Evolution of parasitism and mutualism between filamentous phage M13 andEscherichia coli

Abstract

Background. How host-symbiont interactions coevolve between mutualism and parasitism depends on the ecology of the system and on the genetic and physiological constraints of the organisms involved. Theory often predicts that greater reliance on horizontal transmission favors increased costs of infection and may result in more virulent parasites or less beneficial mutualists. We set out to understand transitions between parasitism and mutualism by evolving the filamentous bacteriophage M13 and its host Escherichia coli.Results. The effect of phage M13 on bacterial fitness depends on the growth environment, and initial assays revealed that infected bacteria reproduce faster and to higher density than uninfected bacteria in 96-well microplates. These data suggested that M13 is, in fact, a facultative mutualist of E. coli. We then allowed E. coli and M13 to evolve in replicated environments, which varied in the relative opportunity for horizontal and vertical transmission of phage in order to assess the evolutionary stability of this mutualism. After 20 experimental passages, infected bacteria from treatments with both vertical and horizontal transmission of phage had evolved the fastest growth rates. At the same time, phage from these treatments no longer benefited the ancestral bacteria.Conclusions. These data suggest a positive correlation between the positive effects of M13 on E. coli hosts from the same culture and the negative effects of the same phage toward the ancestral bacterial genotype. The results also expose flaws in applying concepts from the virulence-transmission tradeoff hypothesis to mutualism evolution. We discuss the data in the context of more recent theory on how horizontal transmission affects mutualisms and explore how these effects influence phages encoding virulence factors in pathogenic bacteria.

Evolution of mutualism from parasitism in experimental virus populations

“…We evolved this virus in a previous experiment (Shapiro et al. ), and six virus populations were chosen at random from the “Low Host Addition” treatment, in which opportunities for horizontal transmission were rare. Here, we will refer to these populations as A, B, C, D, E, and F. We fully sequenced each of these populations using the Illumina HiSeq platform with 150 bp paired‐end reads (raw reads available through NCBI; see Table S1 for SRA IDs).…”

“…The growth medium (Davis minimal medium supplemented with thiamine hydrochloride at 2 × 10 −3 μg/mL and 1000 μg/mL glucose; DM1000) and general culturing methods were as described previously (Carlton and Brown ; Shapiro et al. ). Each of the six virus populations chosen from the first experiment was used to initiate infections in 15 replicate wells of a 96‐well plate, for a total of 90 experimental populations.…”

“…In a previous study, we found that “wild‐type” M13 increases the growth rate and yield of Escherichia coli in 96‐well microplates despite decreasing bacterial growth in well‐mixed Erlenmeyer flasks (Shapiro et al. ). This conditional mutualism provided a unique opportunity to evolve M13 and E. coli under experimental conditions expected to favor either more helpful or more harmful viruses (Shapiro et al.…”

“…, ; Shapiro et al. ). Relatively few studies, though, have explored the evolution of mutualism breakdown experimentally, and we are aware of no prior work that has explored a transition back to mutualism after the evolution of parasitism.…”

“…This conditional mutualism provided a unique opportunity to evolve M13 and E. coli under experimental conditions expected to favor either more helpful or more harmful viruses (Shapiro et al. ). By growing infected bacteria in 96‐well microplates, it was possible to select for more or less beneficial phage by varying the relative availability of horizontal transmission of the virus.…”