Persistence of root-colonizing Pseudomonas protegens in herbivorous insects throughout different developmental stages and dispersal to new host plants

Abstract

The discovery of insecticidal activity in root-colonizing pseudomonads, best-known for their plant-beneficial effects, raised fundamental questions about the ecological relevance of insects as alternative hosts for these bacteria. Since soil bacteria are limited in their inherent abilities of dispersal, insects as vectors might be welcome vehicles to overcome large distances. Here, we report on the transmission of the root-colonizing, plant-beneficial and insecticidal bacterium Pseudomonas protegens CHA0 from root to root by the cabbage root fly, Delia radicum. Following ingestion by root-feeding D. radicum larvae, CHA0 persisted inside the insect until the pupal and adult stages. The emerging flies were then able to transmit CHA0 to a new plant host initiating bacterial colonization of the roots. CHA0 did not reduce root damages caused by D. radicum and had only small effects on Delia development suggesting a rather commensal than pathogenic relationship. Interestingly, when the bacterium was fed to two highly susceptible lepidopteran species, most of the insects died, but CHA0 could persist throughout different life stages in surviving individuals. In summary, this study investigated for the first time the interaction of P. protegens CHA0 and related strains with an insect present in their rhizosphere habitat. Our results suggest that plant-colonizing pseudomonads have different strategies for interaction with insects. They either cause lethal infections and use insects as food source or they live inside insect hosts without causing obvious damages and might use insects as vectors for dispersal, which implies a greater ecological versatility of these bacteria than previously thought.

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

“…P. protegens and P. chlororaphis colonize the insect gut after oral intake and transmigrate into the hemolymph, causing systemic infections and the eventual death of several Lepidoptera, Diptera, Coleoptera, and Hemiptera insect species [15][16][17][18][19][20][21][22][23]. The P. fluorescens subgroup [2] harbors insecticidal strains with lower pathogenicity than the P. protegens/P.…”

“…Studies on P. protegens CHA0 and other P. protegens / P. chlororaphis strains related insecticidal activity and host persistence to additional factors, including type VI secretion components [ 28 ], chitinase and phospholipase C [ 16 ], hydrogen cyanide [ 29 ], the cyclic lipopeptide orfamide [ 29 , 30 ], the toxins rhizoxin [ 31 ] and IPD072Aa [ 32 ], and specific lipopolysaccharide O-antigens [ 33 ]. P. protegens / P. chlororaphis strains can also cause nonlethal infections [ 18 , 22 , 23 , 31 ]. Even if the infection does not kill the insect after oral uptake, strains such as CHA0 can persist until pupal and imago stages, thus affecting the insect development as shown for Delia radicum , Plutella xylostella and Pieris brassicae , and be transmitted to new host plants by D. radicum [ 23 ].…”

“…P. protegens / P. chlororaphis strains can also cause nonlethal infections [ 18 , 22 , 23 , 31 ]. Even if the infection does not kill the insect after oral uptake, strains such as CHA0 can persist until pupal and imago stages, thus affecting the insect development as shown for Delia radicum , Plutella xylostella and Pieris brassicae , and be transmitted to new host plants by D. radicum [ 23 ]. Therefore, the ability of P. protegens to colonize cross-kingdom insect and plant hosts is impressively demonstrated by work on the model strain CHA0.…”

Interactive potential of Pseudomonas species with plants

“…P. fluorescens SF4c produces more than one functional bacteriocin (such as S-type bacteriocin and phage-tail-like bacteriocin-Tailocins) by their regulator PrtR gene [75]. Flury et al (2019) showed the role of insects such as cabbage root fly, Delia radicum in different developmental stages by harboring persistant root-colonizing P. protegens CHA0 as dispersal agents to new host plants [76].…”

Insights into Chemical Interaction between Plants and Microbes and its Potential Use in Soil Remediation

“…Pseudomonas is a bacterial specie which can compete for limited carbon source and is capable of catabolizing a wide range of plant root exudates. This ability has made pseudomonas one of the most successful root colonizers [24,25].…”