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Global exploration of microbial symbionts in stinkbugs: host-symbiont diversity and evolution

Research Project

Project/Area Number 18KK0211
Research Category

Fund for the Promotion of Joint International Research (Fostering Joint International Research (B))

Allocation TypeMulti-year Fund
Review Section Medium-sized Section 45:Biology at organismal to population levels and anthropology, and related fields
Research InstitutionNational Institute of Advanced Industrial Science and Technology

Principal Investigator

Yoshitomo Kikuchi  国立研究開発法人産業技術総合研究所, 生命工学領域, 研究グループ長 (30571864)

Co-Investigator(Kenkyū-buntansha) 伊藤 英臣  国立研究開発法人産業技術総合研究所, 生命工学領域, 主任研究員 (70748425)
細川 貴弘  九州大学, 理学研究院, 助教 (80722206)
松浦 優  琉球大学, 熱帯生物圏研究センター, 助教 (80723824)
Project Period (FY) 2018-10-09 – 2023-03-31
Project Status Completed (Fiscal Year 2022)
Budget Amount *help
¥17,810,000 (Direct Cost: ¥13,700,000、Indirect Cost: ¥4,110,000)
Fiscal Year 2021: ¥5,330,000 (Direct Cost: ¥4,100,000、Indirect Cost: ¥1,230,000)
Fiscal Year 2020: ¥5,330,000 (Direct Cost: ¥4,100,000、Indirect Cost: ¥1,230,000)
Fiscal Year 2019: ¥5,330,000 (Direct Cost: ¥4,100,000、Indirect Cost: ¥1,230,000)
Fiscal Year 2018: ¥1,820,000 (Direct Cost: ¥1,400,000、Indirect Cost: ¥420,000)
Keywords共生 / 進化 / 微生物 / 昆虫 / 多様性 / 共生細菌 / 細菌
Outline of Final Research Achievements

In this study, our focus was on 25 families of the infraorder Pentatomomorpha, which had not yet been investigated for their endosymbiosis due to their absence in Japan. Our primary objective was to conduct a comprehensive global survey of symbiosis patterns within these stinkbug groups. Despite the challenges posed by the COVID-19 pandemic, we successfully enhanced our collaboration with the University of Arizona (USA) and CNRS (France), who played a pivotal role as our main collaborators for this project. Consequently, we conducted: 1) Identification of a novel symbiosis-related gene in a stink bug species; 2) Intercontinental comparison of symbiotic bacteria in an invasive pest bug (the pine bug); 3) Functional analyses of a facultative symbiont, Lariskella, in stink bugs; 4) Mitochondrial genome analysis of the superfamily Lygaeoidea and exploration of the symbiosis system in the family Heterogastridae.

Academic Significance and Societal Importance of the Research Achievements

緊密な国際共同研究により、カメムシ下目昆虫の微生物共生系について多くの新知見を得ることができた。特に本研究では、腸内細菌の維持において気管による酸素供給が重要な役割を果たすことを明らかにし、さらにその気管の形成に活性酸素種が必須であることを突きとめた。これは、昆虫と微生物の共生維持機構に関する新発見であるとともに、昆虫における気管形成の新規メカニズムの解明に繋がる重要な成果と言える。本研究ではさらに、国際ネットワークを駆使することで、世界的侵入害虫マツヘリカメムシについて内部共生系の大陸間比較を行うことに初めて成功し、宿主の分布拡大とともに共生系にどのような変化が引き起こされたのか解明した。

Report

(7 results)
  • 2022 Annual Research Report   Final Research Report ( PDF )
  • 2021 Research-status Report
  • 2020 Research-status Report
  • 2019 Research-status Report
  • 2018 Research-status Report
  • Products Report
  • Research Products

    (58 results)

All 2023 2022 2021 2020 2019 2018 Other

All Int'l Joint Research (15 results) Journal Article (16 results) (of which Int'l Joint Research: 13 results,  Peer Reviewed: 16 results,  Open Access: 10 results) Presentation (26 results) (of which Int'l Joint Research: 6 results,  Invited: 11 results) Patent(Industrial Property Rights) (1 results) (of which Overseas: 1 results)

