Reduced Genome of the Gut Symbiotic Bacterium "Candidatus Benitsuchiphilus tojoi" Provides Insight Into Its Possible Roles in Ecology and Adaptation of the Host Insect.

Shakhinur Islam Mondal,Arzuba Akter,Taisei Kikuchi,Mehmet Dayi,Ryusei Tanaka,Ryuichi Koga,Takahiro Hosokawa,Shuji Shigenobu,Takema Fukatsu,Kazunori Murase

doi:10.3389/fmicb.2020.00840

Abstract

Diverse animals, including insects, harbor microbial symbionts within their gut, body cavity, or cells. The subsocial parastrachiid stinkbug Parastrachia japonensis is well-known for its peculiar ecological and behavioral traits, including its prolonged non-feeding diapause period and maternal care of eggs/nymphs in an underground nest. P. japonensis harbors a specific bacterial symbiont within the gut cavity extracellularly, which is vertically inherited through maternal excretion of symbiont-containing white mucus. Thus far, biological roles of the symbiont in the host lifecycle has been little understood. Here we sequenced the genome of the uncultivable gut symbiont “Candidatus Benitsuchiphilus tojoi.” The symbiont has an 804 kb circular chromosome encoding 606 proteins and a 14.5 kb plasmid encoding 13 proteins. Phylogenetic analysis indicated that the bacterium is closely related to other obligate insect symbionts belonging to the Gammaproteobacteria, including Buchnera of aphids and Blochmannia of ants, and the most closely related to Ishikawaella, an extracellular gut symbiont of plataspid stinkbugs. These data suggested that the symbiont genome has evolved like highly reduced gamma-proteobacterial symbiont genomes reported from a variety of insects. The presence of genes involved in biosynthesis pathways for amino acids, vitamins, and cofactors in the genome implicated the symbiont as a nutritional mutualist, supplementing essential nutrients to the host. Interestingly, the symbiont’s plasmid encoded genes for thiamine and carotenoid synthesis pathways, suggesting the possibility of additional functions of the symbiont for protecting the host against oxidative stress and DNA damage. Finally, possible involvement of the symbiont in uric acid metabolism during diapause is discussed.

Highlights

Many insects harbor symbiotic bacteria within their gut, body cavity, or cells (Buchner, 1965; Bourtzis and Miller, 2003; Engel and Moran, 2013)
These results indicated the isolated DNA contained the host insect DNA, whose sequences were scarcely available in the public database, and a small amount of Wolbachia-like bacterial DNA, in addition to the DNA of Benitsuchiphilus
To speculate the origin of the prophage-like regions, we have performed BLAST search of the eight phage-related genes and found that they are most similar to genes identified in Pantoea and Erwinia species (Supplementary Table S2), which were placed at the basal position of Benitsuchiphilus-containing cluster in the phylogenetic analysis (Figure 2, please see below), suggesting phage-related genes in Benitsuchiphilus have evolved from the same common ancestor of these bacterial species of the Erwiniaceae family

Summary

Introduction

Many insects harbor symbiotic bacteria within their gut, body cavity, or cells (Buchner, 1965; Bourtzis and Miller, 2003; Engel and Moran, 2013). These symbiotic associations form a dynamic spectrum with regards to the necessity as well as the effects of the symbiont on the host (Baumann, 2005). As a rule, symbionts are vertically transmitted to the where the symbiont transmission is integrated into the intricate development of the host insect (Braendle et al, 2003) Both the host and symbiont depend on each other for their development and reproduction (Wernegreen, 2002). By contrast, survival of the host insects is not dependent of their bacterial symbionts (Oliver et al, 2010), which exhibit the aforementioned genomic characteristics to a much lesser extent (Wu et al, 2004; Degnan et al, 2009; Klasson et al, 2009; Burke and Moran, 2011)

Methods

Results

Conclusion