Abstract

SummaryVirulence traits are essential for pathogen fitness, but whether they affect microbial performance in the environment, where they are not needed, remains experimentally unconfirmed. We investigated this question with the facultative pathogen L isteria monocytogenes and its PrfA virulence regulon. PrfA‐regulated genes are activated intracellularly (PrfA ‘ON’) but shut down outside the host (PrfA ‘OFF’). Using a mutant PrfA regulator locked ON (PrfA*) and thus causing PrfA‐controlled genes to be constitutively activated, we show that virulence gene expression significantly impairs the listerial growth rate (μ) and maximum growth (A) in rich medium. Deletion analysis of the PrfA regulon and complementation of a L. monocytogenes mutant lacking all PrfA‐regulated genes with PrfA* indicated that the growth reduction was specifically due to the unneeded virulence determinants and not to pleiotropic regulatory effects of PrfA ON. No PrfA*‐associated fitness disadvantage was observed in infected eukaryotic cells, where PrfA‐regulated virulence gene expression is critical for survival. Microcosm experiments demonstrated that the constitutively virulent state strongly impaired L . monocytogenes performance in soil, the natural habitat of these bacteria. Our findings provide empirical proof that virulence carries a significant cost to the pathogen. They also experimentally substantiate the assumed, although not proven, key role of virulence gene regulation systems in suppressing the cost of bacterial virulence outside the host.

Highlights

  • The ability of a microbe to infect and cause harm correlates with its multiplication rate within the host, itself a direct determinant of between-host transmission success (Read, 1994; Lipsitch and Moxon, 1997)

  • Taking advantage of the properties conferred by the prfA* allele, we show that virulence gene activation imposes a significant burden on L. monocytogenes outside the host

  • The prfA*-associated growth reduction was noted by others, the effect was relatively minor compared with wild-type prfA and was not statistically confirmed (Marr et al, 2006)

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Summary

Introduction

The ability of a microbe to infect and cause harm (virulence) correlates with its multiplication rate within the host, itself a direct determinant of between-host transmission success (Read, 1994; Lipsitch and Moxon, 1997). A number of studies with phytopathogens have examined the fitness costs of ‘avirulence’ gene mutations to virulence in susceptible plant populations without the matching resistance (R) gene (where the pathogen’s avirulence/virulence gene is irrelevant) (Leach et al, 2001; Bahri et al, 2009; Huang et al, 2010; Montarry et al, 2010). These studies have generally measured the cost of virulence via the effects on within-host fitness attributes (e.g. in planta multiplication, amount of disease symptoms or pathogen released from leaves) but not on saprophytic growth and survival (Sacristan and Garcia-Arenal, 2008). Gene deletion analysis suggested that the growth defect was at least in part attributable to TTSS-1 virulence factor expression, the possibility that it was due to global, pleiotropic regulatory effects was not excluded (Sturm et al, 2011)

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