The Significance of Mutualistic Phages for Bacterial Ecology and Evolution

Temperate phages can provide a plethora of benefits to bacterial hosts, including the ability to respond rapidly to changes in the environment. Bacterial biofilms can benefit from lysogeny. When phages are induced in a few cells, the lysing cells release nutrients and extracellular DNA locally, which may strengthen biofilm structure. Further, lysis breaks biofilm bonds, allowing for enhanced cell dispersal. In bacterial competition, phages can facilitate bacteriocin release or act as ‘weapons’ against competitors themselves. Recent evidence indicates that bacterial populations may modulate phage infections, as individual cells may lose immunity or selectively allow infections to occur. The capacity of CRISPR-Cas immune systems to discriminate between lytic and temperate phages (based on gene expression) may enable bacterial hosts to selectively permit temperate phages to enter. Bacteria and phages have traditionally been viewed as ‘antagonists’. However, temperate phages can transfer genes, which can broaden their bacterial hosts’ metabolic repertoire, confer or enhance virulence, or eliminate competing organisms, and so enhance bacterial fitness. Recent evidence shows that phages can also promote biofilm formation leading to population-level benefits for their bacterial hosts. Here, we provide a perspective on the ecological and evolutionary consequences for the bacteria interacting with phages, when phage and host interests are aligned. Furthermore, we examine the question whether bacterial hosts can lower immune barriers to phage infection, thereby facilitating infection by beneficial phages. Taking recent evidence together, we suggest that in many cases temperate phages are to be considered as being mutualistic as well as parasitic, at the same time. Bacteria and phages have traditionally been viewed as ‘antagonists’. However, temperate phages can transfer genes, which can broaden their bacterial hosts’ metabolic repertoire, confer or enhance virulence, or eliminate competing organisms, and so enhance bacterial fitness. Recent evidence shows that phages can also promote biofilm formation leading to population-level benefits for their bacterial hosts. Here, we provide a perspective on the ecological and evolutionary consequences for the bacteria interacting with phages, when phage and host interests are aligned. Furthermore, we examine the question whether bacterial hosts can lower immune barriers to phage infection, thereby facilitating infection by beneficial phages. Taking recent evidence together, we suggest that in many cases temperate phages are to be considered as being mutualistic as well as parasitic, at the same time. particle or chemical produced by a cell that influences the growth or survival of surrounding cells. co-evolutionary dynamics in which consecutive selective sweeps fix alleles in host and parasite populations. This is expected to result in rapid evolution with transient polymorphisms and low standing genetic variation. genes carried by phages that affect host metabolism, for example by increasing photosynthesis, nucleotide synthesis, or the biosynthesis of alternative electron acceptors. bacterial defense systems that target incoming foreign genetic material. Examples are enzymatic restriction–modification (R–M) systems, clustered regularly interspaced short palindromic repeat (CRISPR) loci and CRISPR-associated (CRISPR-Cas) immunity, and bacterial exclusion (BREX) systems. interference competition between bacteria, which may include the use of bacteriocins or phages that decrease growth or survival of competing strains or species. theoretical framework that assumes individuals optimize their long-term fitness by following strategies that reduce variance in fitness. evolutionary process in which interacting organisms evolve together as they reciprocally influence each other. genetic interaction in which the expression of a gene (and the resulting phenotype) depends on the genetic background. bacterial cell containing one or more prophages within its genome. phenotypic change in a host bacterium caused by the insertion of a phage. state of phage integration into the bacterial genome. bacterial virus, which, upon entering its host, produces offspring and lyses the bacterial cell to release its progeny. temperate phage integrated in the bacterial genome. co-evolutionary dynamics in which allele frequencies in host and parasite populations fluctuate cyclically. This is expected to result in stable polymorphisms and high standing genetic variation. bacterial immunity that tolerates infection by certain phages (e.g., temperate) whilst preventing infection of other (e.g., lytic) phages. prevention of a secondary infection by a phage through (phage-dependent) cell-surface modifications. bacterial virus that can integrate into a bacterial genome (or be maintained extrachromosomally), become stabilized in this way, and, upon receiving a cue, can excise and propagate. process of horizontal gene transfer, wherein a region of a bacterial genome is packaged into phage particles that, upon release and entrance into a new host, is inserted into the genome of the latter.