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      • Insect’s intestinal organ for symbiont sorting

        Ohbayashi, Tsubasa,Takeshita, Kazutaka,Kitagawa, Wataru,Nikoh, Naruo,Koga, Ryuichi,Meng, Xian-Ying,Tago, Kanako,Hori, Tomoyuki,Hayatsu, Masahito,Asano, Kozo,Kamagata, Yoichi,Lee, Bok Luel,Fukatsu, Tak National Academy of Sciences 2015 PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF Vol.112 No.37

        <P><B>Significance</B></P><P>In general, animals have a mouth for feeding, an anus for defecation, and a gut connecting them for digestion and absorption. However, we discovered that the stinkbug’s gut is functionally disconnected in the middle by a previously unrecognized organ for symbiont sorting, which blocks food fluid and nonsymbiotic bacteria but selectively allows passing of a specific bacterial symbiont. Though very tiny and inconspicuous, the organ governs the configuration and specificity of stinkbug gut symbiosis, wherein the posterior gut region is devoid of food flow, populated by a specific bacterial symbiont, and transformed into an isolated organ for symbiosis. Mutant analyses showed that the symbiont’s flagellar motility is needed for passing the host organ, highlighting intricate host–symbiont interactions underpinning the symbiont sorting process.</P><P>Symbiosis has significantly contributed to organismal adaptation and diversification. For establishment and maintenance of such host–symbiont associations, host organisms must have evolved mechanisms for selective incorporation, accommodation, and maintenance of their specific microbial partners. Here we report the discovery of a previously unrecognized type of animal organ for symbiont sorting. In the bean bug <I>Riptortus pedestris</I>, the posterior midgut is morphologically differentiated for harboring specific symbiotic bacteria of a beneficial nature. The sorting organ lies in the middle of the intestine as a constricted region, which partitions the midgut into an anterior nonsymbiotic region and a posterior symbiotic region. Oral administration of GFP-labeled <I>Burkholderia</I> symbionts to nymphal stinkbugs showed that the symbionts pass through the constricted region and colonize the posterior midgut. However, administration of food colorings revealed that food fluid enters neither the constricted region nor the posterior midgut, indicating selective symbiont passage at the constricted region and functional isolation of the posterior midgut for symbiosis. Coadministration of the GFP-labeled symbiont and red fluorescent protein-labeled <I>Escherichia coli</I> unveiled selective passage of the symbiont and blockage of <I>E. coli</I> at the constricted region, demonstrating the organ’s ability to discriminate the specific bacterial symbiont from nonsymbiotic bacteria. Transposon mutagenesis and screening revealed that symbiont mutants in flagella-related genes fail to pass through the constricted region, highlighting that both host’s control and symbiont’s motility are involved in the sorting process. The blocking of food flow at the constricted region is conserved among diverse stinkbug groups, suggesting the evolutionary origin of the intestinal organ in their common ancestor.</P>

      • Trojan horse in an insect symbiosis

        Seonghan Jang,Kota Ishigami,Aoba Yoshioka,Hiroyuki Morimura,Kazutaka Takeshita,Aya Yokota,Lionel Moulin,Peter Mergaert,Daisuke Nakane,Yoshitomo Kikuchi 한국응용곤충학회 2023 한국응용곤충학회 학술대회논문집 Vol.2023 No.10

        Many insects form mutualistic relationships with microbial symbionts, crucial for their physiological processes. The bean bug, Riptortus pedestris, establishes a unique gut symbiosis with the genus Caballeronia and consistently acquires these symbionts from surrounding soil with each generation. As a result, the bean bug unavoidably consumes a variety of environmental microbes, including potential pathogens. To address this, the bean bug has developed a specialized organ in its midgut that selectively filters out non-symbiotic microbes, thereby preventing contamination of its symbiotic organ. In this study, we identified a pathogenic strain from the genus Burkholderia that lethally affects the bean bug post-invasion of the symbiotic organ. This pathogen employs a strategy of mimicking the motility of native symbionts to infiltrate the symbiont sorting organ and displays a pronounced resistance against antimicrobial agents produced by the host. Upon establishing itself in the symbiotic organ, the pathogen breaches the midgut cells, leading to host mortality, and subsequently disperses into the external environment. Our findings unveil a cunning pathogenic tactic that exploits the mimicry of native symbionts within an insect's symbiotic framework.

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