Evolution of symbiotic organs and endosymbionts in lygaeid stinkbugs

Yu Matsuura, Yoshitomo Kikuchi, Takahiro Hosokawa, Ryuichi Koga, Xian Ying Meng, Yoichi Kamagata, Naruo Nikoh, Takema Fukatsu

Research output: Contribution to journalArticle

40 Citations (Scopus)

Abstract

We investigated seed bugs of the genus Nysius (Insecta: Hemiptera: Lygaeidae) for their symbiotic bacteria. From all the samples representing 4 species, 18 populations and 281 individuals, specific bacterial 16S rRNA gene sequences were consistently identified, which formed a distinct clade in the Gammaproteobacteria. In situ hybridization showed that the bacterium was endocellularly localized in a pair of large bacteriomes that were amorphous in shape, deep red in color, and in association with gonads. In the ovary of adult females, the endosymbiont was also localized in the 'infection zone' in the middle of each germarium and in the 'symbiont ball' at the anterior pole of each oocyte, indicating vertical transmission of the endosymbiont through the ovarial passage. Phylogenetic analyses based on bacterial 16S rRNA, groEL and gyrB genes consistently supported a coherent monophyly of the Nysius endosymbionts. The possibility of a sister relationship to 'Candidatus Kleidoceria schneideri', the bacteriome-associated endosymbiont of a lygaeid bug Kleidocerys resedae, was statistically rejected, indicating independent evolutionary origins of the endosymbionts in the Lygaeidae. The endosymbiont genes consistently exhibited AT-biased nucleotide compositions and accelerated rates of molecular evolution, and the endosymbiont genome was only 0.6 Mb in size. The endosymbiont phylogeny was congruent with the host insect phylogeny, suggesting strict vertical transmission and host-symbiont co-speciation over evolutionary time. Based on these results, we discuss the evolution of bacteriomes and endosymbionts in the Heteroptera, most members of which are associated with gut symbiotic bacteria. The designation Candidatus Schneideria nysicola is proposed for the endosymbiont clade.

Original languageEnglish
Pages (from-to)397-409
Number of pages13
JournalISME Journal
Volume6
Issue number2
DOIs
Publication statusPublished - Feb 1 2012

Fingerprint

endosymbiont
endosymbionts
Phylogeny
Bacteria
Insects
Heteroptera
Nysius
Gammaproteobacteria
Lygaeidae
Hemiptera
Molecular Evolution
Gonads
rRNA Genes
Genes
Oocytes
In Situ Hybridization
Ovary
Seeds
vertical transmission
Nucleotides

All Science Journal Classification (ASJC) codes

  • Microbiology
  • Ecology, Evolution, Behavior and Systematics

Cite this

Matsuura, Y., Kikuchi, Y., Hosokawa, T., Koga, R., Meng, X. Y., Kamagata, Y., ... Fukatsu, T. (2012). Evolution of symbiotic organs and endosymbionts in lygaeid stinkbugs. ISME Journal, 6(2), 397-409. https://doi.org/10.1038/ismej.2011.103

Evolution of symbiotic organs and endosymbionts in lygaeid stinkbugs. / Matsuura, Yu; Kikuchi, Yoshitomo; Hosokawa, Takahiro; Koga, Ryuichi; Meng, Xian Ying; Kamagata, Yoichi; Nikoh, Naruo; Fukatsu, Takema.

In: ISME Journal, Vol. 6, No. 2, 01.02.2012, p. 397-409.

Research output: Contribution to journalArticle

Matsuura, Y, Kikuchi, Y, Hosokawa, T, Koga, R, Meng, XY, Kamagata, Y, Nikoh, N & Fukatsu, T 2012, 'Evolution of symbiotic organs and endosymbionts in lygaeid stinkbugs', ISME Journal, vol. 6, no. 2, pp. 397-409. https://doi.org/10.1038/ismej.2011.103
Matsuura Y, Kikuchi Y, Hosokawa T, Koga R, Meng XY, Kamagata Y et al. Evolution of symbiotic organs and endosymbionts in lygaeid stinkbugs. ISME Journal. 2012 Feb 1;6(2):397-409. https://doi.org/10.1038/ismej.2011.103
Matsuura, Yu ; Kikuchi, Yoshitomo ; Hosokawa, Takahiro ; Koga, Ryuichi ; Meng, Xian Ying ; Kamagata, Yoichi ; Nikoh, Naruo ; Fukatsu, Takema. / Evolution of symbiotic organs and endosymbionts in lygaeid stinkbugs. In: ISME Journal. 2012 ; Vol. 6, No. 2. pp. 397-409.
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