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Proc Natl Acad Sci U S A. 2017 Oct 3;114(40):E8382-E8391. doi: 10.1073/pnas.1712857114. Epub 2017 Sep 18.

Small genome symbiont underlies cuticle hardness in beetles.

Author information

1
Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology, Tsukuba 305-8566, Japan; h-anbutsu@aist.go.jp t-fukatsu@aist.go.jp.
2
Computational Bio Big-Data Open Innovation Laboratory, National Institute of Advanced Industrial Science and Technology, Tokyo 169-8555, Japan.
3
Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology, Tsukuba 305-8566, Japan.
4
Department of Liberal Arts, The Open University of Japan, Chiba 261-8586, Japan.
5
Faculty of Science, Kyushu University, Fukuoka 819-0395, Japan.
6
National Agriculture and Food Research Organization, Kyushu Okinawa Agricultural Research Center, Okinawa 901-0336, Japan.
7
Faculty of Education, Kagoshima University, Kagoshima 890-0065, Japan.
8
Division of Applied Life Sciences, Graduate School of Agriculture, Kyoto University, Kyoto 606-8502, Japan.
9
Graduate School of Frontier Sciences, University of Tokyo, Chiba 277-8561, Japan.
10
Graduate School of Advanced Science and Engineering, Waseda University, Tokyo 169-8555, Japan.
11
DNA Sequencing Section, Okinawa Institute of Science and Technology Graduate University, Okinawa 904-0495, Japan.
12
Marine Genomics Unit, Okinawa Institute of Science and Technology Graduate University, Okinawa 904-0495, Japan.
13
NIBB Core Research Facilities, National Institute for Basic Biology, Okazaki 444-8585, Japan.
14
Department of Biological Sciences, Graduate School of Science, University of Tokyo, Tokyo 113-0033, Japan.
15
Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba 305-8572, Japan.

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.

KEYWORDS:

Nardonella; genome; symbiont; tyrosine; weevil

PMID:
28923972
PMCID:
PMC5635926
DOI:
10.1073/pnas.1712857114
[Indexed for MEDLINE]
Free PMC Article

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