  • [Int'l Joint Research] CNRS(フランス)

    • Related Report
      2022 Annual Research Report
  • [Int'l Joint Research] University of Arizona/University of Texas(米国)

    • Related Report
      2022 Annual Research Report
  • [Int'l Joint Research] CSIRO(オーストリア)

    • Related Report
      2022 Annual Research Report
  • [Int'l Joint Research] アリゾナ大学/テキサス大学(米国)

    • Related Report
      2021 Research-status Report
  • [Int'l Joint Research] CNRS(フランス)

    • Related Report
      2021 Research-status Report
  • [Int'l Joint Research] CSIRO(オーストラリア)

    • Related Report
      2021 Research-status Report
  • [Int'l Joint Research] アリゾナ大学(米国)

    • Related Report
      2020 Research-status Report
  • [Int'l Joint Research] CNRS(フランス)

    • Related Report
      2020 Research-status Report
  • [Int'l Joint Research] CSIRO(オーストラリア)

    • Related Report
      2020 Research-status Report
  • [Int'l Joint Research] アリゾナ大学(米国)

    • Related Report
      2019 Research-status Report
  • [Int'l Joint Research] CNRS(フランス)

    • Related Report
      2019 Research-status Report
  • [Int'l Joint Research] CSIRO(オーストラリア)

    • Related Report
      2019 Research-status Report
  • [Int'l Joint Research] CNRS(フランス)

    • Related Report
      2018 Research-status Report
  • [Int'l Joint Research] Ghent University(ベルギー)

    • Related Report
      2018 Research-status Report
  • [Int'l Joint Research] University of Arizona(米国)

    • Related Report
      2018 Research-status Report
  • [Journal Article] Symbiont coordinates stem cell proliferation, apoptosis, and morphogenesis of gut symbiotic organ in the stinkbug-Caballeronia symbiosis2023

    • Author(s)
      Jang Seonghan、Matsuura Yu、Ishigami Kota、Mergaert Peter、Kikuchi Yoshitomo
    • Journal Title

      Frontiers in Physiology

      Volume: 13 Pages: 01-13

    • DOI

      10.3389/fphys.2022.1071987

    • Related Report
      2022 Annual Research Report
    • Peer Reviewed / Open Access / Int'l Joint Research
  • [Journal Article] Intercontinental Diversity of <i>Caballeronia</i> Gut Symbionts in the Conifer Pest Bug <i>Leptoglossus occidentalis</i>2022

    • Author(s)
      Ohbayashi Tsubasa、Cossard Raynald、Lextrait Ga?lle、Hosokawa Takahiro、Lesieur Vincent、Takeshita Kazutaka、Tago Kanako、Mergaert Peter、Kikuchi Yoshitomo
    • Journal Title

      Microbes and Environments

      Volume: 37 Issue: 3 Pages: n/a

    • DOI

      10.1264/jsme2.ME22042

    • ISSN
      1342-6311, 1347-4405
    • Related Report
      2022 Annual Research Report
    • Peer Reviewed / Open Access / Int'l Joint Research
  • [Journal Article] Obligate Gut Symbiotic Association with Caballeronia in the Mulberry Seed Bug Paradieuches dissimilis (Lygaeoidea: Rhyparochromidae)2022

    • Author(s)
      Ishigami Kota、Jang Seonghan、Itoh Hideomi、Kikuchi Yoshitomo
    • Journal Title

      Microbial Ecology

      Volume: - Issue: 2 Pages: 1307-1318

    • DOI

      10.1007/s00248-022-02117-2

    • Related Report
      2022 Annual Research Report
    • Peer Reviewed / Open Access / Int'l Joint Research
  • [Journal Article] Insecticide resistance governed by gut symbiosis in a rice pest, Cletus punctiger, under laboratory conditions2021

