Multiple toxins and a protease contribute to the aphid‐killing ability of Pseudomonas fluorescens PpR24

• Published in: Environmental microbiology Vol. 26; no. 4; pp. e16604 - n/a
• Main Authors: Paliwal, Deepa, Rabiey, Mojgan, Mauchline, Tim H., Hassani‐Pak, Keywan, Nauen, Ralf, Wagstaff, Carol, Andrews, Simon, Bass, Chris, Jackson, Robert W.
• Format: Journal Article
• Language: English
• Published: Hoboken, USA John Wiley & Sons, Inc 01.04.2024; Wiley Subscription Services, Inc
• Subjects: Biological control; biological control agents; Biosynthesis; Detoxification; Gene expression; gene expression regulation; Gene regulation; Gene sequencing; Genes; genome; Genomes; Insecticide resistance; Insecticides; Insects; Metabolites; microbiology; mortality; Myzus persicae; Oxidation resistance; Oxidative stress; Pest control; Pesticide resistance; Pests; Protease; proteinases; Pseudomonas fluorescens; secondary metabolites; sequence analysis; stress tolerance; Toxins; Transcriptomics; Virulence; Virulence factors
• ISSN: 1462-2912; 1462-2920; 1462-2920
• DOI: 10.1111/1462-2920.16604

Aphids are globally important pests causing damage to a broad range of crops. Due to insecticide resistance, there is an urgent need to develop alternative control strategies. In our previous work, we found Pseudomonas fluorescens PpR24 can orally infect and kill the insecticide‐resistant green‐peach aphid (Myzus persicae). However, the genetic basis of the insecticidal capability of PpR24 remains unclear. Genome sequencing of PpR24 confirmed the presence of various insecticidal toxins such as Tc (toxin complexes), Rhs (rearrangement hotspot) elements, and other insect‐killing proteases. Upon aphids infection with PpR24, RNA‐Seq analysis revealed 193 aphid genes were differentially expressed with down‐regulation of 16 detoxification genes. In addition, 1325 PpR24 genes (542 were upregulated and 783 downregulated) were subject to differential expression, including genes responsible for secondary metabolite biosynthesis, the iron‐restriction response, oxidative stress resistance, and virulence factors. Single and double deletion of candidate virulence genes encoding a secreted protease (AprX) and four toxin components (two TcA‐like; one TcB‐like; one TcC‐like insecticidal toxins) showed that all five genes contribute significantly to aphid killing, particularly AprX. This comprehensive host–pathogen transcriptomic analysis provides novel insight into the molecular basis of bacteria‐mediated aphid mortality and the potential of PpR24 as an effective biocontrol agent. Wildtype Pseudomonas fluorescens PpR24 (left) kills Myzus persicae aphids using toxins and a protease—an aprX protease mutant is severely impacted in its ability to kill aphids with most remaining alive (a representation is provided on the right).