Transcriptome plasticity underlying plant root colonization and insect invasion by Pseudomonas protegens

Abstract

Pseudomonas protegens shows a high degree of lifestyle plasticity since it can establish both plant-beneficial and insect-pathogenic interactions. While P. protegens protects plants against soilborne pathogens, it can also invade insects when orally ingested leading to the death of susceptible pest insects. The mechanism whereby pseudomonads effectively switch between lifestyles, plant-beneficial or insecticidal, and the specific factors enabling plant or insect colonization are poorly understood. We generated a large-scale transcriptomics dataset of the model P. protegens strain CHA0 which includes data from the colonization of wheat roots, the gut of Plutella xylostella after oral uptake and the Galleria mellonella hemolymph after injection. We identified extensive plasticity in transcriptomic profiles depending on the environment and specific factors associated to different hosts or different stages of insect infection. Specifically, motor-activity and Reb toxin-related genes were highly expressed on wheat roots but showed low expression within insects, while certain antimicrobial compounds (pyoluteorin), exoenzymes (a chitinase and a polyphosphate kinase), and a transposase exhibited insect-specific expression. We further identified two-partner secretion systems as novel factors contributing to pest insect invasion. Finally, we use genus-wide comparative genomics to retrace the evolutionary origins of cross-kingdom colonization.

Oral Toxicity of Pseudomonas protegens against Muscoid Flies

“…According to our observations and to the discovery of several metabolites P. protegens may produce, the pathogenic interaction this bacterium can establish with different targets appear to be complex and multifactorial [16]. Evidence in our study of the biocidal potential against pests of veterinary importance, provides additional biological information to the previously reported bioinsecticidal action this bacterial species shows against crop pests and its plasticity establishing plant-beneficial interactions [19]. Despite different degrees of virulence are expected to be associated with diverse P. protegens strains, the maintenance within the species of an arsenal of toxins and virulence factors, suggests an evolutionary process in which a conserved pathogenic relationship with insects became established.…”

Phylogenetically closely related pseudomonads isolated from arthropods exhibit differential insect‐killing abilities and genetic variations in insecticidal factors

“…Although pseudomonads were detected in field and laboratory-reared Lepidoptera (Çakici et al, 2014;Chen et al, 2016;Mashtoly et al, 2019;Skowronek et al, 2020) and Coleoptera (Bahar and Demirba g, 2007;Montagna et al, 2015a;Montagna et al, 2015b), and in laboratory-reared Diptera (Wong et al, 2015), it is still uncertain whether they have established a relationship with these insects or if they are just transient bacteria in their gut. Some plant-beneficial pseudomonads belonging to the Pseudomonas protegens, Pseudomonas chlororaphis and P. fluorescens species can also be pathogens of diverse pest insect species (Péchy-Tarr et al, 2008;Jang et al, 2013;Kupferschmied et al, 2013Kupferschmied et al, , 2014Péchy-Tarr et al, 2013;Ruffner et al, 2013Ruffner et al, , 2015Flury et al, 2016Flury et al, , 2019Loper et al, 2016;Vacheron et al, 2019;Vesga et al, 2020). Pseudomonas protegens and P. chlororaphis are known root colonizers and they can control soil-borne fungal pathogens (Haas and Défago, 2005).…”

“…This toxin is very similar to the Mcf (make caterpillars floppy) toxins of Photorhabdus luminescens and Xenorhabdus nematophila (Daborn et al, 2002;Waterfield et al, 2003;Ruffner et al, 2015). Subsequent work established that insecticidal activity in P. protegens and P. chlororaphis is a multifactorial trait that involves, besides the Fit toxin, various elements such as lipopolysaccharide O-antigens (Kupferschmied et al, 2014), the type VI secretion system (Vacheron et al, 2019), the cyclic lipopeptide orfamide A (Jang et al, 2013;Flury et al, 2016), a chitinase and a phospholipase C (Flury et al, 2016), hydrogen cyanide (Flury et al, 2017), the toxins rhizoxin (Loper et al, 2016) or IPD072Aa (Schellenberger et al, 2016), and two-partner secretion (TPS) systems (Vesga et al, 2020).…”

ExlA Pore-Forming Toxin: Localization at the Bacterial Membrane, Regulation of Secretion by Cyclic-Di-GMP, and Detection In Vivo

“…ExlA is a 172-kDa protein harboring (i) at the N-terminal end, a signal peptide (SP) followed by a TPS domain allowing interaction with its transporter ExlB, (ii) in the central part, a shaft consisting of a type-2 filamentous haemagglutinin adhesin (FHA2) domain, and (iii) a C-terminal domain that behaves like a molten globule in solution and has no characterized homolog [ 8 , 9 ] ( Figure S1 ). Interestingly, ExlA-like toxins have been identified in other Pseudomonas species ( P. putida , P. entomophila and P. protegens ) [ 10 , 11 ]. The ExlA-ExlB TPS is structurally related to TPSs present in other bacterial pathogens and exhibiting cytolytic activities, including ShlA-ShlB in Serratia marcescens , HpmA-HpmB in Proteus mirabilis , EthA-EthB in Edwardsiella tarda and HhdA-HhdB in Haemophilus ducreyi [ 12 ].…”