    • Author(s)
      Ishigami Kota、Jang Seonghan、Itoh Hideomi、Kikuchi Yoshitomo
    • Journal Title

      Biology Letters

      Volume: 17 Issue: 3 Pages: 20200780-20200780

    • DOI

      10.1098/rsbl.2020.0780

    • Related Report
      2021 Research-status Report 2020 Research-status Report
    • Peer Reviewed / Int'l Joint Research
  • [Journal Article] Dual oxidase enables insect gut symbiosis by mediating respiratory network formation2021

    • Author(s)
      Jang Seonghan、Mergaert Peter、Ohbayashi Tsubasa、Ishigami Kota、Shigenobu Shuji、Itoh Hideomi、Kikuchi Yoshitomo
    • Journal Title

      Proceedings of the National Academy of Sciences

      Volume: 118 Issue: 10

    • DOI

      10.1073/pnas.2020922118

    • Related Report
      2021 Research-status Report 2020 Research-status Report
    • Peer Reviewed / Int'l Joint Research
  • [Journal Article] Insecticide resistance by a host-symbiont reciprocal detoxification2021

    • Author(s)
      Sato Yuya、Jang Seonghan、Takeshita Kazutaka、Itoh Hideomi、Koike Hideaki、Tago Kanako、Hayatsu Masahito、Hori Tomoyuki、Kikuchi Yoshitomo
    • Journal Title

      Nature Communications

      Volume: 12 Issue: 1 Pages: 6432-6432

    • DOI

      10.1038/s41467-021-26649-2

    • Related Report
      2021 Research-status Report
    • Peer Reviewed / Open Access
  • [Journal Article] Impact of the insect gut microbiota on ecology, evolution, and industry2020

    • Author(s)
      Jang Seonghan、Kikuchi Yoshitomo
    • Journal Title

      Current Opinion in Insect Science

      Volume: 41 Pages: 33-39

    • DOI

      10.1016/j.cois.2020.06.004

    • Related Report
      2020 Research-status Report
    • Peer Reviewed / Int'l Joint Research
  • [Journal Article] Burkholderia insecticola triggers midgut closure in the bean bug Riptortus pedestris to prevent secondary bacterial infections of midgut crypts2020

    • Author(s)
      Kikuchi Yoshitomo、Ohbayashi Tsubasa、Jang Seonghan、Mergaert Peter
    • Journal Title

      The ISME Journal

      Volume: 14 Issue: 7 Pages: 1627-1638

    • DOI

      10.1038/s41396-020-0633-3

    • Related Report
      2020 Research-status Report
    • Peer Reviewed / Int'l Joint Research
  • [Journal Article] Genomic Comparison of Insect Gut Symbionts from Divergent Burkholderia Subclades2020

    • Author(s)
      Takeshita Kazutaka、Kikuchi Yoshitomo
    • Journal Title

      Genes

      Volume: 11 Issue: 7 Pages: 744-744

    • DOI

      10.3390/genes11070744

    • Related Report
      2020 Research-status Report
    • Peer Reviewed / Open Access
  • [Journal Article] Re-opening of the symbiont sorting organ with aging in Riptortus pedestris2020

    • Author(s)
      Jang Seonghan、Kikuchi Yoshitomo
    • Journal Title

      Journal of Asia-Pacific Entomology

      Volume: 23 Issue: 4 Pages: 1089-1095

    • DOI

      10.1016/j.aspen.2020.09.005

    • Related Report
      2020 Research-status Report
    • Peer Reviewed / Int'l Joint Research
  • [Journal Article] Complete Genome Sequence of Burkholderia sp. Strain THE68, a Bacterial Symbiont Isolated from Midgut Crypts of the Seed Bug Togo hemipterus2020

    • Author(s)
      Takeshita Kazutaka、Jang Seonghan、Kikuchi Yoshitomo
    • Journal Title

