Novel bacteriocyte-associated pleomorphic symbiont of the grain pest beetle Rhyzopertha dominica (Coleoptera: Bostrichidae)

Genta Okude,Xian-Ying Meng,Yudai Nishide,Takema Fukatsu,Toshinari Hayashi,Akihiro Miyanoshita,Ryuichi Koga,Naruo Nikoh

doi:10.1186/s40851-017-0073-8

Abstract

BackgroundThe lesser grain borer Rhyzopertha dominica (Coleoptera: Bostrichidae) is a stored-product pest beetle. Early histological studies dating back to 1930s have reported that R. dominica and other bostrichid species possess a pair of oval symbiotic organs, called the bacteriomes, in which the cytoplasm is densely populated by pleomorphic symbiotic bacteria of peculiar rosette-like shape. However, the microbiological nature of the symbiont has remained elusive.ResultsHere we investigated the bacterial symbiont of R. dominica using modern molecular, histological, and microscopic techniques. Whole-mount fluorescence in situ hybridization specifically targeting symbiotic bacteria consistently detected paired bacteriomes, in which the cytoplasm was full of pleomorphic bacterial cells, in the abdomen of adults, pupae and larvae, confirming previous histological descriptions. Molecular phylogenetic analysis identified the symbiont as a member of the Bacteroidetes, in which the symbiont constituted a distinct bacterial lineage allied to a variety of insect-associated endosymbiont clades, including Uzinura of diaspidid scales, Walczuchella of giant scales, Brownia of root mealybugs, Sulcia of diverse hemipterans, and Blattabacterium of roaches. The symbiont gene exhibited markedly AT-biased nucleotide composition and significantly accelerated molecular evolution, suggesting degenerative evolution of the symbiont genome. The symbiotic bacteria were detected in oocytes and embryos, confirming continuous host–symbiont association and vertical symbiont transmission in the host life cycle.ConclusionsWe demonstrate that the symbiont of R. dominica constitutes a novel bacterial lineage in the Bacteroidetes. We propose that reductive evolution of the symbiont genome may be relevant to the amorphous morphology of the bacterial cells via disruption of genes involved in cell wall synthesis and cell division. Genomic and functional aspects of the host-symbiont relationship deserve future studies.

Highlights

The lesser grain borer Rhyzopertha dominica (Coleoptera: Bostrichidae) is a stored-product pest beetle
We show in the present study that the symbiont of R. dominica belongs to the Bacteroidetes, which is phylogenetically distant from the γ-Proteobacteria
In this study, we demonstrated that the pleomorphic symbiont of R. dominica, whose microbiological affiliation has been obscure for decades, constitutes a distinct bacterial lineage in the Bacteroidetes

Summary

Introduction

The lesser grain borer Rhyzopertha dominica (Coleoptera: Bostrichidae) is a stored-product pest beetle. Some beetles cause significant damage to stored cereals, beans, seeds, spices, dried fruits, and other durable commodities, and are regarded as stored-product pests [21, 22] Relevant to their peculiar ecological niche, namely continuous living on non-fresh and monotonous food sources under low-humidity conditions, many, if not all, stored-product pest beetles are associated with symbiotic microorganisms (reviewed in [1]). Pioneering early research provided detailed descriptions of well-developed bacteria-containing symbiotic organs in other stored-product pests belonging to such beetle families as the Silvanidae and the Bostrichidae [32,33,34,35,36], but the microbiological aspects of these symbiotic relationships have remained unstudied in the decades since the original descriptions

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