Localization and transmission route of Coriobacterium glomerans, the endosymbiont of pyrrhocorid bugs

Abstract

Endosymbiotic gut bacteria play an essential role in the nutrition of many insects. Most of the nutritional interactions investigated so far involve gammaproteobacterial symbionts, whereas other groups have received comparatively little attention. Here, we report on the localization and the transmission route of the specific actinobacterial symbiont Coriobacterium glomerans from the gut of the red firebug, Pyrrhocoris apterus (Hemiptera: Pyrrhocoridae). The symbionts were detected by diagnostic PCRs and FISH in the midgut section M3, in the rectum and in feces of the bugs as well as in the hemolymph of some females. Furthermore, adult female bugs apply the symbionts to the surface of the eggs during oviposition, from where they are later taken up by the hatchlings. Surface sterilization of egg clutches generated aposymbiotic insects and thereby confirmed the vertical transmission route via the egg surface. However, symbionts were readily acquired horizontally when the nymphs were reared in the presence of symbiont-containing eggshells, feces, or adult bugs. Using diagnostic PCRs and partial sequencing of the 16S rRNA gene, closely related bacterial symbionts were detected in the cotton stainer bug Dysdercus fasciatus (Hemiptera: Pyrrhocoridae), suggesting that the symbiosis with Actinobacteria may be widespread among pyrrhocorid bugs.

An out-of-body experience: the extracellular dimension for the transmission of mutualistic bacteria in insects

“…For example, firebugs (Pyrrhocoridae) deposit excretion droplets that are later taken up from the egg surface by young nymphs, ensuring successful transfer of the two co-occurring actinobacterial symbionts Coriobacterium glomerans and Gordonibacter sp. [14] (figure 2c-e). Similarly, in shield bugs of the family Acanthosomatidae, a g-proteobacterial symbiont is harboured in cavities that are sealed off from the midgut main tract, as well as in a pair of lubricating organs associated with the female ovipositor [39].…”

“…Owing to the high selective pressures of endowing beneficial symbionts efficiently to offspring, the majority of specific mutualistic insect-bacteria interactions appear to transition to vertical or mixed-mode transmission routes over the course of evolution. Extracellular nutritional symbionts are usually localized within the gut, and significant numbers of cells are often shed and excreted along with faecal matter [14,24]. Thus, transmission via faeces (i.e.…”

“…Horizontal transmission of Rickettsia among whiteflies (Bemisia tabaci) (a) involves the use of the insect's host plant [13] (b). Transmission of beneficial gut symbionts in the European firebug (c) relies on secretions that are smeared over the egg surface following oviposition (d,e) [14]. Beewolves (f ) cultivate the defensive symbiont 'Candidatus Streptomyces philanthi' in specialized antennal gland reservoirs (g,h) and transmit it via the brood cell [15].…”

Symbiont transmission entails the risk of parasite infection

“…Upon drying, the faeces were fixed with 70% and 99% ethanol in succession. Cor653 [7] and SSUR2 (5 0 -GAGTCAACACTGCTGGGTGT-3 0 ) probes were used to localize C. glomerans and L. pyrrhocoris, respectively. The SSUR2 probe was designed using the 18S rRNA sequence of L. pyrrhocoris (GenBank accession no.…”

“…The two Coriobacteriaceae symbionts Coriobacterium glomerans and Gordonibacter sp. are vertically transmitted across host generations through the faecal smearing of egg surfaces by females during oviposition, but can also be horizontally acquired through contact with conspecifics [7]. Experimental sterilization of egg surfaces disrupts the transmission cycle of the Coriobacteriaceae symbionts, resulting in aposymbiotic (symbiont-free) firebugs that suffer retarded growth, high mortality and low fecundity [8], which is owing to the deficiency in B vitamins that are provided by the symbionts [9].…”