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        The lipopolysaccharide core oligosaccharide of <i>Burkholderia</i> plays a critical role in maintaining a proper gut symbiosis with the bean bug <i>Riptortus pedestris</i>

        Kim, Jiyeun Kate,Jang, Ho Am,Kim, Min Seon,Cho, Jae Hyun,Lee, Junbeom,Di Lorenzo, Flaviana,Sturiale, Luisa,Silipo, Alba,Molinaro, Antonio,Lee, Bok Luel American Society for Biochemistry and Molecular Bi 2017 The Journal of biological chemistry Vol.292 No.47

        <P>Lipopolysaccharide, the outer cell-wall component of Gram-negative bacteria, has been shown to be important for symbiotic associations. We recently reported that the lipopolysaccharide O-antigen of <I>Burkholderia</I> enhances the initial colonization of the midgut of the bean bug, <I>Riptortus pedestris</I>. However, the midgut-colonizing <I>Burkholderia</I> symbionts lack the O-antigen but display the core oligosaccharide on the cell surface. In this study, we investigated the role of the core oligosaccharide, which directly interacts with the host midgut, in the <I>Riptortus–Burkholderia</I> symbiosis. To this end, we generated the core oligosaccharide mutant strains, Δ<I>wabS</I>, Δ<I>wabO</I>, Δ<I>waaF,</I> and Δ<I>waaC,</I> and determined the chemical structures of their oligosaccharides, which exhibited different compositions. The symbiotic properties of these mutant strains were compared with those of the wild-type and O-antigen–deficient Δ<I>wbiG</I> strains. Upon introduction into <I>Riptortus</I> via the oral route, the core oligosaccharide mutant strains exhibited different rates of colonization of the insect midgut. The symbiont titers in fifth-instar insects revealed significantly reduced population sizes of the inner core oligosaccharide mutant strains Δ<I>waaF</I> and Δ<I>waaC</I>. These two strains also negatively affected host growth rate and fitness. Furthermore, <I>R. pedestris</I> individuals colonized with the Δ<I>waaF</I> and Δ<I>waaC</I> strains were vulnerable to septic bacterial challenge, similar to insects without a <I>Burkholderia</I> symbiont. Taken together, these results suggest that the core oligosaccharide from <I>Burkholderia</I> symbionts plays a critical role in maintaining a proper symbiont population and in supporting the beneficial effects of the symbiont on its host in the <I>Riptortus–Burkholderia</I> symbiosis.</P>

      • Bacterial Cell Wall Synthesis Gene <i>uppP</i> Is Required for <i>Burkholderia</i> Colonization of the Stinkbug Gut

        Kim, Jiyeun Kate,Lee, Ho Jin,Kikuchi, Yoshitomo,Kitagawa, Wataru,Nikoh, Naruo,Fukatsu, Takema,Lee, Bok Luel American Society for Microbiology 2013 Applied and environmental microbiology Vol.79 No.16

        <P>To establish a host-bacterium symbiotic association, a number of factors involved in symbiosis must operate in a coordinated manner. In insects, bacterial factors for symbiosis have been poorly characterized at the molecular and biochemical levels, since many symbionts have not yet been cultured or are as yet genetically intractable. Recently, the symbiotic association between a stinkbug, <I>Riptortus pedestris</I>, and its beneficial gut bacterium, <I>Burkholderia</I> sp., has emerged as a promising experimental model system, providing opportunities to study insect symbiosis using genetically manipulated symbiotic bacteria. Here, in search of bacterial symbiotic factors, we targeted cell wall components of the <I>Burkholderia</I> symbiont by disruption of <I>uppP</I> gene, which encodes undecaprenyl pyrophosphate phosphatase involved in biosynthesis of various bacterial cell wall components. Under culture conditions, the Δ<I>uppP</I> mutant showed higher susceptibility to lysozyme than the wild-type strain, indicating impaired integrity of peptidoglycan of the mutant. When administered to the host insect, the Δ<I>uppP</I> mutant failed to establish normal symbiotic association: the bacterial cells reached to the symbiotic midgut but neither proliferated nor persisted there. Transformation of the Δ<I>uppP</I> mutant with <I>uppP</I>-encoding plasmid complemented these phenotypic defects: lysozyme susceptibility <I>in vitro</I> was restored, and normal infection and proliferation in the midgut symbiotic organ were observed <I>in vivo</I>. The Δ<I>uppP</I> mutant also exhibited susceptibility to hypotonic, hypertonic, and centrifugal stresses. These results suggest that peptidoglycan cell wall integrity is a stress resistance factor relevant to the successful colonization of the stinkbug midgut by <I>Burkholderia</I> symbiont.</P>

