The Crypt-Dwelling Primary Bacterial Symbiont of the Polyphagous Pentatomid PestHalyomorpha halys(Hemiptera: Pentatomidae)

Abstract

A recent invader of North America, the brown marmorated stink bug (Halyomorpha halys Stål) is a polyphagous pentatomid that harbors a gammaproteobacterial mutualist in the crypts of specialized midgut gastric caeca (region V4). Histological analyses revealed a single rod-shaped morphology abundant in distal V4 midgut caecal crypts. A strong fluorescence signal was detected when thin sections of these tissues were hybridized with a fluorescently-labeled, Enterobacteriaceae-specific oligonucleotide probe. A single operational taxonomic unit (OTU) assigned to the Pantoea genus represented >99% of 3,454 16S rDNA amplicons obtained from midgut V4 tissues and egg samples. Detection of H. halys primary symbiont in DNA extracted from eggs suggested vertical maternal inheritance as the mode of intergenerational transmission. Consistent detection of the bacterial symbiont in geographically distinct H. halys populations strongly supports an intimate association between these two organisms. An inferred phylogeny of gammaproteobacterial symbionts of pentatomids placed the Pantoea-assigned OTU from H. halys within a clade distinct from primary bacterial symbionts of related stink bugs, Nezara viridula (L.) and Eurydema rugosa Motschulsky. Given these data, Candidatus "Pantoea carbekii" is proposed as the name of the primary bacterial symbiont of H. halys.

Transcriptome of the Invasive Brown Marmorated Stink Bug, Halyomorpha halys (Stål) (Heteroptera: Pentatomidae)

“…The phosphopantothenoylcysteine decarboxylase/phosphopantothenate-cysteine ligase, which functions in coenzyme A biosynthesis, was preferentially highly expressed in H. halys eggs and appears to have originated from gammaproteobacteria. The high levels of expression in eggs with substantial expression in adult females suggest this could be associated with symbionts vertically transmitted to eggs by adult females [13], [14].…”

“…This was not surprising based on recent evidence highlighting the importance of gut symbionts in the overall survival and success of H. halys in the field [13]: Surface sterilization of eggs to remove vertically transmitted gut colonizing bacteria (primarily Pantoea agglomerans ) resulted in smaller clutches in the first generation and dramatically reduced survivorship in the second generation. Bansal et al [14] recently examined the gammaproteobacterial endosymbiont harbored in midgut gastric caeca and identified Candidatus “Pantoea carbekii”, a close relative of P. agglomerans , as the primary bacterial symbiont of H. halys based on 16S rRNA sequences. In the present H. halys transcriptome data, more than 50 PUTs similar to hypothetical proteins from various Pantoea species were identified and were more abundantly expressed in adults versus nymphs (nymphs: 2 nd and 4 th instars combined).…”

Female-Specific Specialization of a Posterior End Region of the Midgut Symbiotic Organ in Plautia splendens and Allied Stinkbugs

“…4). Such obligate symbiotic bacteria associated with the midgut symbiotic organs have been described from a variety of stinkbugs of the families Pentatomidae (15,17,18,20,21,34,44), Scutelleridae (16,45,46), Cydnidae (19), Plataspidae (24,25,47,48), Acanthosomatidae (14), Parastrachiidae (22), Urostylididae (26), and others. As are the cases of the gut symbiotic bacteria associated with the stinkbugs representing the superfamily Pentatomoidea (21,49,50), the gut symbiont of P. splendens was placed within the Enterobacteriaceae of the Gammaproteobacteria, in contrast to the betaproteobacterial gut symbionts widely found across the superfamilies Lygaeoidea and Coreoidea (5).…”

“…In acanthosomatid stinkbugs, novel paired organs for symbiont transmission, which are similar to but anatomically distinct from those of urostylidid stinkbugs, are present near the female genital chamber (14). On the other hand, such femalespecific traits for vertical symbiont transmission have been poorly described for stinkbugs of the family Pentatomidae, except for a few early morphological observations (1,30,31), although members of the largest stinkbug group, embracing over 900 genera and 4,500 species and economically the most important (32,33), are generally associated with midgut symbiotic bacteria that are vertically transmitted via egg surface contamination (1,12,12,13,15,17,18,20,34).…”

Current status of research progress on the biology and management of Halyomorpha halys (Hemiptera: Pentatomidae) as an invasive species

“…This negative effect was significant in the first generation and manifests dramatically in the subsequent generation (Taylor et al 2014). H. halys harbors a gammaproteobacterial mutualist in the crypts of specialized midgut gastric caeca (region V4) and consistent detection of the bacterial symbiont supports an intimate association between these two organisms (Bansal et al 2014).…”