Contrasted coevolutionary dynamics between a bacterial pathogen and its bacteriophages

Betts, Alexander; Kaltz, Oliver; Hochberg, Michael

doi:10.1073/pnas.1406763111

Cited by 97 publications

(106 citation statements)

References 68 publications

(92 reference statements)

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“…Studies performed in chemostats have addressed the coevolution dynamics of phage and bacteria in controlled growth conditions (Betts et al, 2014;Buckling & Rainey, 2002). Two possible outcomes were described in some assays where prey and predators are left to evolve for a long time.…”

Section: Red Queen Dynamics/arms Race Coevolutionmentioning

confidence: 99%

Pseudolysogeny and sequential mutations build multiresistance to virulent bacteriophages in Pseudomonas aeruginosa

Latino

2016

Microbiology

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Coevolution between bacteriophages (phages) and their prey is the result of mutualistic interactions. Here, we show that pseudolysogeny is a frequent outcome of infection by virulent phages of Pseudomonas aeruginosa and that selection of resistant bacterial mutants is favoured by continuous production of phages. We investigated the frequency and characteristics of P. aeruginosa strain PAO1 variants resisting infection by different combinations of virulent phages belonging to four genera. The frequency of resistant bacteria was 10 25 for single phage infection and 10 26 for infections with combinations of two or four phages. The genome of 27 variants was sequenced and the comparison with the genome of the parental PAO1 strain allowed the identification of point mutations or small indels. Four additional variants were characterized by a candidate gene approach. In total, 27 independent mutations were observed affecting 14 genes and a regulatory region. The mutations affected genes involved in biosynthesis of type IV pilus, alginate, LPS and O-antigen. Half of the variants possessed changes in homopolymer tracts responsible for frameshift mutations and these phase variation mutants were shown to be unstable. Eleven double mutants were detected. The presence of free phage DNA was observed in association with exclusion of superinfection in half of the variants and no chromosomal mutation could be found in three of them. Upon further growth of these pseudolysogens, some variants with new chromosomal mutations were recovered, presumably due to continuous evolutionary pressure.

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Section: Red Queen Dynamics/arms Race Coevolutionmentioning

confidence: 99%

Pseudolysogeny and sequential mutations build multiresistance to virulent bacteriophages in Pseudomonas aeruginosa

Latino

2016

Microbiology

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“…For example, co‐evolutionary dynamics can follow either an arms race or fluctuating selection dynamics depending on the interacting parasite species (Betts, Kaltz, & Hochberg, 2014), while considerable variation exists in host species sensitivity to a one given parasite species (Thompson, 2005). This is especially true with bacteria, where small differences between different genotypes can have large effects on fitness.…”

Section: Introductionmentioning

confidence: 99%

Bacterial cell‐to‐cell signaling promotes the evolution of resistance to parasitic bacteriophages

Moreau

Diggle

Friman

2017

Ecology and Evolution

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The evolution of host–parasite interactions could be affected by intraspecies variation between different host and parasite genotypes. Here we studied how bacterial host cell‐to‐cell signaling affects the interaction with parasites using two bacteria‐specific viruses (bacteriophages) and the host bacterium Pseudomonas aeruginosa that communicates by secreting and responding to quorum sensing (QS) signal molecules. We found that a QS‐signaling proficient strain was able to evolve higher levels of resistance to phages during a short‐term selection experiment. This was unlikely driven by demographic effects (mutation supply and encounter rates), as nonsignaling strains reached higher population densities in the absence of phages in our selective environment. Instead, the evolved nonsignaling strains suffered relatively higher growth reduction in the absence of the phage, which could have constrained the phage resistance evolution. Complementation experiments with synthetic signal molecules showed that the Pseudomonas quinolone signal (PQS) improved the growth of nonsignaling bacteria in the presence of a phage, while the activation of las and rhl quorum sensing systems had no effect. Together, these results suggest that QS‐signaling can promote the evolution of phage resistance and that the loss of QS‐signaling could be costly in the presence of phages. Phage–bacteria interactions could therefore indirectly shape the evolution of intraspecies social interactions and PQS‐mediated virulence in P. aeruginosa.

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“…We found that in ironlimited monocultures, producer bacteria were able to recover from phage predation, suggestive of resistance evolution [48], rspb.royalsocietypublishing.org Proc. R. Soc.…”

Section: Discussionmentioning

confidence: 78%

Phage selection for bacterial cheats leads to population decline

2015

Self Cite

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While predators and parasites are known for their effects on bacterial population biology, their impact on the dynamics of bacterial social evolution remains largely unclear. Siderophores are iron-chelating molecules that are key to the survival of certain bacterial species in iron-limited environments, but their production can be subject to cheating by non-producing genotypes. In a selection experiment conducted over approximately 20 bacterial generations and involving 140 populations of the pathogenic bacterium Pseudomonas aeruginosa PAO1, we assessed the impact of a lytic phage on competition between siderophore producers and non-producers. We show that the presence of lytic phages favours the non-producing genotype in competition, regardless of whether iron use relies on siderophores. Interestingly, phage pressure resulted in higher siderophore production, which constitutes a cost to the producers and may explain why they were outcompeted by nonproducers. By the end of the experiment, however, cheating load reduced the fitness of mixed populations relative to producer monocultures, and only monocultures of producers managed to grow in the presence of phage in situations where siderophores were necessary to access iron. These results suggest that public goods production may be modulated in the presence of natural enemies with consequences for the evolution of social strategies.

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Contrasted coevolutionary dynamics between a bacterial pathogen and its bacteriophages

Cited by 97 publications

References 68 publications

Pseudolysogeny and sequential mutations build multiresistance to virulent bacteriophages in Pseudomonas aeruginosa

Pseudolysogeny and sequential mutations build multiresistance to virulent bacteriophages in Pseudomonas aeruginosa

Bacterial cell‐to‐cell signaling promotes the evolution of resistance to parasitic bacteriophages

Phage selection for bacterial cheats leads to population decline

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