      • Insect Pest Control by Manipulating Insect’s Symbiont - Insights from Studying the Bean Bug Symbiosis

        Jiyeun Kate Kim,Jong Wook Kim,You Seon Lee,Bok Luel Lee 한국응용곤충학회 2014 한국응용곤충학회 학술대회논문집 Vol.2014 No.10

        Symbiotic bacteria are common in insects. Because symbiotic bacteria are known to intimately affect the various aspects of insect host biology, ideally insects can be controlled by manipulating their symbiont. However, the attempts to control insects through their symbiont have been very limited. The paucity of the insect pest control using their symbiont is most likely due to the poor understanding of the symbiotic interactions between host insect and symbiont, which is attributed to the difficulty in cultivation of insect symbionts. However, the recently established bean bug, Riptortus pedestris, symbiotic system provides good opportunities to study insect’s symbiont in molecular level through their cultivable symbionts. Bean bugs acquire genus Burkholderia cells from environment and harbor them as their gut symbionts in the specialized posterior midgut. The genome of the Burkholderia symbiont was sequenced, and the genomic information has been used to generate the genetically manipulated Burkholderia symbiont strains. After orally administering the mutant Burkholderia symbionts into bean bugs for symbiotic association, the bacterial colonization levels in the host gut and host phenotypes were analyzed. As a result, we have identified novel symbiotic factors necessary for establishing successful association with host. Our recent understandings on the bacterial symbiotic factors demonstrate a great possibility to control the bean bug pest using genetically modified Burkholderia symbiont.

      • Specific Midgut Region Controlling the Symbiont Population in an Insect-Microbe Gut Symbiotic Association

        Kim, Jiyeun Kate,Kim, Na Hyang,Jang, Ho Am,Kikuchi, Yoshitomo,Kim, Chan-Hee,Fukatsu, Takema,Lee, Bok Luel American Society for Microbiology 2013 Applied and environmental microbiology Vol.79 No.23

        <P>Many insects possess symbiotic bacteria that affect the biology of the host. The level of the symbiont population in the host is a pivotal factor that modulates the biological outcome of the symbiotic association. Hence, the symbiont population should be maintained at a proper level by the host's control mechanisms. Several mechanisms for controlling intracellular symbionts of insects have been reported, while mechanisms for controlling extracellular gut symbionts of insects are poorly understood. The bean bug <I>Riptortus pedestris</I> harbors a betaproteobacterial extracellular symbiont of the genus <I>Burkholderia</I> in the midgut symbiotic organ designated the M4 region. We found that the M4B region, which is directly connected to the M4 region, also harbors <I>Burkholderia</I> symbiont cells, but the symbionts therein are mostly dead. A series of experiments demonstrated that the M4B region exhibits antimicrobial activity, and the antimicrobial activity is specifically potent against the <I>Burkholderia</I> symbiont but not the cultured <I>Burkholderia</I> and other bacteria. The antimicrobial activity of the M4B region was detected in symbiotic host insects, reaching its highest point at the fifth instar, but not in aposymbiotic host insects, which suggests the possibility of symbiont-mediated induction of the antimicrobial activity. This antimicrobial activity was not associated with upregulation of antimicrobial peptides of the host. Based on these results, we propose that the M4B region is a specialized gut region of <I>R. pedestris</I> that plays a critical role in controlling the population of the <I>Burkholderia</I> gut symbiont. The molecular basis of the antimicrobial activity is of great interest and deserves future study.</P>

      • SCISCIESCOPUS

        Purine Biosynthesis, Biofilm Formation, and Persistence of an Insect-Microbe Gut Symbiosis

