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A New Perspective on Lysogeny: Prophages As Active Regulatory

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A New Perspective on Lysogeny: Prophages As Active Regulatory PERSPECTIVES that do enter the lysogenic cycle, sponta- OPINION neous induction of lytic production can still occur in the absence of an obvious A new perspective on lysogeny: stressor13,14. Phage genome excision and integration prophages as active regulatory are crucial steps in the onset of the lytic and lysogenic cycles, respectively. These events are mediated by phage-encoded DNA switches of bacteria recombinases, such as integrases and excisio- nases, and take place at a specific attachment Ron Feiner, Tal Argov, Lev Rabinovich, Nadejda Sigal, Ilya Borovok and site in the bacterial genome (attB), which is Anat A. Herskovits identical to an attachment site (attP) in the phage genome15. Although these sequences Abstract | Unlike lytic phages, temperate phages that enter lysogeny maintain a determine the phage specificity to the bacte- long-term association with their bacterial host. In this context, mutually beneficial rial genome, secondary sites can be used if interactions can evolve that support efficient reproduction of both phages and the original attB site is lost, as was shown 16 bacteria. Temperate phages are integrated into the bacterial chromosome as with Escherichia coli phage λ . Moreover, some phages integrate randomly within their large DNA insertions that can disrupt gene expression, and they may pose a host genome, such as phage Mu, and thus fitness burden on the cell. However, they have also been shown to benefit their increase variation and possible mutations bacterial hosts by providing new functions in a bacterium–phage symbiotic within the bacterial population17. interaction termed lysogenic conversion. In this Opinion article, we discuss Another documented, but less common, another type of bacterium–phage interaction, active lysogeny, in which phages phage life cycle is pseudolysogeny, which or phage-like elements are integrated into the bacterial chromosome within represents an unstable situation in which the phage genome fails to replicate as in lytic critical genes or operons and serve as switches that regulate bacterial genes via production or to become established as a genome excision. prophage18,19. This occurs most frequently under nutrient-deprived conditions, when Bacterial viruses, or phages, were first discov- released through bacterial lysis (FIG. 1a). By bacterial cells cannot support DNA rep- ered by Fredrick Twort and Felix D’Herelle in contrast, temperate phages can enter a lyso- lication or protein synthesis. The phage 1915 and 1917, respectively1,2. Soon after, it genic cycle, during which the phage genome genome remains as a non-integrated and became clear that phages are pivotal to many is integrated into the bacterial chromosome non-replicating preprophage, which resem- aspects of bacterial evolution. Subsequent to become a prophage, and persist in what bles an episome, until the nutritional status studies illustrated the never-ending con- is considered a latent or dormant state that is restored, at which point the phage enters flict between phages and bacteria, which is does not promote cell death or the produc- either a lysogenic or a lytic life cycle20 (FIG. 1c). evident from the plentiful ‘scars’ of phage tion of phage particles (FIG. 1b). Of note, Phages are natural predators that exploit remnants in bacterial genomes and the vari- some prophages persist as low copy number bacterial cells for growth. This phenomenon ety of defence mechanisms acquired by each plasmids and do not integrate into the bac- generates a predation pressure that enhances adversary3–6. terial chromosome (for example, P1 and natural selection, as the acquisition of a Bacteria and phages are two of the most N15 phages)10,11. Prophages are replicated defence mechanism by the bacteria could abundant and genetically diverse entities together with the bacterial host chromo- potentially lead to near extinction of the known to exist in biology, with phages some, and this lysogenic state is maintained phages, and, conversely, an increase in phage exceeding bacteria in number by tenfold (the by the repression of the phage lytic genes. A virulence risks the extinction of the bacterial number of phage particles is estimated to be switch to lytic production is initiated when population. Evolution of bacteria and phages in the order of 1031)7,8. Phages are obligate stressful conditions (that is, DNA damage)12 is thus driven by co‑adaptation that supports parasites that can typically sustain two dis- induce the excision of the phage genome, the reproduction of both6. This bacterium– tinct life cycles — lytic and lysogenic — as which is followed by the expression of lytic phage co‑evolution is extremely rapid, owing