Putative host-derived growth factors inducing colonization of Burkholderia gut symbiont in Riptortus pedestris insect

Lee, Junbeom; Mao, Xinrui; Lee, You Seon; Lee, Dong Jung; Kim, Jung-Hyun; Kim, Jiyeun Kate; Lee, Bok Luel

doi:10.1016/j.dci.2019.103570

Cited by 4 publications

(5 citation statements)

References 18 publications

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“…Additionally, as a large number of naïve Burkholderia gut symbionts can be collected from M4 crypts, it is feasible to study biochemical differences between in vitro -cultured Burkholderia cells and in vivo -colonized symbiotic cells ( Kim et al, 2013c , 2015b ; Byeon et al, 2015 ). Accordingly, we recently reported unexpected observations and extended our understanding of how this symbiont interacts with host insects at the molecular and biochemical levels ( Lee et al, 2019 , 2020 ).…”

Section: Introductionmentioning

confidence: 87%

“…The bean bugs, R. pedestris , were reared in our insect laboratory at 28°C under a photoperiod of 16 h light and 8 h dark, as previously described ( Lee et al, 2020 ). Nymphal insects were reared in clean plastic containers containing soybean seeds and distilled water containing 0.05% ascorbic acid (DWA).…”

Section: Methodsmentioning

confidence: 99%

“…Bacterial cells were washed with 10 mM PB and suspended in Grace’s Insect Medium (Gibco, United States) to 1.0 × 10 7 cells/ml bacterial solutions ( Kim et al, 2013a ; Lee et al, 2020 ). Briefly, two microliters of thanatins dsRNA were systemically injected into 3-day-old R. pedestris male adults for immune suppression.…”

Section: Methodsmentioning

confidence: 99%

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Multiple Precursor Proteins of Thanatin Isoforms, an Antimicrobial Peptide Associated With the Gut Symbiont of Riptortus pedestris

2022

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Thanatin is an antimicrobial peptide (AMP) generated by insects for defense against bacterial infections. In the present study, we performed cDNA cloning of thanatin and found the presence of multiple precursor proteins from the bean bug, Riptortus pedestris. The cDNA sequences encoded 38 precursor proteins, generating 13 thanatin isoforms. In the phylogenetic analysis, thanatin isoforms were categorized into two groups based on the presence of the membrane attack complex/perforin (MACPF) domain. In insect-bacterial symbiosis, specific substances are produced by the immune system of the host insect and are known to modulate the symbiont’s population. Therefore, to determine the biological function of thanatin isoforms in symbiosis, the expression levels of three AMP genes were compared between aposymbiotic insects and symbiotic R. pedestris. The expression levels of the thanatin genes were significantly increased in the M4 crypt, a symbiotic organ, of symbiotic insects upon systemic bacterial injection. Further, synthetic thanatin isoforms exhibited antibacterial activity against gut-colonized Burkholderia symbionts rather than in vitro-cultured Burkholderia cells. Interestingly, the suppression of thanatin genes significantly increased the population of Burkholderia gut symbionts in the M4 crypt under systemic Escherichia coli K12 injection. Overgrown Burkholderia gut symbionts were observed in the hemolymph of host insects and exhibited insecticidal activity. Taken together, these results suggest that thanatin of R. pedestris is a host-derived symbiotic factor and an AMP that controls the population of gut-colonized Burkholderia symbionts.

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Section: Introductionmentioning

confidence: 87%

Section: Methodsmentioning

confidence: 99%

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Multiple Precursor Proteins of Thanatin Isoforms, an Antimicrobial Peptide Associated With the Gut Symbiont of Riptortus pedestris

2022

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“…Riptortus pedestris was maintained in an insectary at 28°C under a long-day cycle of 16 h light and 8 h dark, as described previously ( Lee et al, 2020 ). The nymphs were reared in clean plastic containers with soybean seeds and distilled water containing 0.05% ascorbic acid.…”

Section: Methodsmentioning

confidence: 99%

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

Lee

2022

Front. Microbiol.

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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.

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“…Upon reaching adulthood, the insects were transferred to larger containers provided with soybean plant pots and cotton pads for egg laying. B. insecticola was cultured to mid‐log phase at 30°C in YG‐rifampicin medium (0.5% yeast extract, 0.4% glucose, and 0.1% NaCl supplemented with 30 μg/ml rifampicin) (Lee et al, 2020). A cotton dish soaked in in vitro‐cultured Burkholderia (10 7 cells/ml DWA) was exposed to the second‐instar nymphs for 2 days to generate Burkholderia ‐harboring Sym‐insects (Lee et al, 2017b).…”

Section: Methodsmentioning

confidence: 99%

Burkholderia gut symbiont induces insect host fecundity by modulating Kr‐h1 gene expression

Lee

2022

Arch Insect Biochem Physiol

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Full-length cDNAs of the Broad-Complex (BR-C) from Riptortus pedestris were cloned. Moreover, Kr-h1 and BR-C expression levels in apo-symbiotic and symbiotic host insects were compared to verify whether they are modulated by Burkholderia gut symbionts. Interestingly, Kr-h1 expression level was significantly increased in symbiotic females. To determine how Kr-h1 affects fecundity in insects, the biosynthesis of two reproduction-associated proteins, hexamerin-α and vitellogenin, was investigated in R. pedestris females. Hexamerin-α and vitellogenin expression at the transcriptional and translational levels decreased in Kr-h1suppressed symbiotic females, subsequently reduced egg production. These results suggest that Burkholderia gut symbiont modulates Kr-h1 expression to enhance ovarian development and egg production of R. pedestris by increasing the biosynthesis of the two proteins.

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Putative host-derived growth factors inducing colonization of Burkholderia gut symbiont in Riptortus pedestris insect

Cited by 4 publications

References 18 publications

Multiple Precursor Proteins of Thanatin Isoforms, an Antimicrobial Peptide Associated With the Gut Symbiont of Riptortus pedestris

Multiple Precursor Proteins of Thanatin Isoforms, an Antimicrobial Peptide Associated With the Gut Symbiont of Riptortus pedestris

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

Burkholderia gut symbiont induces insect host fecundity by modulating Kr‐h1 gene expression

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