        Kim, Jiyeun Kate,Kwon, Jeong Yun,Kim, Soo Kyoung,Han, Sang Heum,Won, Yeo Jin,Lee, Joon Hee,Kim, Chan-Hee,Fukatsu, Takema,Lee, Bok Luel American Society for Microbiology 2014 Applied and environmental microbiology Vol.80 No.14

        <P>The <I>Riptortus-Burkholderia</I> symbiotic system is an experimental model system for studying the molecular mechanisms of an insect-microbe gut symbiosis. When the symbiotic midgut of <I>Riptortus pedestris</I> was investigated by light and transmission electron microscopy, the lumens of the midgut crypts that harbor colonizing <I>Burkholderia</I> symbionts were occupied by an extracellular matrix consisting of polysaccharides. This observation prompted us to search for symbiont genes involved in the induction of biofilm formation and to examine whether the biofilms are necessary for the symbiont to establish a successful symbiotic association with the host. To answer these questions, we focused on <I>purN</I> and <I>purT</I>, which independently catalyze the same step of bacterial purine biosynthesis. When we disrupted <I>purN</I> and <I>purT</I> in the <I>Burkholderia</I> symbiont, the Δ<I>purN</I> and Δ<I>purT</I> mutants grew normally, and only the Δ<I>purT</I> mutant failed to form biofilms. Notably, the Δ<I>purT</I> mutant exhibited a significantly lower level of cyclic-di-GMP (c-di-GMP) than the wild type and the Δ<I>purN</I> mutant, suggesting involvement of the secondary messenger c-di-GMP in the defect of biofilm formation in the Δ<I>purT</I> mutant, which might operate via impaired purine biosynthesis. The host insects infected with the Δ<I>purT</I> mutant exhibited a lower infection density, slower growth, and lighter body weight than the host insects infected with the wild type and the Δ<I>purN</I> mutant. These results show that the function of <I>purT</I> of the gut symbiont is important for the persistence of the insect gut symbiont, suggesting the intricate biological relevance of purine biosynthesis, biofilm formation, and symbiosis.</P>

      • Purine biosynthesis-deficient Burkholderia mutants are incapable of symbiotic accommodation in the stinkbug

        Kim, Jiyeun Kate,Jang, Ho Am,Won, Yeo Jin,Kikuchi, Yoshitomo,Heum Han, Sang,Kim, Chan-Hee,Nikoh, Naruo,Fukatsu, Takema,Lee, Bok Luel Springer Science and Business Media LLC 2014 The ISME journal Vol.8 No.3

        <P>The Riptortus-Burkholderia symbiotic system represents a promising experimental model to study the molecular mechanisms involved in insect-bacterium symbiosis due to the availability of genetically manipulated Burkholderia symbiont. Using transposon mutagenesis screening, we found a symbiosis-deficient mutant that was able to colonize the host insect but failed to induce normal development of host's symbiotic organ. The disrupted gene was identified as purL involved in purine biosynthesis. In vitro growth impairment of the purL mutant and its growth dependency on adenine and adenosine confirmed the functional disruption of the purine synthesis gene. The purL mutant also showed defects in biofilm formation, and this defect was not rescued by supplementation of purine derivatives. When inoculated to host insects, the purL mutant was initially able to colonize the symbiotic organ but failed to attain a normal infection density. The low level of infection density of the purL mutant attenuated the development of the host's symbiotic organ at early instar stages and reduced the host's fitness throughout the nymphal stages. Another symbiont mutant-deficient in a purine biosynthesis gene, purM, showed phenotypes similar to those of the purL mutant both in vitro and in vivo, confirming that the purL phenotypes are due to disrupted purine biosynthesis. These results demonstrate that the purine biosynthesis genes of the Burkholderia symbiont are critical for the successful accommodation of symbiont within the host, thereby facilitating the development of the host's symbiotic organ and enhancing the host's fitness values.</P>

      • Polyester synthesis genes associated with stress resistance are involved in an insect–bacterium symbiosis

        Kim, Jiyeun Kate,Won, Yeo Jin,Nikoh, Naruo,Nakayama, Hiroshi,Han, Sang Heum,Kikuchi, Yoshitomo,Rhee, Young Ha,Park, Ha Young,Kwon, Jeong Yun,Kurokawa, Kenji,Dohmae, Naoshi,Fukatsu, Takema,Lee, Bok Lue National Academy of Sciences 2013 PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF Vol.110 No.26

