was inhibited, which indicated a positive role of G. soli-harboring prophages in Fe(III) oxide reduction. A comparison of gene expression and released phage particles in the cells grown with Fe(III)-citrate and ferrihydrite suggested that microbial ferrihydrite reduction would activate the SOS response and consequently induce the prophages to enter lytic cycles. The prophage-mediated lysis of the subpopulation resulted in an increased release of extracellular DNA and membrane vesicles that were conducive to Fe(III) oxide reduction, which might explain the positive role of prophages in ferrihydrite reduction. In summary, our results revealed the functional roles and underlying mechanisms of FRB-associated prophages in facilitating the dissimilatory reduction of Fe(III) oxides, which will advance our understanding of iron cycling in natural ecosystems.