Small genome symbiont underlies cuticle hardness in beetles

Hisashi Anbutsu, Minoru Moriyama, Naruo Nikoh, Takahiro Hosokawa, Ryo Futahashi, Masahiko Tanahashi, Xian Ying Meng, Takashi Kuriwada, Naoki Mori, Kenshiro Oshima, Masahira Hattori, Manabu Fujie, Noriyuki Satoh, Taro Maeda, Shuji Shigenobu, Ryuichi Koga, Takema Fukatsu

    Research output: Contribution to journalArticle

    18 Citations (Scopus)

    Abstract

    Beetles, representing the majority of the insect species diversity, are characterized by thick and hard cuticle, which plays important roles for their environmental adaptation and underpins their inordinate diversity and prosperity. Here, we report a bacterial endosymbiont extremely specialized for sustaining beetle’s cuticle formation. Many weevils are associated with a γ-proteobacterial endosymbiont lineage Nardonella, whose evolutionary origin is estimated as older than 100 million years, but its functional aspect has been elusive. Sequencing of Nardonella genomes from diverse weevils unveiled drastic size reduction to 0.2 Mb, in which minimal complete gene sets for bacterial replication, transcription, and translation were present but almost all of the other metabolic pathway genes were missing. Notably, the only metabolic pathway retained in the Nardonella genomes was the tyrosine synthesis pathway, identifying tyrosine provisioning as Nardonella’s sole biological role. Weevils are armored with hard cuticle, tyrosine is the principal precursor for cuticle formation, and experimental suppression of Nardonella resulted in emergence of reddish and soft weevils with low tyrosine titer, confirming the importance of Nardonella-mediated tyrosine production for host’s cuticle formation and hardening. Notably, Nardonella’s tyrosine synthesis pathway was incomplete, lacking the final step transaminase gene. RNA sequencing identified host’s aminotransferase genes up-regulated in the bacteriome. RNA interference targeting the aminotransferase genes induced reddish and soft weevils with low tyrosine titer, verifying host’s final step regulation of the tyrosine synthesis pathway. Our finding highlights an impressively intimate and focused aspect of the host–symbiont metabolic integrity via streamlined evolution for a single biological function of ecological relevance.

    Original languageEnglish
    Pages (from-to)E8382-E8391
    JournalProceedings of the National Academy of Sciences of the United States of America
    Volume114
    Issue number40
    DOIs
    Publication statusPublished - 2017 Oct 3

    Fingerprint

    Beetles
    Hardness
    Tyrosine
    Weevils
    Genome
    Transaminases
    Metabolic Networks and Pathways
    Genes
    RNA Sequence Analysis
    Bacterial Genes
    Gene Targeting
    RNA Interference
    Insects

    Keywords

    • Genome
    • Nardonella
    • Symbiont
    • Tyrosine
    • Weevil

    ASJC Scopus subject areas

    • General

    Cite this

    Anbutsu, H., Moriyama, M., Nikoh, N., Hosokawa, T., Futahashi, R., Tanahashi, M., ... Fukatsu, T. (2017). Small genome symbiont underlies cuticle hardness in beetles. Proceedings of the National Academy of Sciences of the United States of America, 114(40), E8382-E8391. https://doi.org/10.1073/pnas.1712857114

    Small genome symbiont underlies cuticle hardness in beetles. / Anbutsu, Hisashi; Moriyama, Minoru; Nikoh, Naruo; Hosokawa, Takahiro; Futahashi, Ryo; Tanahashi, Masahiko; Meng, Xian Ying; Kuriwada, Takashi; Mori, Naoki; Oshima, Kenshiro; Hattori, Masahira; Fujie, Manabu; Satoh, Noriyuki; Maeda, Taro; Shigenobu, Shuji; Koga, Ryuichi; Fukatsu, Takema.

    In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 114, No. 40, 03.10.2017, p. E8382-E8391.

    Research output: Contribution to journalArticle

    Anbutsu, H, Moriyama, M, Nikoh, N, Hosokawa, T, Futahashi, R, Tanahashi, M, Meng, XY, Kuriwada, T, Mori, N, Oshima, K, Hattori, M, Fujie, M, Satoh, N, Maeda, T, Shigenobu, S, Koga, R & Fukatsu, T 2017, 'Small genome symbiont underlies cuticle hardness in beetles', Proceedings of the National Academy of Sciences of the United States of America, vol. 114, no. 40, pp. E8382-E8391. https://doi.org/10.1073/pnas.1712857114
    Anbutsu, Hisashi ; Moriyama, Minoru ; Nikoh, Naruo ; Hosokawa, Takahiro ; Futahashi, Ryo ; Tanahashi, Masahiko ; Meng, Xian Ying ; Kuriwada, Takashi ; Mori, Naoki ; Oshima, Kenshiro ; Hattori, Masahira ; Fujie, Manabu ; Satoh, Noriyuki ; Maeda, Taro ; Shigenobu, Shuji ; Koga, Ryuichi ; Fukatsu, Takema. / Small genome symbiont underlies cuticle hardness in beetles. In: Proceedings of the National Academy of Sciences of the United States of America. 2017 ; Vol. 114, No. 40. pp. E8382-E8391.
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    AU - Futahashi, Ryo

    AU - Tanahashi, Masahiko

    AU - Meng, Xian Ying

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