      Microbiology Resource Announcements

      Volume: 9 Issue: 10

    • DOI

      10.1128/mra.00041-20

    • Related Report
      2019 Research-status Report
    • Peer Reviewed / Open Access / Int'l Joint Research
  • [Journal Article] <i>Burkholderia</i> Gut Symbionts Associated with European and Japanese Populations of the Dock Bug <i>Coreus marginatus</i> (Coreoidea: Coreidae)2019

    • Author(s)
      Ohbayashi Tsubasa、Itoh Hideomi、Lachat Joy、Kikuchi Yoshitomo、Mergaert Peter
    • Journal Title

      Microbes and Environments

      Volume: 34 Issue: 2 Pages: 219-222

    • DOI

      10.1264/jsme2.ME19011

    • NAID

      130007668566

    • ISSN
      1342-6311, 1347-4405
    • Related Report
      2019 Research-status Report
    • Peer Reviewed / Open Access / Int'l Joint Research
  • [Journal Article] Comparative cytology, physiology and transcriptomics of Burkholderia insecticola in symbiosis with the bean bug Riptortus pedestris and in culture2019

    • Author(s)
      Ohbayashi Tsubasa、Futahashi Ryo、Terashima Mia、Barri?re Quentin、Lamouche Florian、Takeshita Kazutaka、Meng Xian-Ying、Mitani Yasuo、Sone Teruo、Shigenobu Shuji、Fukatsu Takema、Mergaert Peter、Kikuchi Yoshitomo
    • Journal Title

      The ISME Journal

      Volume: 印刷中 Issue: 6 Pages: 1469-1483

    • DOI

      10.1038/s41396-019-0361-8

    • Related Report
      2019 Research-status Report 2018 Research-status Report
    • Peer Reviewed / Open Access / Int'l Joint Research
  • [Journal Article] Host?symbiont specificity determined by microbe?microbe competition in an insect gut2019

    • Author(s)
      Itoh Hideomi、Jang Seonghan、Takeshita Kazutaka、Ohbayashi Tsubasa、Ohnishi Naomi、Meng Xian-Ying、Mitani Yasuo、Kikuchi Yoshitomo
    • Journal Title

      Proceedings of the National Academy of Sciences

      Volume: 116 Issue: 45 Pages: 22673-22682

    • DOI

      10.1073/pnas.1912397116

    • Related Report
      2019 Research-status Report
    • Peer Reviewed / Open Access / Int'l Joint Research
  • [Journal Article] Identification of active and taxonomically diverse 1,4-dioxane degraders in a full-scale activated sludge system by high-sensitivity stable isotope probing2018

    • Author(s)
      Aoyagi Tomo、Morishita Fumiaki、Sugiyama Yutaka、Ichikawa Daisuke、Mayumi Daisuke、Kikuchi Yoshitomo、Ogata Atsushi、Muraoka Kenji、Habe Hiroshi、Hori Tomoyuki
    • Journal Title

      The ISME Journal

      Volume: 12 Issue: 10 Pages: 2376-2388

    • DOI

      10.1038/s41396-018-0201-2

    • Related Report
      2018 Research-status Report
    • Peer Reviewed / Open Access
  • [Journal Article] Burkholderia insecticola sp. nov., a gut symbiotic bacterium of the bean bug Riptortus pedestris2018

    • Author(s)
      Takeshita Kazutaka、Tamaki Hideyuki、Ohbayashi Tsubasa、Meng Xian-Ying、Sone Teruo、Mitani Yasuo、Peeters Charlotte、Kikuchi Yoshitomo、Vandamme Peter
    • Journal Title

      International Journal of Systematic and Evolutionary Microbiology

      Volume: 68 Issue: 7 Pages: 2370-2374

    • DOI

      10.1099/ijsem.0.002848

    • Related Report
      2018 Research-status Report
    • Peer Reviewed / Int'l Joint Research
  • [Presentation] 昆虫の腸内共生における特異性の進化2022

    • Author(s)
      菊池 義智
    • Organizer
      第6回原生生物学・共生生物学談話会
    • Related Report
      2022 Annual Research Report
    • Invited
  • [Presentation] 昆虫の生き方を決める腸内微生物2022

