Abstract
In the symbiosis of the bean bug Riptortus pedestris with Burkholderia insecticola, the bacteria occupy an exclusive niche in the insect midgut and favor insect development and reproduction. In order to understand how the symbiotic bacteria stably colonize the midgut crypts and which services they provide to the host, we compared the cytology, physiology, and transcriptomics of free-living and midgut-colonizing B. insecticola. The analyses revealed that midgut-colonizing bacteria were smaller in size and had lower DNA content, they had increased stress sensitivity, lost motility, and an altered cell surface. Transcriptomics revealed what kinds of nutrients are provided by the bean bug to the Burkholderia symbiont. Transporters and metabolic pathways of diverse sugars such as rhamnose and ribose, and sulfur compounds like sulfate and taurine were upregulated in the midgut-colonizing symbionts. Moreover, pathways enabling the assimilation of insect nitrogen wastes, i.e. allantoin and urea, were also upregulated. The data further suggested that the midgut-colonizing symbionts produced all essential amino acids and B vitamins, some of which are scarce in the soybean food of the host insect. Together, these findings suggest that the Burkholderia symbiont is fed with specific nutrients and also recycles host metabolic wastes in the insect gut, and in return, the bacterial symbiont provides the host with essential nutrients limited in the insect food, contributing to the rapid growth and enhanced reproduction of the bean bug host.
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Acknowledgements
Part of this work was performed at the Open Facility of Hokkaido University and the Imagerie-Gif facilities. This work has benefited from the expertise of the High-throughput Sequencing Platform of I2BC and from support by the Labex ‘Saclay Plant Sciences’ (ANR-11-IDEX-0003-02). This work was supported by the MEXT KAKENHI (15H05638 to Y.K.), the JSPS Research Fellowship for Young Scientists (14J03996 and 20170267 to T.O.) and the JSPS Invitation Fellowship for Research in Japan (L-14556 to P.M.).
Author contributions
TO, PM, and YK designed the project. TO, TS, and PM performed the stress tests. MT and QB conducted flow cytometry analyses. XYM and YM performed electron microscopy. TO, RF, SS, TF, FL, KT, and PM conducted RNA-seq and analyzed transcriptome data. TO, PM, and YK wrote the manuscript. All co-authors edited the manuscript before submission.
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Ohbayashi, T., Futahashi, R., Terashima, M. et al. Comparative cytology, physiology and transcriptomics of Burkholderia insecticola in symbiosis with the bean bug Riptortus pedestris and in culture. ISME J 13, 1469–1483 (2019). https://doi.org/10.1038/s41396-019-0361-8
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DOI: https://doi.org/10.1038/s41396-019-0361-8
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