Abstract

Interference competition among bacteria requires a highly specialized, narrow-spectrum weaponry when targeting closely-related competitors while sparing individuals from the same clonal population. Here we investigated mechanisms by which environmentally important Pseudomonas bacteria with plant-beneficial activity perform kin interference competition. We show that killing between phylogenetically closely-related strains involves contractile phage tail-like devices called R-tailocins that puncture target cell membranes. Using live-cell imaging, we evidence that R-tailocins are produced at the cell center, transported to the cell poles and ejected by explosive cell lysis. This enables their dispersal over several tens of micrometers to reach targeted cells. We visualize R-tailocin-mediated competition dynamics between closely-related Pseudomonas strains at the single-cell level, both in non-induced condition and upon artificial induction. We document the fatal impact of cellular self-sacrifice coupled to deployment of phage tail-like weaponry in the microenvironment of kin bacterial competitors, emphasizing the necessity for microscale assessment of microbial competitions.

Highlights

  • Interference competition among bacteria requires a highly specialized, narrow-spectrum weaponry when targeting closely-related competitors while sparing individuals from the same clonal population

  • Strains belonging to the Pseudomonas protegens (Pp) or Pseudomonas chlororaphis (Pc) subgroups within the Pseudomonas fluorescens species complex[2] typically are highly competitive root colonizers that, are able to establish themselves in contrasting ecological niches, notably in insects[3,4]

  • PHASTER classified as intact prophages another set of gene clusters that are incomplete, as they no longer contain the genes encoding the synthesis of the viral capsid. These regions correspond to gene clusters encoding phage tail-related structures designated as R-tailocins and are present in all Pseudomonas genomes used in this study (Fig. 1)

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Summary

Introduction

Interference competition among bacteria requires a highly specialized, narrow-spectrum weaponry when targeting closely-related competitors while sparing individuals from the same clonal population. As well as competing against distantly-related organisms, pseudomonads are in competition with kin bacteria, i.e., phylogenetically close relatives, which we consider as strains belonging to the same subgroup in this study They produce narrow-spectrum toxins, called bacteriocins that typically target close relatives[10]. Phages may impact species diversity by multiple mechanisms such as reducing the number of highly competitive bacteria (“killing the winner”), releasing nutrients and DNA into the environment and immunizing bacteria against similar viral relatives or equip them with new traits[15,17,18,19] When bacteriophages integrate their genome into bacteria, it may give rise to complex structures such as phage tail-like particles that can be used against other competitors[20,21,22]. F-type and R-type tailocins are thought to be evolutionarily related to phages from the families

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