Complex host/symbiont integration of a multi-partner symbiotic system in the eusocial aphid Ceratovacuna japonica

Shunta Yorimoto; Mitsuru Hattori; Maki Kondo; Shuji Shigenobu

doi:10.1016/j.isci.2022.105478

Complex host/symbiont integration of a multi-partner symbiotic system in the eusocial aphid Ceratovacuna japonica

iScience. 2022 Nov 2;25(12):105478. doi: 10.1016/j.isci.2022.105478. eCollection 2022 Dec 22.

Authors

Shunta Yorimoto^{1

2}, Mitsuru Hattori³, Maki Kondo⁴, Shuji Shigenobu^{1

2}

Affiliations

¹ Laboratory of Evolutionary Genomics, National Institute for Basic Biology, 38 Nishigonaka, Myodaiji, Okazaki, Aichi 444-8585, Japan.
² Department of Basic Biology, School of Life Science, The Graduate University for Advanced Studies, SOKENDAI, 38 Nishigonaka, Myodaiji, Okazaki, Aichi 444-8585, Japan.
³ Graduate School of Fisheries and Environmental Sciences, Nagasaki University, 1-14 Bunkyo-machi, Nagasaki 852-8521, Japan.
⁴ Spectrography and Bioimaging Facility, National Institute for Basic Biology, 38 Nishigonaka, Myodaiji, Okazaki, Aichi 444-8585, Japan.

Abstract

Some hemipteran insects rely on multiple endosymbionts for essential nutrients. However, the evolution of multi-partner symbiotic systems is not well-established. Here, we report a co-obligate symbiosis in the eusocial aphid, Ceratovacuna japonica. 16S rRNA amplicon sequencing unveiled co-infection with a novel Arsenophonus sp. symbiont and Buchnera aphidicola, a common obligate endosymbiont in aphids. Both symbionts were housed within distinct bacteriocytes and were maternally transmitted. The Buchnera and Arsenophonus symbionts had streamlined genomes of 432,286 bp and 853,149 bp, respectively, and exhibited metabolic complementarity in riboflavin and peptidoglycan synthesis pathways. These anatomical and genomic properties were similar to those of independently evolved multi-partner symbiotic systems, such as Buchnera-Serratia in Lachninae and Periphyllus aphids, representing remarkable parallelism. Furthermore, symbiont populations and bacteriome morphology differed between reproductive and soldier castes. Our study provides the first example of co-obligate symbiosis in Hormaphidinae and gives insight into the evolutionary genetics of this complex system.

Keywords: Evolutionary biology; Genetics; Molecular biology.