    • Author(s)
      菊池 義智
    • Organizer
      バイオミメティクス市民セミナー
    • Related Report
      2022 Annual Research Report
    • Invited
  • [Presentation] 昆虫と腸内細菌の共生特異性を決める多層メカニズム2022

    • Author(s)
      菊池 義智
    • Organizer
      日本マイコトキシン学会第 88 回学術講演会
    • Related Report
      2022 Annual Research Report
    • Invited
  • [Presentation] Transmissible Pesticide Resistance: Invisible Friends of Insects2022

    • Author(s)
      菊池 義智
    • Organizer
      Gordon Research Conference (GRC) Drug Resistance
    • Related Report
      2022 Annual Research Report
    • Int'l Joint Research / Invited
  • [Presentation] Homeobox遺伝子によって調節される共生器官の驚くべき形態変化!2021

    • Author(s)
      JANG Seonghan, 石神広太, 大林翼, 松浦優, MERGAERT Peter, 菊池義智
    • Organizer
      日本進化学会第23回東京大会
    • Related Report
      2021 Research-status Report
  • [Presentation] カビが運命付けるバクテリア-昆虫の相利共生2021

    • Author(s)
      石神広太, Jang Seonghan, 伊藤英臣, Mergaert Peter, 菊池義智
    • Organizer
      日本進化学会第23回東京大会
    • Related Report
      2021 Research-status Report
  • [Presentation] カびが繋ぐ昆虫とバクテリアの共生系サイクル2021

    • Author(s)
      石神 広太, Seonghan Jang, 伊藤 英臣, 大林 翼, Peter Mergaert, 菊池 義智
    • Organizer
      日本微生物生態学会第34回大会
    • Related Report
      2021 Research-status Report
  • [Presentation] 昆虫腸内共生の成立機構2021

    • Author(s)
      菊池義智
    • Organizer
      第62回日本植物生理学会年会
    • Related Report
      2020 Research-status Report
    • Invited
  • [Presentation] 共生細菌であるということ2020

    • Author(s)
      菊池 義智
    • Organizer
      第93会日本細菌学会
    • Related Report
      2019 Research-status Report
    • Invited
  • [Presentation] The simplest gut microbiota shaped by partner choice and microbial competition2020

    • Author(s)
      菊池 義智
    • Organizer
      日本生態学会第67回全国大会
    • Related Report
      2019 Research-status Report
    • Invited
  • [Presentation] The bean bug Riptortus pedestris and its Burkholderia symbiont2019

    • Author(s)
      菊池 義智
    • Organizer
      Harmful Organisms 2019 (South Kore)
    • Related Report
      2019 Research-status Report
    • Int'l Joint Research / Invited
  • [Presentation] Comparative cytology, physiology and transcriptomics between free-living and symbiotic Burkholderia symbionts reveal adaptations for colonization of its bean bug host2019

    • Author(s)
      大林翼, 二橋 亮, 重信秀治, 深津 武馬, Peter Mergaert, 菊池 義智
    • Organizer
      International Symbiosis Society 2018
    • Related Report
      2019 Research-status Report
    • Int'l Joint Research
  • [Presentation] Host-symbiont cooperation for in vivo detoxification of an insecticide2019

    • Author(s)
      菊池 義智
    • Organizer
      Gordon Research Conference (U.S.A.)
    • Related Report
      2019 Research-status Report
    • Int'l Joint Research
  • [Presentation] 昆虫における腸内共生の分子基盤2019

    • Author(s)
      菊池 義智
    • Organizer
      日本放線菌学会第65回学術講演会
    • Related Report
      2019 Research-status Report
    • Invited
  • [Presentation] 土壌微生物が昆虫に及ぼす生態系サービスの解明2019

    • Author(s)
      伊藤 英臣, 菊池 義智
    • Organizer
      日本土壌肥料学会2019年度大会
    • Related Report
      2019 Research-status Report
  • [Presentation] A novel function of Duox in insect-microbe gut symbiosis: development of trachea network and stabilization of symbiont colonization2019

