Evolution of symbiotic organs and endosymbionts in lygaeid stinkbugs
Open Access
- 4 August 2011
- journal article
- research article
- Published by Oxford University Press (OUP) in The ISME Journal
- Vol. 6 (2), 397-409
- https://doi.org/10.1038/ismej.2011.103
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.Keywords
This publication has 57 references indexed in Scilit:
- Characterization of an Obligate Intracellular Bacterium in the Midgut Epithelium of the Bulrush Bug Chilacis typhae (Heteroptera, Lygaeidae, Artheneinae)Applied and Environmental Microbiology, 2011
- Aphid genome expression reveals host–symbiont cooperation in the production of amino acidsProceedings of the National Academy of Sciences of the United States of America, 2011
- An ancient but promiscuous host–symbiont association between Burkholderia gut symbionts and their heteropteran hostsThe ISME Journal, 2010
- Phylogenetic Position and Peculiar Genetic Traits of a Midgut Bacterial Symbiont of the Stinkbug Parastrachia japonensisApplied and Environmental Microbiology, 2010
- Primary Gut Symbiont and Secondary, Sodalis -Allied Symbiont of the Scutellerid Stinkbug Cantao ocellatusApplied and Environmental Microbiology, 2010
- Insect-Microbe Mutualism without Vertical Transmission: a Stinkbug Acquires a Beneficial Gut Symbiont from the Environment Every GenerationApplied and Environmental Microbiology, 2007
- RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed modelsBioinformatics, 2006
- Genome evolution in bacterial endosymbionts of insectsNature Reviews Genetics, 2002
- Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidiaNature Genetics, 2002
- The Complete Genome Sequence of Escherichia coli K-12Science, 1997