Comparative cytology, physiology and transcriptomics of Burkholderia insecticola in symbiosis with the bean bug Riptortus pedestris and in culture

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.

Study on the community structure and function of symbiotic bacteria from different growth and developmental stages of Hypsizygus marmoreus

“…With the advancement of microecological research [5][6][7], many resources have been made available which show the beneficial relationship between microorganisms and mushrooms [8], the environment [9] and human health [10]. This provides excellent references for studying the beneficial microorganisms of edible fungi.…”

Interfaces between microbes and membranes of host epithelial cells in hemipteran midguts

“…In the Alydus midgut cells, a subset of microbes is ensconced within phagosome membranes with no evidence of being digested in the midgut caeca. However, eventual digestion of another subset of microbes that remain free in the midgut lumen may occur as symbionts proliferate and pass anteriorly into the anterior‐most section of M4 that lacks caeca known as M4B (Kim et al, ; Ohbayashi et al, ). The latter two manuscripts provide evidence that although many microbial symbionts remain intact within the M4 caeca, some symbionts are digested in this M4B region and their nutrients absorbed by host cells.…”

“…Symbiotic bacteria of hemipteran midgut epithelia provide nutrients such as amino acids and vitamins for their hosts (Eichler & Schaub, ; Kikuchi et al, ; Prado, Hung, Daugherty, & Almeida, ; Salem et al, ) and recycle metabolic wastes of the host (Ohbayashi et al, ); in the absence of these symbionts, lifespans of hosts are reduced and their development is retarded. A wide range of interactions between hemipteran midgut host cells and their symbionts has been described—both extracellular and intracellular.…”

Study on the community structure and function of symbiotic bacteria at different growth and developmental stages of Hypsizygus marmoreus

“…With the development of microecological research [5][6][7], the application of bene cial microorganisms in plants [8], for the environment [9] and human health [10] is increasing rapidly. This provides excellent references for studying the bene cial microorganisms of edible fungi.…”