    • Author(s)
      Jang Seonghan, 菊池 義智
    • Organizer
      第63回日本応用動物昆虫学会大会
    • Related Report
      2018 Research-status Report
  • [Presentation] 腸内細菌による殺虫剤のin vivo解毒プロセスの解明2019

    • Author(s)
      佐藤 由也,Jang Seonghan,伊藤 英臣,堀 知行,菊池 義智
    • Organizer
      第63回日本応用動物昆虫学会大会
    • Related Report
      2018 Research-status Report
  • [Presentation] Molecular bases of the stinkbug-Burkholderia gut symbiosis2018

    • Author(s)
      菊池 義智
    • Organizer
      2018 ESA, ESC and ESBC Joint Annual Meeting
    • Related Report
      2018 Research-status Report
    • Int'l Joint Research
  • [Presentation] 共生微物による害虫の進化~そ多様性と機能2018

    • Author(s)
      菊池 義智
    • Organizer
      平成 30 年度(第 28 回)植物細菌病談話会
    • Related Report
      2018 Research-status Report
  • [Presentation] 昆虫のプロバイオティクス2018

    • Author(s)
      菊池 義智
    • Organizer
      2018年度日本乳酸菌学会セミナー
    • Related Report
      2018 Research-status Report
    • Invited
  • [Presentation] Hidden diversity under ground: ant- and nest-associated bacterial communities revealed by meta-genomic analyses2018

    • Author(s)
      下地 博之,伊藤 英臣,松浦 優,菊池 義智
    • Organizer
      International Union for the Study of Social Insects 2018
    • Related Report
      2018 Research-status Report
    • Int'l Joint Research
  • [Presentation] ”害虫”の誕生と共生微生物2018

    • Author(s)
      菊池 義智
    • Organizer
      2018年度北日本支部札幌シンポジウム
    • Related Report
      2018 Research-status Report
    • Invited
  • [Presentation] Fish egg-associated microbiota acquired from ambient soils 水生動物の卵が土壌から獲得する細菌叢2018

    • Author(s)
      佐野 友紀,木原 稔,堀 知行,曾根 輝雄,菊池 義智,伊藤 英臣
    • Organizer
      日本微生物生態学会第32回大会
    • Related Report
      2018 Research-status Report
  • [Presentation] Diversity and distribution of microbiota associated with medaka fish メダカ常在細菌叢の多様性と分布 : エラ、体表、ヒレ、腸、卵に発達する細菌叢の解明2018

    • Author(s)
      伊藤 英臣,堀 知行,菊池 義智
    • Organizer
      日本微生物生態学会第32回大会
    • Related Report
      2018 Research-status Report
  • [Presentation] Intracellular symbiosis in lygaeoid species 腸内から細胞内へ:ナガカメムシの細胞内共生進化2018

    • Author(s)
      栗原 駿太,竹下和貴,松浦 優,徳田岳,曾根 輝雄,伊藤 英臣,菊池 義智
    • Organizer
      日本微生物生態学会第32回大会
    • Related Report
      2018 Research-status Report
  • [Presentation] "Ant- and nest-associated bacterial communities revealed by meta-genomic analyses メタゲノムで解き明かすトゲオオハリアリの細菌叢 -社会に潜むその多様性と分布-"2018

    • Author(s)
      下地 博之,伊藤 英臣,松浦 優,菊池 義智
    • Organizer
      日本微生物生態学会第32回大会
    • Related Report
      2018 Research-status Report
  • [Patent(Industrial Property Rights)] 害虫の呼吸器形成機構を標的とする新規害虫防除方法2023

    • Inventor(s)
      菊池 義智
    • Industrial Property Rights Holder
      国立研究開発法人産業技術総合研究所
    • Industrial Property Rights Type
      特許
    • Filing Date
      2023
    • Related Report
      Products Report
    • Overseas

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Published: 2018-10-12   Modified: 2025-03-27  

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