Life history trade-offs and relaxed selection can decrease bacterial virulence in environmental reservoirs

Abstract

Pathogen virulence is usually thought to evolve in reciprocal selection with the host. While this might be true for obligate pathogens, the life histories of opportunistic pathogens typically alternate between within-host and outside-host environments during the infection-transmission cycle. As a result, opportunistic pathogens are likely to experience conflicting selection pressures across different environments, and this could affect their virulence through life-history trait correlations. We studied these correlations experimentally by exposing an opportunistic bacterial pathogen Serratia marcescens to its natural protist predator Tetrahymena thermophila for 13 weeks, after which we measured changes in bacterial traits related to both anti-predator defence and virulence. We found that anti-predator adaptation (producing predator-resistant biofilm) caused a correlative attenuation in virulence. Even though the direct mechanism was not found, reduction in virulence was most clearly connected to a predator-driven loss of a red bacterial pigment, prodigiosin. Moreover, life-history trait evolution was more divergent among replicate populations in the absence of predation, leading also to lowered virulence in some of the 'predator absent' selection lines. Together these findings suggest that the virulence of non-obligatory, opportunistic bacterial pathogens can decrease in environmental reservoirs through life history trade-offs, or random accumulation of mutations that impair virulence traits under relaxed selection.

Figure 1. Effect of predation on bacterial defence and biofilm formation.

(A) The bacterial clones' defence, i.e. ability to sustain biomass, and (B) ability to form biofilm in the presence of predators within the ‘predator present’ and ‘predator absent’ treatments. White bars denote white, and grey bars denote red bacterial clones. Error bars denote 2 s.e.m.

Figure 2. Survival of G. mellonella larvae when infected with different bacterial clones.

Larvae infected with (A) clones from the ‘predator present’ and ‘predator absent’ treatments, the ancestral clone, and the water control, with (B) white and red clones from the ‘predator present’ and ‘predator absent’ treatments, and with (C & D) the clones from different replicate populations of the ‘predator present’ and ‘predator absent’ treatments.

Figure 3. Bacterial life-history trait correlations within predation treatments.

Population-level (replicate selection lines numbered 5–8) correlations between (A) predation-resistant biofilm and maximum growth rate, and (B) virulence and predation-resistant biofilm. Correlations between (C) predation-resistant biofilm and maximum growth rate by colony colour, and (D) virulence and predation-resistant biofilm by colony colour.