        <P>Many bacteria accumulate granules of polyhydroxyalkanoate (PHA) within their cells, which confer resistance to nutritional depletion and other environmental stresses. Here, we report an unexpected involvement of the bacterial endocellular storage polymer, PHA, in an insect–bacterium symbiotic association. The bean bug <I>Riptortus pedestris</I> harbors a beneficial and specific gut symbiont of the β-proteobacterial genus <I>Burkholderia</I>, which is orally acquired by host nymphs from the environment every generation and easily cultivable and genetically manipulatable. Biochemical and cytological comparisons between symbiotic and cultured <I>Burkholderia</I> detected more PHA granules consisting of poly-3-hydroxybutyrate and associated phasin (PhaP) protein in the symbiotic <I>Burkholderia</I>. Among major PHA synthesis genes, <I>phaB</I> and <I>phaC</I> were disrupted by homologous recombination together with the <I>phaP</I> gene, whereby <I>ΔphaB</I>, <I>ΔphaC</I>, and <I>ΔphaP</I> mutants were generated. Both in culture and in symbiosis, accumulation of PHA granules was strongly suppressed in <I>ΔphaB</I> and <I>ΔphaC</I>, but only moderately in <I>ΔphaP.</I> In symbiosis, the host insects infected with <I>ΔphaB</I> and <I>ΔphaC</I> exhibited significantly lower symbiont densities and smaller body sizes. These deficient phenotypes associated with <I>ΔphaB</I> and <I>ΔphaC</I> were restored by complementation of the mutants with plasmids encoding a functional <I>phaB</I>/<I>phaC</I> gene. Retention analysis of the plasmids revealed positive selection acting on the functional <I>phaB</I>/<I>phaC</I> in symbiosis. These results indicate that the PHA synthesis genes of the <I>Burkholderia</I> symbiont are required for normal symbiotic association with the <I>Riptortus</I> host. In vitro culturing analyses confirmed vulnerability of the PHA gene mutants to environmental stresses, suggesting that PHA may play a role in resisting stress under symbiotic conditions.</P>

      • Immunogenicity and Immuno-susceptibility of Burkholderia Symbionts in Stinkbug, Riptortus pedestris

        Dae Woo Son,Jiyeun Kate Kim,Chan Hee Kim,Bok Luel Lee 한국응용곤충학회 2014 한국응용곤충학회 학술대회논문집 Vol.2014 No.10

        Riptortus pedestris possesses Burkholderia as gut symbiont in a symbiotic organ M4 midgut. To answer why Burkholderia symbionts are not eliminated by Riptortu s immune responses, we developed two hypotheses: (i) Burkholderia symbionts do not activate host innate immunity, or (ii) Burkholderia symbionts are resistant to th e host immune responses. For the first hypothesis, we compared the antimicrobial activities of the cultured Burkholderia-injected hemolymph and symbiotic Burkhol deria-injected hemolymphs. As a result, the symbiotic Burkholderia induced antim icrobial activity like the cultured Burkholderia, indicating the symbiotic cells are st ill immunogentic to host. However, when the activated hemolymph was treated to the Burkholderia cells, the symbiotic Burkholderia showed much higher susceptibi lity than the cultured Burkholderia. To understand molecular basis of these results, we purified antimicrobial peptides (AMPs) from Riptortus hemolymph. Similarly, the symbiotic Burkholderia exhibited the high susceptibility to the purified AMPs, riptocin and rip-defensin. To understand how symbiotic Burkholderia can survive in host in spite of their immuno-susceptibility, we examined the AMP expression i n the M4 midgut. Interestingly, the expression of AMPs is suppressed in the M4 mi dgut in comparison to that of the fat body. Finally, we proposed that the immuno-su sceptibility of Burkholderia symbiont helps them to retain in the symbiotic organ. Our in vivo data showing the rapid clearance of the symbiotic Burkholderia after inj ection to host Riptortus supports our proposal.

