Abstract
Some of the bacterial cells in isogenic populations behave differently from others. We describe here how a new type of phenotypic heterogeneity relating to resistance to cationic antimicrobial peptides (CAMPs) is determinant for the pathogenic infection process of the entomopathogenic bacterium Photorhabdus luminescens. We demonstrate that the resistant subpopulation, which accounts for only 0.5% of the wild-type population, causes septicemia in insects. Bacterial heterogeneity is driven by the PhoPQ two-component regulatory system and expression of pbgPE, an operon encoding proteins involved in lipopolysaccharide (LPS) modifications. We also report the characterization of a core regulon controlled by the DNA-binding PhoP protein, which governs virulence in P. luminescens. Comparative RNAseq analysis revealed an upregulation of marker genes for resistance, virulence and bacterial antagonism in the pre-existing resistant subpopulation, suggesting a greater ability to infect insect prey and to survive in cadavers. Finally, we suggest that the infection process of P. luminescens is based on a bet-hedging strategy to cope with the diverse environmental conditions experienced during the lifecycle.
Highlights
Phenotypic switching is a frequent occurrence in the genus Photorhabdus[16]
As previously reported[25], TT01 was resistant to high doses of cationic antimicrobial peptides (CAMPs), whereas the phoP and pbgE mutant strains were susceptible to very low doses of antimicrobial compounds, such as polymyxin B (Table 1)
We assayed the resistance of TT01 to the synthetic Spodoptera frugiperda cecropin B (Sf-CecB1), to mimic the antimicrobial activities naturally found in the plasma of insect larvae challenged with bacteria[30]
Summary
Phenotypic variants generally emerge after prolonged in vitro culture of the wild-type strain collected from the nematode[17]. The emergence of secondary variants has been shown to be unrelated to genomic rearrangements[19] Another source of phenotypic heterogeneity in P. luminescens is switching between the ON and OFF states of expression of the fimbrial maternal adhesion locus (mad genes), through an inversion of the promoter region. In the ON state, mad genes are transcribed and the bacteria are covered with fimbriae[20] This form of Photorhabdus is called the M form (for “mutualistic”) and it is observed only during symbiosis with the nematode. The resistant bacteria account for only 0.5% of the wild-type population in P. luminescens TT01 during in vitro culture This bacterial heterogeneity depends on PhoP and pbgPE
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