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• Chemotaxis promotes early colonization and microbiogeography of <i>Caballeronia insecticola</i> in the gut symbiotic organ of <i>Riptortus pedestris</i>

  Kota Ishigami, Antoine-Olivier Lirette, Hiroyuki Shimoji, Yoshitomo Kikuchi

  Applied and Environmental Microbiology ( American Society for Microbiology )    2026.09 [ Peer Review Accepted ]

  Type of publication: Research paper (scientific journal)

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  ABSTRACT Many plants and animals form specific symbioses with microorganisms, relying on bidirectional host–bacteria interactions. However, knowledge about the evolution of symbiont traits enabling such specificity remains limited. The bean bug Riptortus pedestris acquires Caballeronia from environmental soil and harbors it in its gut symbiotic organ. This bug- Caballeronia symbiosis is an ideal model to clarify the evolutionary process of symbiotic bacteria because members of outgroups, such as Paraburkholderia and Pandoraea , can also colonize the host symbiotic organ but are outcompeted when co-inoculated with the native symbiont, Caballeronia . Here, we investigated mechanisms underlying the competitive performance of Caballeronia within the insect gut. Spatial analyses revealed that wild-type Caballeronia showed directional localization toward the symbiotic organ and colonized the M4 region faster than related bacteria. A cheA insertion mutant exhibited delayed early colonization and reduced competitive performance in co-infection assays although both strains ultimately reached similar levels of crypt colonization. In addition, microscopic observations revealed strain-specific aggregation patterns within the symbiotic organ, providing additional insight into bacterial spatial organization during host colonization. Together, these findings suggest that chemotaxis accelerates early symbiotic organ colonization and enhances competitive performance during the initial stages of symbiont establishment. More broadly, our results highlight the importance of spatial and temporal dynamics in shaping host–microbe associations and provide a framework for understanding how bacterial traits contribute to the evolution of symbiotic specificity. IMPORTANCE Riptortus pedestris , a major soybean pest in East Asia, acquires symbiotic bacteria from the environment every generation, yet its gut is consistently and specifically colonized by Caballeronia species. The evolutionary traits that underlie this strong symbiotic specificity remain poorly understood. Here, we demonstrate that chemotaxis accelerates early colonization of the symbiotic organ by Caballeronia and enhances its competitive performance relative to closely related bacteria. Using comparative colonization assays with wild-type, chemotaxis-deficient mutants, closely related bacteria, and an out-group species, we show that chemotaxis contributes to competitive performance during the initial stages of symbiotic organ colonization. Our findings indicate that ecological and behavioral traits, including chemotaxis, contribute to the establishment of exclusive symbiotic associations, providing new insight into how symbiotic specificity may evolve in horizontally transmitted systems.

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• Soil pH as an external filter shaping stink bug–Burkholderia gut symbiosis

  Hideomi Itoh, Hiroyuki Shimoji, Daisuke Nakane, Seonghan Jang, Yoshitomo Kikuchi

  Microbiome ( Springer Science and Business Media LLC )  14 ( 1 )   2026.05 [ Peer Review Accepted ]

  Type of publication: Research paper (scientific journal)

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  Abstract Background Many animals and plants establish intimate symbiotic relationships with specific microorganisms acquired from the environment. Given the immense diversity of environmental microbiomes, selecting appropriate partners from such a vast microbial pool poses a critical challenge for host organisms. To meet this challenge, hosts have evolved sophisticated internal partner-choice mechanisms that ensure stable associations with beneficial microbes. However, because these symbionts primarily inhabit external environments, environmental conditions themselves are also expected to influence the establishment of symbiosis. Despite this expectation, the mechanistic role of external environmental filters in shaping the intended symbiosis remains largely unexplored. Focusing on stink bugs, which acquire their symbiotic bacteria from soil each generation, we investigated how soil properties influence the establishment of gut symbiosis in terrestrial insects. Results Microbiome analyses confirmed that Burkholderia sensu lato overwhelmingly dominates a specific gut organ in six stink bug species from the superfamilies Coreoidea and Lygaeoidea, including serious agricultural pests (relative abundance ranging from 74.5 to 100%). Rearing experiments with isolated Burkholderia revealed that insects were strictly dependent on this symbiont; failure to acquire it from soil severely reduced host growth and reproduction, indicating that the availability of symbionts from soil can represent an ecological constraint. Field surveys identified patches of exceptionally high stink bug density in weedy fields with soil pH &lt; 7.0, whereas such aggregations were absent in fields with pH ≥ 7.0. Laboratory experiments with collected field soils showed that the abundance of Burkholderia in soils was negatively correlated with soil pH, and stink bugs readily acquired their symbionts from soils with pH &lt; 7.0 but rarely from soils with pH ≥ 7.0. Experimental manipulations of soil pH followed by rearing experiments confirmed that increasing soil pH to 7–8 markedly suppressed symbiont acquisition by the host, likely by impairing symbiont growth and motility. Conclusions We demonstrate that, beyond host-intrinsic mechanisms, a soil chemical property can act as an externally filter that constrains symbiont acquisition prior to colonization inside the host in a stink bug– Burkholderia symbiosis. This finding highlights how local environmental conditions can shape the assembly of environmentally acquired insect–microbe symbioses.

