Ecological and Evolutionary Benefits of Temperate Phage: What Does or Doesn't Kill You Makes You Stronger

Harrison, Ellie; Brockhurst, Michael A.

doi:10.1002/bies.201700112

Cited by 183 publications

(162 citation statements)

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“…Like Longfellow's “little girl who had a little curl” (Longfellow ), when temperate phages exploit their hosts, they are deadly; but they can also coexist with the host genome for generations, conferring growth and survival benefits (Harrison and Brockhurst ). In the parallel work, we have examined the critical role of prophage sequences in the evolution and co‐evolution of viruses and bacteria (Nadeem and Wahl ; Wahl and Pattenden ).…”

Section: Discussionmentioning

confidence: 99%

“…The mutant strain has a higher propensity for lysis, and consistent with the results described here, the mutant is favored when the number of susceptible host cells is high (early in the epidemic), and disfavored when susceptible host cells are rare. Like Longfellow's "little girl who had a little curl 1 " (Longfellow 1922), when temperate phages exploit their hosts, they are deadly; but they can also coexist with the host genome for generations, conferring growth and survival benefits (Harrison and Brockhurst 2017). In the parallel work, we have examined the critical role of prophage sequences in the evolution and co-evolution of viruses and bacteria (Nadeem and Wahl 2017;Wahl and Pattenden 2017).…”

Section: Discussionmentioning

confidence: 99%

“…About half of sequenced bacterial genomes carry one or more prophages (Touchon et al 2016). Prophage sequences can provide a number of fitness benefits to these hosts, encoding virulence factors, facilitating horizontal gene transfer, and acting as reservoirs of genetic material for evolutionary innovation (see Harrison and Brockhurst (2017) for review). Growth and survival benefits can be conferred by active prophages but also by cryptic prophages, that is, by prophage sequences that are mutationally degraded and can no longer be induced to form infectious virus (Wang et al 2010).…”

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confidence: 99%

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Evolutionary stability of the lysis‐lysogeny decision: why be virulent?

et al. 2018

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Lytic viruses infect and kill host cells, producing a large number of viral copies. Temperate viruses, in contrast, are able to integrate viral genetic material into the host cell DNA, leaving a viable host cell. The evolutionary advantage of this strategy, lysogeny, has been demonstrated in complex environments that include spatial structure, oscillating population dynamics, or periodic environmental collapse. Here, we examine the evolutionary stability of the lysis–lysogeny decision, that is, we predict the long‐term outcome of the evolution of lysogeny rates. We demonstrate that viruses with high rates of lysogeny are stable against invasion by more virulent viral strains even in simple environments, as long as the pool of susceptible hosts is not unlimited. This mirrors well‐known results in both r‐K selection theory and virulence evolution: although virulent viruses have a faster potential growth rate, temperate strains are able to maintain positive growth on a lower density of the limiting resource, susceptible hosts. We then outline scenarios in which the rate of lysogeny is predicted to evolve either toward full lysogeny or full lysis. Finally, we demonstrate conditions under which intermediate rates of lysogeny, as observed in temperate viruses in nature, can be sustained long‐term. In general, intermediate lysogeny rates persist when the coupling between susceptible host density and virus density is relaxed.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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confidence: 99%

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Evolutionary stability of the lysis‐lysogeny decision: why be virulent?

et al. 2018

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“…3-The prophage of temperate viruses can carry genes that in some environments augment the fitness of their host bacteria and thereby the fitness of the bacteriophage (specifically virulence factors [10][11][12] and drug-resistance cassettes [13,14], but including genes whose functions have not been identified [15,16]). 4-By induction and release of free phage, lysogeny can provide an advantage to its host population by allelopathy, killing members of susceptible competing populations [17][18][19][20][21]. There are, however, two major caveats to these arguments about a universal advantage of a temperate mode of phage replication and transmission relative to a purely lytic mode, both based on the conditions under which lytic phage might be able to invade a temperate population.…”

