Insecticidal Serralysin of Serratia marcescens Is Detoxified in M3 Midgut Region of Riptortus pedestris

Abstract

Riptortus pedestris insect indiscriminately acquires not only the symbiotic bacterium Burkholderia insecticola, but also entomopathogens that are abundant in the soil via feeding. However, it is unclear how the host insect survives oral infections of entomopathogens. A previous study suggested that serralysin, a potent virulence factor produced by Serratia marcescens, suppresses cellular immunity by degrading adhesion molecules, thereby contributing to bacterial pathogenesis. Here, we observed that S. marcescens orally administered to R. pedestris stably colonized the insect midgut, while not exhibiting insecticidal activity. Additionally, oral infection with S. marcescens did not affect the host growth or fitness. When co-incubated with the midgut lysates of R. pedestris, serralysin was remarkably degraded. The detoxification activity against serralysin was enhanced in the midgut extract of gut symbiont-colonizing insects. The mRNA expression levels of serralysin genes were negligible in M3-colonizing S. marcescens. M3-colonizing S. marcescens did not produce serralysin toxin. Immunoblot analyses revealed that serralysin was not detected in the M3 midgut region. The findings of our study suggest that orally infected S. marcescens lose entomopathogenicity through host-derived degrading factors and suppression of serralysin.

Identification and expression patterns of somatic piRNAs and PIWI genes in Riptortus pedestris (Hemiptera: Alydidae)

“…Antibiotic treatment that disturbs the gut bacterial communities was applied to explore their benefit in the maintenance of host homeostasis at the transcriptional and posttranscriptional levels in insects, such as Bactrocera dorsalis , Altica viridicyanea , A. mellifera , and Plagiodera versicolora (Ma et al, 2021; Ren, Chen, Wang, et al, 2023; Xie et al, 2023; Zhang, Mu, et al, 2022). In previous reports, it is plausible that the available research model of gut bacteria− R. pedestris has been constructed and validated for their roles in host physiology and immunity (Lee & Lee, 2022; Lee, Kim, et al, 2019; Lee et al, 2022). On the basis of these results, we applied the samples of gut bacterial disturbance by antibiotic feeding and two laboratory‐reared to compare the relationships between piRNA expression and gut bacterial shifts, combined the wild samples using WTS technology.…”

Assessment of the Entomopathogenic Potential of Fungal and Bacterial Isolates from Fall Armyworm Cadavers Against Spodoptera frugiperda Caterpillars and the Adult Boll Weevil, Anthonomus grandis

“…This factor suppresses cellular immunity by degrading adhesion molecules and increasing bacterial pathogenesis (Lee et al 2017 ; Tambong et al 2014 ). However, Lee and Lee ( 2022 ) demonstrated that some insects can show high detoxification activity against serralysin in the midgut, while the activity of the lytic enzymes protease and phospholipase and of oxidative stress enzymes increases in the gut and also in the hemolymph. This was demonstrated for S. litura caterpillars fed a diet supplemented with S. marcescens (Aggarwal et al 2021 ).…”

The gut bacterium Serratia marcescens mediates detoxification of organophosphate pesticide in Riptortus pedestris by microbial degradation

“…Microscopic observation presented that the S. marcescens was mostly colonized in the M2 and M3 regions of the insect midgut (Figure 4f,g). The successful colonization of S. marcescens is related to a potent virulent metalloprotease produced by the bacteria to escape from the host's immune response, and this symbiotic association does not affect host growth or fitness (Lee et al, 2017; Lee & Lee, 2022). In the present study, we discovered that S. marcescens inoculation also had no significant influence on the survival rate of R. pedestris (Figure 5a).…”

“…Some S. marcescens strains are opportunistic pathogens of plants and animals (Konecka et al, 2019). The bacteria are also important entomopathogens that show pathogenicity to silkworms, mosquitoes, honey bees, stinkbugs and other insects (Ishii et al, 2014; Lee & Lee, 2022; Raymann et al, 2018; Wei et al, 2017). Additionally, some S. marcescens strains have excellent biodegradation capabilities of organophosphorus pesticides (Wang et al, 2018; Wu et al, 2021).…”