      • Selection Mechanism for the Burkholderia Gut Symbiont via Host Salivary Gland

        Ho Am Jang,Jiyeun Kate Kim,Bok Luel Lee 한국응용곤충학회 2014 한국응용곤충학회 학술대회논문집 Vol.2014 No.10

        The Riptortus pedestris-Burkholderia symbiotic system is a promising model for understanding molecular mechanism of symbiosis. In previous studies, the Burkholderia symbiont has been shown to play important biological roles in the growth and fitness of host R. pedestris. The Burkholderia symbiont, one of bacteria found in the soil, is the only bacterium that can colonize the symbiotic midgut region of R. pedestris. However, the molecular mechanism of host selectivity for the Burkholderia symbiont remains unknown. To determine where the selection occurs, we firstly compared initial infectivity of different mid-gut regions after oral infection of Escherichia coli and Burkholderia. Interestingly, E. coli were not detected in any regions of mid-gut, while Burkholderia could reach to the posterior region of mid-gut. Therefore, we hypothesized that host selectivity for the Burkholderia symbiont is occurred in the salivary gland. To address this hypothesis, we treated E. coli and Burkholderia with lysate of salivary gland and examined their survival by estimation of colony forming unit (CFU) on the plate. We found that E. coli, but not Burkholderia, was susceptible to the lysate of salivary gland. To determine molecular basis of the selective mechanism in the salivary gland, we analyzed antimicrobial proteins (AMPs) from lysate of salivary gland. we identified three AMPs, namely rip-trialysin1, rip-trialysin2 and lysozyme and further purified rip-trialysin1 and rip-trialysin2. When E. coli and Burkholderia were treated with rip-trialysin1 and rip-trialysin2, rip-trialysin1 exhibited little antimicrobial activity, but rip-trialysin2 exhibited antimicrobial activity. Furthermore, we found that E. coli was susceptible, but Burkholderia is resistant to commerciallypurchased egg white lysozyme. Our results suggest that R. pedestris salivary gland provides a chance of selection for the Burkholderia symbiont and lysozyme in salivary gland seems to play an important role for the selection of gut symbiont.

      • Gut Symbiont Burkholderia are Susceptible to Host Humoral Immunity After Established Infection on Stinkbug Symbiosis

        Dae Woo Son,Chan-Hee Kim,Ye Rang Heo,Jun Beom Lee,Ho Am Jang,Jong Wook Kim,Min Young Seong,Jae Hyun Cho,Jiyeun Kate Kim,Bok Luel Lee 한국응용곤충학회 2014 한국응용곤충학회 학술대회논문집 Vol.2014 No.04

        The Riptortus (stinkbug) has a specialized symbiotic organ, M4 midgut, to harboring symbiont Burkholderia. M4 midgut is located in abdomen and surrounded with insect hemolymph. Recently our group demonstrated that symbiotic Burkholderia showed different physiology after adapting in M4 gut compare with in vitro cultured Burkholderia. And population of symbiotic Burkholderia in the M4 midgut is regulated by special organ. However, the molecular mechanism to prevent spreading and migrating symbiont bacteria to other host tissues from symbiotic organ is not clear. Therefore, we assumed that symbiont Burkholderia are susceptible to host humoral immunity after established infection in M4 midgut to prevent spreading and migrating into the other host tissues through Riptortus hemolymph. To prove this assuming, we tested the susceptibility and survival rate of symbiont Burkholderia in hemolymph of Riptortus in vitro and in vivo. We also examined the susceptibility of symbiont Burkholderia using purified antimicrobial peptides (AMP), pyrrhocoricin-like, thanatin-like and defensin-like AMPs. Finally, we tested inducing ability for AMPs by systemic infection of symbiotic Burkholderia. Gene expression of purified AMPs was not different after systemic infection of both symbiont and in vitro cultured Burkholderia. Surprisingly, in vitro cultured Burkholderia resisted on bacteria injected hemolymph and purified AMPs but symbiont Burkholderia were highly susceptible in bacteria injected hemolymph and purified AMP. These results suggest that symbiont Burkholderia can't survive in the hemolymph after escaping symbiotic organ. Moreover, humoral immunity of host Riptortus is important to prevent spreading and migrating symbiont Burkholderia into the other host tissue or organ from symbiotic organ.

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