Bacteriome-Associated Endosymbiotic Bacteria of Nosodendron Tree Sap Beetles (Coleoptera: Nosodendridae)

Abstract

The family Nosodendridae is a small group of tree sap beetles with only 91 described species representing three genera from the world. In 1930s, bacteria-harboring symbiotic organs, called bacteriomes, were briefly described in a European species Nosodendron fasciculare. Since then, however, no studies have been conducted on the nosodendrid endosymbiosis for decades. Here we investigated the bacteriomes and the endosymbiotic bacteria of Nosodendron coenosum and Nosodendron asiaticum using molecular phylogenetic and histological approaches. In adults and larvae, a pair of slender bacteriomes were found along both sides of the midgut. The bacteriomes consisted of large bacteriocytes at the center and flat sheath cells on the surface. Fluorescence in situ hybridization detected preferential localization of the endosymbiotic bacteria in the cytoplasm of the bacteriocytes. In reproductive adult females, the endosymbiotic bacteria were also detected at the infection zone in the ovarioles and on the surface of growing oocytes, indicating vertical symbiont transmission via ovarial passage. Transmission electron microscopy unveiled bizarre structural features of the bacteriocytes, whose cytoplasm exhibited degenerate cytology with deformed endosymbiont cells. Molecular phylogenetic analysis revealed that the nosodendrid endosymbionts formed a distinct clade in the Bacteroidetes. The nosodendrid endosymbionts were the most closely related to the bacteriome endosymbionts of bostrichid powderpost beetles and also allied to the bacteriome endosymbionts of silvanid grain beetles, uncovering an unexpected endosymbiont relationship across the unrelated beetle families Nosodendridae, Bostrichidae and Silvanidae. Hostsymbiont co-evolution and presumable biological roles of the endosymbiotic bacteria are discussed.

Inhibition of a nutritional endosymbiont by glyphosate abolishes mutualistic benefit on cuticle synthesis in Oryzaephilus surinamensis

“…The genus name Shikimatogenerans refers to its ability to perform the shikimate pathway. Previous studies have shown that there might be other closely related Bacteroidetes bacteria associated with other beetle families 42 , 66 , 67 . Thus, we propose silvanidophilus as species name to indicate that this symbiont is associated with beetles of the family Silvanidae.…”

Nutritional symbionts enhance structural defence against predation and fungal infection in a grain pest beetle

“…This benefit probably extends to many other beetles in which tyrosine-provisioning microbes have been identified, including S. oryzae , P. infernalis and E. postfasciatus ( Vigneron et al, 2014 ; Anbutsu et al, 2017 ; Anbatsu and Fukatsu, 2020 ; Kuriwada et al, 2010 ) as well as many other weevils harbouring intracellular symbionts ( Zhang et al, 2017 preprint). In addition, symbionts localised in bacteriomes have been described for at least five additional beetle families (Brentidae, Bostrichidae, Nosodendridae, Throscidae and Dasytidae), and the close phylogenetic relationships of some Brentidae symbionts with Nardonella ( Zhang et al, 2017 preprint) and of the Bostrichidae and Nosodendridae symbionts with Shikimatogenerans ( Engl et al, 2018 ; Hirota et al, 2020 ) suggest that these symbionts may be functionally similar ( Salem and Kaltenpoth, 2022 ). Hence, symbioses in insects can have multifaceted phenotypic impacts beyond immediate nutritional effects, and studying these more comprehensively will provide us with a better understanding of the implications of symbiotic interactions on the ecology and evolution of insects.…”

Cuticle supplementation and nitrogen recycling by a dual bacterial symbiosis in a family of xylophagous beetles (Coleoptera: Bostrichidae)

“…To our knowledge, the Bostrichidae are thus far unique in containing species that harbor two Bacteroidota endosymbionts, which are closely related but diverged to metabolically complementary symbionts. This finding highlights the versatile nature of symbioses with Bacteroidota bacteria that are emerging as widespread beneficial symbionts across at least four beetle families (Silvanidae: (Engl et al, 2018;Hirota et al, 2017), Coccinellidae: (Hurst et al, 1996;Hurst, Bandi, et al, 1999), Nosodendridae (Hirota et al, 2020), and Bostrichidae: this study and Engl et al 2018) as well as at least two other insect orders (Bandi et al, 1995;Engl et al, 2018;. The repeated independent acquisitions of these specific clades of Bacteroidota symbionts suggest that these bacteria were once specialized in establishing lasting infections in insects, akin to Wolbachia (Kiefer et al, 2022) or Sodalis (McCutcheon et al, 2019).…”

“…The genus name Shikimatogenerans refers to its ability to perform the shikimate pathway. Previous studies have shown that closely related Bacteroidota bacteria are also associated with other beetle families such as the Silvanidae and the Nosodendridae (Engl et al, 2018; Hirota et al, 2020). Thus, we propose bostrichidophilus as a species epithet to indicate that this symbiont clade is associated with beetles of the family Bostrichidae.…”