Intercontinental Diversity of <i>Caballeronia</i> Gut Symbionts in the Conifer Pest Bug <i>Leptoglossus occidentalis</i>

Abstract

Many stinkbugs in the superfamily Coreoidea (Hemiptera: Heteroptera) develop crypts in the posterior midgut, harboring Caballeronia (Burkholderia) symbionts. These symbionts form a monophyletic group in Burkholderia sensu lato, called the "stinkbug-associated beneficial and environmental (SBE)" group, recently reclassified as the new genus Caballeronia. SBE symbionts are separated into the subclades SBE-α and SBE-β. Previous studies suggested a regional effect on the symbiont infection pattern; Japanese and American bug species are more likely to be associated with SBE-α, while European bug species are almost exclusively associated with SBE-β. However, since only a few insect species have been investigated, it remains unclear whether region-specific infection is general. We herein investigated Caballeronia gut symbionts in diverse Japanese, European, and North American populations of a cosmopolitan species, the Western conifer seed bug Leptoglossus occidentalis (Coreoidea: Coreidae). A molecular phylogenetic analysis of the 16S rRNA gene demonstrated that SBE-β was the most dominant in all populations. Notably, SBE-α was rarely detected in any region, while a third clade, the "Coreoidea clade" occupied one fourth of the tested populations. Although aposymbiotic bugs showed high mortality, SBEα-and SBE-β-inoculated insects both showed high survival rates; however, a competition assay demonstrated that SBE-β outcompeted SBE-α in the midgut crypts of L. occidentalis. These results strongly suggest that symbiont specificity in the Leptoglossus-Caballeronia symbiotic association is influenced by the host rather than geography, while the geographic distribution of symbionts may be more important in other bugs.

Symbiont coordinates stem cell proliferation, apoptosis, and morphogenesis of gut symbiotic organ in the stinkbug-Caballeronia symbiosis

“…Members of the superfamily Pentatomidae develop midgut crypts in four rows, in which vertically-transmitted gammaproteobacterial symbionts colonize ( Kikuchi et al, 2012 ; Karamipour et al, 2016 ; Oishi et al, 2019 ; Cossolin et al, 2020 ). Members of the superfamily Coreoidae harbor Caballeronia symbionts in midgut crypts organized in two rows ( Ohbayashi et al, 2019b ; Ishigami et al, 2021 ; Ohbayashi et al, 2022 ), as shown in the bean bug. Members of the superfamily Lygaeoidea carry Caballeronia symbionts in elongated tubular-form midgut crypts ( Kikuchi et al, 2011a ; Ishigami et al, 2022 ).…”

Ecological drift during colonization drives within- and between-host heterogeneity in animal symbiont populations

“…Because each crypt is filled with its own population of symbionts, we asked whether these crypts might exhibit heterogeneity in symbiont composition within the host, consistent with previous unquantified observations from related insect-Caballeronia models [27,38]. If crypts indeed contain heterogeneous populations, we would expect crypts to contain mostly RFP-and mostly GFP-expressing symbionts, as opposed to highly similar populations composed of one or both types.…”

Geographical, seasonal, and growth-related dynamics of gut microbiota in a grapevine pest, Apolygus spinolae (Heteroptera: Miridae) Running title: Gut microbiota of a grapevine pest bug

“…In addition to Serratia, members of Caballeronia were also consistently detected in A. spinolae. The genus Caballeronia is well known as the gut symbiont of several stinkbug species [8, 30,45], wherein the symbiont plays important metabolic roles in recycling metabolic wastes and insecticide resistance [46][47][48]. Phylogenetic analysis showed that OTUs from Tsurunuma and Niseko were classi ed as SBE-β, while OTUs detected from Obihiro and Hakodate were classi ed as SBE-α (Fig.…”