Host’s guardian protein counters degenerative symbiont evolution

Ryuichi Koga, Masahiko Tanahashi, Naruo Nikoh, Takahiro Hosokawa, Xian Ying Meng, Minoru Moriyama, Takema Fukatsu

研究成果: Contribution to journalArticle査読

2 被引用数 (Scopus)

抄録

Microbial symbioses significantly contribute to diverse organisms, where long-lasting associations tend to result in symbiont genome erosion, uncultivability, extinction, and replacement. How such inherently deteriorating symbiosis can be harnessed to stable partnership is of general evolutionary interest. Here, we report the discovery of a host protein essential for sustaining symbiosis. Plataspid stinkbugs obligatorily host an uncultivable and genome-reduced gut symbiont, Ishikawaella. Upon oviposition, females deposit “capsules” for symbiont delivery to offspring. Within the capsules, the fragile symbiotic bacteria survive the harsh conditions outside the host until acquired by newborn nymphs to establish vertical transmission. We identified a single protein dominating the capsule content, which is massively secreted by female-specific intestinal organs, embedding the symbiont cells, and packaged into the capsules. Knockdown of the protein resulted in symbiont degeneration, arrested capsule production, symbiont transmission failure, and retarded nymphal growth, unveiling its essential function for ensuring symbiont survival and vertical transmission. The protein originated from a lineage of odorant-binding protein-like multigene family, shedding light on the origin of evolutionary novelty regarding symbiosis. Experimental suppression of capsule production extended the female’s lifespan, uncovering a substantial cost for maintaining symbiosis. In addition to the host’s guardian protein, the symbiont’s molecular chaperone, GroEL, was overproduced in the capsules, highlighting that the symbiont’s eroding functionality is compensated for by stabilizer molecules of host and symbiont origins. Our finding provides insight into how intimate host–symbiont associations can be maintained over evolutionary time despite the symbiont’s potential vulnerability to degeneration and malfunctioning.

本文言語英語
論文番号e2103957118
ジャーナルProceedings of the National Academy of Sciences of the United States of America
118
25
DOI
出版ステータス出版済み - 6 22 2021

All Science Journal Classification (ASJC) codes

  • 一般

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