Research Article: Domain Shuffling in a Sensor Protein Contributed to the Evolution of Insect Pathogenicity in Plant-Beneficial Pseudomonas protegens

Date Published: February 20, 2014

Publisher: Public Library of Science

Author(s): Peter Kupferschmied, Maria Péchy-Tarr, Nicola Imperiali, Monika Maurhofer, Christoph Keel, Jeffery L. Dangl.

http://doi.org/10.1371/journal.ppat.1003964

Abstract

Pseudomonas protegens is a biocontrol rhizobacterium with a plant-beneficial and an insect pathogenic lifestyle, but it is not understood how the organism switches between the two states. Here, we focus on understanding the function and possible evolution of a molecular sensor that enables P. protegens to detect the insect environment and produce a potent insecticidal toxin specifically during insect infection but not on roots. By using quantitative single cell microscopy and mutant analysis, we provide evidence that the sensor histidine kinase FitF is a key regulator of insecticidal toxin production. Our experimental data and bioinformatic analyses indicate that FitF shares a sensing domain with DctB, a histidine kinase regulating carbon uptake in Proteobacteria. This suggested that FitF has acquired its specificity through domain shuffling from a common ancestor. We constructed a chimeric DctB-FitF protein and showed that it is indeed functional in regulating toxin expression in P. protegens. The shuffling event and subsequent adaptive modifications of the recruited sensor domain were critical for the microorganism to express its potent insect toxin in the observed host-specific manner. Inhibition of the FitF sensor during root colonization could explain the mechanism by which P. protegens differentiates between the plant and insect host. Our study establishes FitF of P. protegens as a prime model for molecular evolution of sensor proteins and bacterial pathogenicity.

Partial Text

Pseudomonas protegens is a beneficial root-associated bacterium of the Pseudomonas fluorescens group that is able to promote the growth of crop plants and to efficiently protect their roots against fungal and oomycete phytopathogens [1], [2]. P. protegens can also turn into an insect pathogen [3]–[5]. The bacterium produces a potent insecticidal toxin termed Fit (for P. fluorescensinsecticidal toxin) which is required for its capacity to efficiently kill larvae of important agricultural pest insects upon oral or systemic infection [5], [6]. The gene encoding the Fit protein toxin is part of an eight-gene cluster which comprises also genes coding for a type I secretion system and three regulatory proteins (Figure S1 and [6], [7]). Expression of the insecticidal toxin is activated during infection of the insect host, but not on plant roots or in standard laboratory media [7]. We recently demonstrated that toxin expression is tightly controlled by two regulators, named FitG (an activator) and FitH (a repressor) [7]. The third regulatory protein encoded in the Fit cluster is named FitF and codes for a putative sensor histidine kinase-response regulator hybrid protein. We hypothesize that FitF is responsible for the detection of the host environment and for activating insecticidal toxin production via FitH and FitG specifically upon infection of the insect host (Figure S1).

 

Source:

http://doi.org/10.1371/journal.ppat.1003964

 

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