期刊
出版社
NATL ACAD SCIENCES
DOI: 10.1073/pnas.2103957118
关键词
symbiont capsule; host secretion protein; vertical transmission; odorant-binding protein; symbiont preservation
资金
- Japan Society for the Promotion of Science KAKENHI [JP25221107]
- Japan Science and Technology Agency ERATO [JPMJER1803, JPMJER1902]
Microbial symbioses play a significant role in diverse organisms, with long-lasting associations leading to symbiont genome erosion and potential extinction. The discovery of a host protein essential for sustaining symbiosis in Plataspid stinkbugs sheds light on how intimate host-symbiont associations can be maintained over evolutionary time. In addition to the host's guardian protein, the symbiont's molecular chaperone, GroEL, is overproduced in capsules, compensating for the symbiont's eroding functionality.
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.
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