Contrasted coevolutionary dynamics between a bacterial pathogen and its bacteriophages

Abstract

Many antagonistic interactions between hosts and their parasites result in coevolution. Although coevolution can drive diversity and specificity within species, it is not known whether coevolutionary dynamics differ among functionally similar species. We present evidence of coevolution within simple communities of Pseudomonas aeruginosa PAO1 and a panel of bacteriophages. Pathogen identity affected coevolutionary dynamics. For five of six phages tested, time-shift assays revealed temporal peaks in bacterial resistance and phage infectivity, consistent with frequency-dependent selection (Red Queen dynamics). Two of the six phages also imposed additional directional selection, resulting in strongly increased resistance ranges over the entire length of the experiment (ca. 60 generations). Cross-resistance to these two phages was very high, independent of the coevolutionary history of the bacteria. We suggest that coevolutionary dynamics are associated with the nature of the receptor used by the phage for infection. Our results shed light on the coevolutionary process in simple communities and have practical application in the control of bacterial pathogens through the evolutionary training of phages, increasing their virulence and efficacy as therapeutics or disinfectants.

Keywords: arms race; fluctuating selection; nosocomial pathogen; phage therapy; type IV pili.

Fig. 1.

Time-shift curves of resistance of P. aeruginosa PAO1 coevolving with six phage types. Each panel shows the curve for each of six replicate populations (dotted lines) and the overall mean ± SE (bold line). Time-shift lag 0 refers to contemporary combinations of bacteria and phages from transfer 5 (vertical dashed line); lag +1 and lag +5 are combinations in which phages are one or five transfers in the future relative to the bacteria; lag −1 and lag −5 are combinations in which bacteria are one or five transfers in the future relative to phages. Intraclass correlation coefficients (r_i) describe the degree of similarity of trajectories among replicate populations (1 = highly correlated; 0 = uncorrelated). Phage types represent Myoviridae or Podoviridae families.

Fig. 2.

Mean resistance of P. aeruginosa PAO1 and mean infectivity of six phage types at three time points during the experiment. Means (± SE) were calculated from a cross-infection matrix using all combinations between bacteria and phages from transfers 0, 5, and 10. Phage types represent Myoviridae or Podoviridae families.

Fig. 3.

Mean (± SE) resistance of evolved P. aeruginosa PAO1 to six ancestral phage types. “Origin of tested bacteria” indicates the phage with which the bacteria had coevolved for 10 transfers. The letter “s” (= sympatric) indicates combinations of coevolved bacteria and phage. “Ancestor” indicates the resistance of the ancestral bacterial strain (P. aeruginosa PAO1). Phage types represent Myoviridae or Podoviridae families.