Phage or foe: an insight into the impact of viral predation on microbial communities

Abstract

Since their discovery, bacteriophages have been traditionally regarded as the natural enemies of bacteria. However, recent advances in molecular biology techniques, especially data from "omics" analyses, have revealed that the interplay between bacterial viruses and their hosts is far more intricate than initially thought. On the one hand, we have become more aware of the impact of viral predation on the composition and genetic makeup of microbial communities thanks to genomic and metagenomic approaches. Moreover, data obtained from transcriptomic, proteomic, and metabolomic studies have shown that responses to phage predation are complex and diverse, varying greatly depending on the bacterial host, phage, and multiplicity of infection. Interestingly, phage exposure may alter different phenotypes, including virulence and biofilm formation. The complexity of the interactions between microbes and their viral predators is also evidenced by the link between quorum-sensing signaling pathways and bacteriophage resistance. Overall, new data increasingly suggests that both temperate and virulent phages have a positive effect on the evolution and adaptation of microbial populations. From this perspective, further research is still necessary to fully understand the interactions between phage and host under conditions that allow co-existence of both populations, reflecting more accurately the dynamics in natural microbial communities.

Fig. 1

Examples of bacterial responses to phage exposure identified with different “omics” analyses. The drawing depicts a bacterial cell showing the physiological processes that changed upon phage predation. In most cases, there was a synchronized infection of the bacterial population with a virulent phage or induction of the lytic cycle in lysogenic bacteria. However, in the case of S. aureus, data represent differences between a biofilm subject to low-level predation with a lytic phage and a control biofilm

Fig. 2

Interplay between bacteriophages and bacterial biofilms. Cell aggregation may favor phage propagation in planktonic cultures or attached cells not surrounded by a matrix. (a) especially if phage pressure is high, resulting in complete eradication of the microbial population. However, arrangement of the cells in a mature biofilm will delay penetration of the viral particles and slow down the infection (b). When phage pressure is low, attachment to a surface may be the difference between life and death. Indeed, planktonic cells may eventually be eradicated by the virus (c) whereas the biofilm lifestyle may delay phage propagation thanks to the matrix and the lower metabolic rate of cells in deep layers of the biofilm (d). Moreover, there are examples of increased eDNA or polysaccharide production in response to viral predation (d) thereby enhancing biofilm formation and/or stability

Fig. 3

Regulation of phage susceptibility by quorum-sensing (QS) signaling. Bacterial cells control their antiphage strategy depending on cell density through QS signals. Thus, accumulation of QS molecules may trigger different strategies depending on the microorganism that will ultimately result in a greater ability of the bacterial population to withstand a phage attack