Section: Introductionmentioning

confidence: 99%

The population and evolutionary dynamics of bacteriophage: Why be temperate revisited

Chaudhry

Vega

Govindan

et al. 2019

Preprint

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Bacteriophages are deemed either lytic (virulent) or temperate, respectively depending on whether their genomes are transmitted solely horizontally, or both horizontally and vertically. To elucidate the ecological and evolutionary conditions under which natural selection will favor the evolution and maintenance of lytic or temperate modes of phage replication and transmission, we use a comprehensive mathematical model of the dynamics of temperate and virulent phage in populations of bacteria sensitive and resistant to these viruses. For our numerical analysis of the properties of this model, we use parameters estimated with the temperate bacteriophage Lambda, l, it's clear and virulent mutants, and E. coli sensitive and resistant -refractory to these phages. Using batch and serial transfer population dynamic and reconstruction experiments, we test the hypotheses generated from this theoretical analysis. Based on the results of this jointly theoretical and experimental study, we postulate the conditions under which natural selection will favor the evolution and maintenance of lytic and temperate modes of phage replication and transmission. A compelling and novel prediction this in silico, in vitro, and in plastico study makes is lysogenic bacteria from natural populations will be resistant-refractory to the phage for which they are lysogenic as well as lytic phage sharing the same receptors as these temperate viruses.

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“…As such, they constitute an important mechanism underlying HGT in addition to conjugation, natural competence, and bacteriophage‐mediated transduction (Sun, ; von Wintersdorff et al, ). It is generally accepted that GTAs originate from defective temperate prophages, in a process that has been conceptualised as “prophage domestication” (Bobay, Touchon, & Rocha, ; Harrison & Brockhurst, ; Olszak, Latka, Roszniowski, Valvano, & Drulis‐Kawa, ). Their independent emergence in different bacterial lineages constitutes a striking example of convergent evolution (Lang et al, ), which can be compared with the recurrent evolution of host‐interacting secretion systems from conjugative systems or from bacterial flagellum (Abby & Rocha, ; Frank, Alsmark, Thollesson, & Andersson, ).…”

Section: Origin and Evolution Of Bagtamentioning

confidence: 99%

Bartonellagene transfer agent: Evolution, function, and proposed role in host adaptation

Québatte

Dehio

2019

Cellular Microbiology

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The processes underlying host adaptation by bacterial pathogens remain a fundamental question with relevant clinical, ecological, and evolutionary implications. Zoonotic pathogens of the genus Bartonella constitute an exceptional model to study these aspects. Bartonellae have undergone a spectacular diversification into multiple species resulting from adaptive radiation. Specific adaptations of a complex facultative intracellular lifestyle have enabled the colonisation of distinct mammalian reservoir hosts. This remarkable host adaptability has a multifactorial basis and is thought to be driven by horizontal gene transfer (HGT) and recombination among a limited genus‐specific pan genome. Recent functional and evolutionary studies revealed that the conserved Bartonella gene transfer agent (BaGTA) mediates highly efficient HGT and could thus drive this evolution. Here, we review the recent progress made towards understanding BaGTA evolution, function, and its role in the evolution and pathogenesis of Bartonella spp. We notably discuss how BaGTA could have contributed to genome diversification through recombination of beneficial traits that underlie host adaptability. We further address how BaGTA may counter the accumulation of deleterious mutations in clonal populations (Muller's ratchet), which are expected to occur through the recurrent transmission bottlenecks during the complex infection cycle of these pathogens in their mammalian reservoir hosts and arthropod vectors.

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Ecological and Evolutionary Benefits of Temperate Phage: What Does or Doesn't Kill You Makes You Stronger

Cited by 183 publications

References 76 publications

Evolutionary stability of the lysis‐lysogeny decision: why be virulent?

Evolutionary stability of the lysis‐lysogeny decision: why be virulent?

The population and evolutionary dynamics of bacteriophage: Why be temperate revisited

Bartonellagene transfer agent: Evolution, function, and proposed role in host adaptation

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