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• Asymmetrical physiological cost of reproduction shapes caste-specific resource allocation in an ant, <i>Diacamma</i> cf. <i>indicum</i> from Japan

  Yasunari Tanaka, Yusuke Ishizuka, Yu Matsuura, Jilin Pan, Hiroyuki Shimoji

  Royal Society Open Science ( The Royal Society )  13 ( 2 )   2026.02 [ Peer Review Accepted ]

  Type of publication: Research paper (scientific journal)

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  Abstract In eusocial insects, queens demonstrate high reproductive capacity and extended longevity, representing examples of the trade-off in resource allocation. Workers perform non-reproductive tasks, such as caring for broods and foraging, thus reducing the energetic demands of queens. As queens dedicate their lives to reproduction, these reduced energetic demands enable them to live longer, laying many eggs. However, the physiological specialization of queens is markedly distinct from that of workers. This study examines the trade-off between immunocompetence and reproduction among castes in an ant species, Diacamma cf. indicum, from Japan, which lacks a morphological queen caste. First, gamergates (functional queens) exhibited higher expression of innate immunity genes than the workers. Second, to experimentally skew resource allocation towards immunocompetence, gamergates and reproductive workers were subjected to an immune challenge. As a result, the expression of the antimicrobial peptide gene Hymenoptaecin was increased in gamergates without compromising reproduction-related genes, such as Vitellogenin. By contrast, the expression of genes associated with reproduction was decreased in reproductive workers. Moreover, we revealed that gamergates possessed a remarkably low fat content, similar to non-reproductive foragers. These findings suggest that, while gamergates can overcome the trade-off, reproductive workers are constrained by the physiological costs of reproduction.

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• A potential risk and management of feces in the queenless ant

  Y. Ishizuka, R. Yamashita, H. Itoh, Y. Matsuura, Y. Kikuchi, H. Shimoji

  Insectes Sociaux ( Springer Science and Business Media LLC )    2024.06 [ Peer Review Accepted ]

  Type of publication: Research paper (scientific journal)

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• Reproductive potentials of task-shifting workers in a queenless ant

  Yasunari Tanaka, Kohei Oguchi, Satoshi Miyazaki, Kiyoto Maekawa, Hiroyuki Shimoji

  Insectes Sociaux ( Springer Science and Business Media LLC )    2024.02 [ Peer Review Accepted ]

  Type of publication: Research paper (scientific journal)

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• Challenging research (sprout)

  Project Year: 2023.06  -  2026.03 

  Direct: 5,000,000 (YEN)  Overheads: 6,500,000 (YEN)  Total: 1,500,000 (YEN)

• Molecular bases and evolutionary process of the in vivo flagellar drill motility.

  Grant-in-Aid for Transformative Research Areas (B)

  Project Year: 2022.05  -  2025.03 

  Direct: 41,200,000 (YEN)  Overheads: 53,560,000 (YEN)  Total: 12,360,000 (YEN)

• Grant-in-Aid for Scientific Research(B)

  Project Year: 2022.04  -  2025.03 

  Direct: 13,300,000 (YEN)  Overheads: 17,290,000 (YEN)  Total: 3,990,000 (YEN)

• Invasion mechanisms of exotic ants with special focus on Japanese invaders

  Grant-in-Aid for Scientific Research(A)

  Project Year: 2015.04  -  2020.03 

  Direct: 32,300,000 (YEN)  Overheads: 41,990,000 (YEN)  Total: 9,690,000 (YEN)

• A new synthesis through the concept of interaction between different levels of the biological hierarchy

  Grant-in-Aid for Scientific Research(B)

  Project Year: 2015.04  -  2018.03 

  Investigator(s): TSUJI Mizuki 

  Direct: 13,900,000 (YEN)  Overheads: 18,070,000 (YEN)  Total: 4,170,000 (YEN)

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  We addressed questions on interaction between different levels of the biological hierarchy in order to integrate micro and macro ecologies. We especially focused on the relationship between intra-specific dynamics, such as kin selection and sexual selection, and inter-specific dynamics, such as host-parasite dynamics and model-mimic dynamics, in the community through theoretical and empirical approaches. We empirically showed examples (though some are yet potential) of such adaptive dynamics in ants, clonal plants, butterflies, fish and other systems.

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Social Activity 【 display / non-display 】

• 2024.04

  　

  　

  

• 2025.11

  　

  　

  

• 2023.07