defined by their genetics and interaction genes that promote DNA replication, phage to the high turnover rates of phage infec- with the bacterial host9. particle assembly, DNA packaging and bac- tions (for example, an estimated 1024 pro- Upon infection, lytic phages immedi- terial lysis. It is important to view temperate ductive phage infections per second in the ately enter a productive cycle, in which the phages as heterogeneous populations as not oceans), as well as the short generation times phage genome is replicated and packaged all temperate phages enter the lysogenic and high mutation rates of bacteria and into progeny phage particles that are then cycle upon infection. Even for those phages phages6,21,22. The extent of bacterium–phage NATURE REVIEWS | MICROBIOLOGY VOLUME 13 | OCTOBER 2015 | 641 © 2015 Macmillan Publishers Limited. All rights reserved PERSPECTIVES a Lytic bacterium–phage co‑existence is beginning Phage capsid to emerge, which we term ‘active lysogeny’. Bacterial In this case, temperate phages are integrated genome within bacterial functional genes, and thus Phage genome need to cooperate with their hosts to regu- late the proper and timely expression of the disrupted genes. Active lysogeny results in a highly controlled rearrangement of phage Capsid and tail proteins genomes that is distinct from spontaneously occurring phage genome rearrangements. Lysis In this Opinion article, we focus on this Assembled phage newly described bacterium–phage interac- tion and propose that the integration and Phage genome excision of prophages in active lysogeny can be viewed as a molecular switch that regu- lates bacterial genes. This phage regulatory b Lysogenic switch (phage‑RS) mechanism represents a unique example of bacterium–phage Prophage co‑evolution that is specific to lysogeny, but distinct from classic (that is, latent) lysog- Insertion eny, and one in which both parties benefit: the bacteria acquire enhanced fitness and the phages ensure their own survival. It is Dormant state c Pseudolysogenic important to note that some examples dis- cussed here are not bona fide phages but are Non-replicating preprophage instead cryptic or defective phages that con- Nutrient-rich Lytic tain viral elements, such as phage integrase conditions or recombinase genes, but are not competent for infection. Lysogenic Starved cell Lysogenic conversion and active lysogeny Figure 1 | The phage replication cycles. Schematic of lytic, lysogenicNature and Reviewspseudolysogenic | Microbiology cycles. Lysogenic conversion is the best-described a | Lytic phages immediately enter a productive cycle, in which the phage genome is replicated and example of a process that provides a mutu- phage capsid and tail proteins are synthesized using bacterial cell machineries; the phage genome is ally beneficial symbiotic interaction between then packaged into progeny phage particles, which are liberated via bacterial lysis. b | Temperate bacteria and phages. In lysogenic conversion, phages enter a lysogenic cycle, in which the phage genome is integrated into the bacterial chromo- a phage encodes factors that increase the some (becoming a prophage) and persists in what is considered a phage latent or dormant state that fitness and survival of the bacterial host24,25 does not promote cell death or production of phage particles. Prophages are replicated together with and that, in most cases, have no apparent the bacterial host chromosome during host cell replication and switch into lytic production upon exposure to DNA damage (not shown). c | Pseudolysogeny is an unstable situation in which the phage value for the phage itself. Although the most genome fails to replicate (as in lytic production) or become established as a prophage (as in lysogeny). common outcome of lysogenic conversion is Pseudolysogeny occurs most frequently under nutrient-deprived conditions, when bacterial cells can- protection from infection by other phages, not support DNA replication or protein synthesis. In this situation, the phage genome remains for an lysogenic conversion events have been extended period of time as a non-integrated preprophage, which resembles an episome, until the shown to influence almost every facet of nutritional status is restored, at which point the phage enters either a lysogenic or a lytic life cycle. bacterial life25,26. Importantly, the pseudolysogenic preprophage does not replicate and so is only inherited by one of The first example of lysogenic conversion the daughter cells following cell division (not shown). was documented in 1927 by Frobisher and Brown27, who showed that non-toxigenic streptococci can acquire scarlatinal toxin co‑evolution is best demonstrated by the that, despite the bacterium–phage evolution- when mixed with filtered supernatants of remarkable number of phage resistance ary conflict, phages profit
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