Endosymbiotic Candidates for Parasitoid Defense in Exotic and Native New Zealand Weevils

White, Jennifer A.; Richards, N.K.; Laugraud, Aurélie; Saeed, Abiya; Curry, Meghan M.; McNeill, M.R.

doi:10.1007/s00248-014-0561-8

Cited by 27 publications

(34 citation statements)

References 70 publications

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“…While the Nardonella symbionts have been conserved among diverse weevils and cospeciated with the weevil hosts for over 100 My (23)(24)(25)(26)(27)(28)(29)(30)(31), previous studies have identified a number of weevil lineages in which the Nardonella symbiont had been either lost or replaced by novel bacterial symbionts (23,24,(32)(33)(34)(35). The extremely reduced Nardonella genome down to 0.2 Mb (Fig.…”

Section: Insights Into Symbiont Replacements and Diversification In Ementioning

confidence: 99%

“…(18)(19)(20), of which weevils comprise the most species-rich group, the superfamily Curculionoidea, with some 70,000 described species in the world (19,21,22). Many, if not all, weevils are associated with an ancient γ-proteobacterial endosymbiont lineage, Nardonella, in the bacteriome, whose evolutionary origin is estimated as older than 100 My (23)(24)(25)(26)(27)(28)(29)(30)(31). Despite the longlasting host-symbiont coevolution, Nardonella's biological role has been poorly understood (26).…”

Section: Significancementioning

confidence: 99%

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Small genome symbiont underlies cuticle hardness in beetles

Anbutsu

Moriyama

Nikoh

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

133

157

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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.

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Section: Insights Into Symbiont Replacements and Diversification In Ementioning

confidence: 99%

Section: Significancementioning

confidence: 99%

Small genome symbiont underlies cuticle hardness in beetles

Anbutsu

Moriyama

Nikoh

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

133

157

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“…Furthermore, it matched bacterial sequences found in Listronotus bonariensis Kuschel by 96% (GenBank accession no. ) (White et al., ) and in Steriphus variabilis Broun by 93% (GenBank accession no. ) (White et al., ), and a bacterial sequence classified as Candidatus Nardonella (γ‐proteobacteria) found in Pachyrhynchus infernalis Fairmaire by 92% (GenBank accession no. )…”

Section: Methodsmentioning

confidence: 99%

“…1) (White et al, 2015) and in Steriphus variabilis Broun by 93% (GenBank accession no. KJ522449.1) (White et al, 2015), and a bacterial sequence classified as Candidatus Nardonella (c-proteobacteria) found in Pachyrhynchus infernalis Fairmaire by 92% (GenBank accession no. AP018160.1) (Anbutsu et al, 2017).…”

Section: Identification Of the Unassigned Otu_0mentioning

confidence: 99%

“…For instance, Hirsch et al (2012) revealed that parthenogenetic species tend to harbour a less diverse bacterial community in comparison with sexual species in the weevil genus Otiorhynchus. White et al (2015) studied the bacterial community associated with exotic and endemic weevils in New Zealand and speculated that the presence of Wolbachia and Rickettsia could be involved in weevil resistance to parasitoids used in biological control. The influence of insect diet on shaping the bacterial microbiota composition was reported in the red palm weevil, Rhynchophorus ferrugineus Olivier, the cotton boll weevil.…”

Section: Introductionmentioning

confidence: 99%

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The bacterial community associated with adult vine weevil (Otiorhynchus sulcatus) in UK populations growing on strawberry is dominated by Candidatus Nardonella

Morera‐Margarit

Bulgarelli

Pope

et al. 2019

Entomologia Exp Applicata

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Otiorhynchus sulcatus (Fabricius) (Coleoptera: Curculionidae), commonly known as black vine weevil or simply vine weevil, is an important pest of soft fruit and ornamental crops. This species is endemic to temperate areas of Europe but has spread to many other areas over the last century, including North America and Australasia. The ability of vine weevils to adapt to such different environments is difficult to reconcile with the parthenogenetic reproduction strategy, which is likely to underpin a low genetic diversity. It is therefore tempting to hypothesize that weevil adaptation to different environments is mediated, at least partly, by the microbial communities inhabiting these insects. As a first step towards testing this hypothesis we characterized the composition of the bacterial microbiota in weevils from populations feeding on strawberry plants across four geographically separate locations in the UK. We performed 16S rRNA gene Illumina amplicon sequencing, generating 2 882 853 high‐quality reads. Ecological indices, namely Chao1 and Shannon, revealed that the populations used for this study harboured a low diversity and an uneven bacterial microbiota. Furthermore, β‐diversity analysis failed to identify a clear association between microbiota composition and location. Notably, a single operational taxonomic unit phylogenetically related to Candidatus Nardonella accounted for 81% of the total sequencing reads for all tested insects. Our results indicate that vine weevil bacterial microbiota resembles that of other insects as it has low diversity and it is dominated by few taxa. A prediction of this observation is that location per se may not be a determinant of the microbiota inhabiting weevil populations. Rather, other or additional selective pressures, such as the plant species used as a food source, ultimately shape the weevil bacterial microbiota. Our results will serve as a reference framework to investigate other or additional hypotheses aimed at elucidating vine weevil adaptation to its environment.

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