Phylogenetic Position and Peculiar Genetic Traits of a Midgut Bacterial Symbiont of the Stinkbug Parastrachia japonensis

Abstract

The stinkbug Parastrachia japonensis (Hemiptera: Parastrachiidae) is known for its prolonged prereproductive nonfeeding period, maternal care of eggs in an underground nest, and maternal collection and provisioning of food (fruits) for nymphs. A previous study suggested that a bacterial symbiont is involved in uric acid recycling in this insect during the nonfeeding period, but the identity of this symbiont has not been determined. Here we characterized a novel bacterial symbiont obtained from P. japonensis. Molecular phylogenetic analyses based on 16S rRNA, gyrB, and groEL gene sequences consistently indicated that this symbiont constituted a distinct lineage in the Gammaproteobacteria that has no close relatives but is allied with gut symbionts of acanthosomatid and plataspid stinkbugs, as well as with endocellular symbionts of sharpshooters, tsetse flies, and aphids. The symbiont genes had a remarkably AT-biased nucleotide composition and exhibited significantly accelerated molecular evolution. The symbiont genome was extremely reduced; its size was estimated to be 0.85 Mb. These results suggest that there has been an intimate host-symbiont association over evolutionary time. The symbiont was localized in swollen crypts in a posterior part of the midgut, which was a specialized symbiotic organ. The possibility that the symbiont is involved in uric acid recycling is discussed. The designation "Candidatus Benitsuchiphilus tojoi" is proposed for the symbiont.

Endosymbiotic microorganisms of aphids (Hemiptera: Sternorrhyncha: Aphidoidea): Ultrastructure, distribution and transovarial transmission

“…members of families Pyrrhocoridae, Plataspididae, Acanthosomatidae, Reduviidae, Pentatomidae, Scutelleridae, Coreidae, Cydnidae, Parastrachiidae and several other families of Pentatomomorpha) are as a rule vertically -postanatally transmitted either by the contamination of the eggs with the symbionts, by deposition of a special capsule filled with symbionts onto the eggs or by feeding on the mother's excrements (see e.g. Buchner, 1965;Fukatsu & Hosokawa, 2002;Prado et al, 2006;Kaltenpoth et al, 2009;Kikuchi, 2009;Kaiwa et al, 2010;Hosokawa et al, 2010Hosokawa et al, , 2013 for further details). In contrast, mycetomic bacteria of the other hemipterans (i.e.…”

An ancient but promiscuous host–symbiont association between Burkholderia gut symbionts and their heteropteran hosts

“…Development of crypts in the midgut fourth section was observed in 96 species representing 15 families ( Table 1). Arrangements of the midgut crypts were distinct among the stinkbug taxa, which were classified into at least four morphological types (Table 1; also see Kikuchi et al, 2008): tubular outgrowths in the Blissidae, Berytidae and most species of the Rhyparochromidae (Figure 2b, c, e, f, h and i); small crypts arranged in two rows in the Coreidae, Alydidae, Plataspidae, Parastrachiidae, Cydnidae, Pachygronthidae and several species of the Rhyparochromidae (Figure 2k, l, n, o, q and r; also see Kikuchi et al, 2005;Hosokawa et al, 2010); small crypts arranged in four rows in the Pentatomidae, Scutelleridae, Urostylidae and Dinidoridae (see Abe et al, 1995;Kaiwa et al, 2010); and a pair of large flat assemblage of crypts in the Acanthosomatidae (see Kikuchi et al, 2009). These results were in agreement with early histological observations of stinkbug alimentary tracts (Glasgow, 1914;Miyamoto, 1961;Buchner, 1965).…”

“…In most of the phytophagous species, a number of sac-or tube-like outgrowths (called crypts or caeca) develop in a posterior region of the midgut (so-called midgut fourth section), wherein specific bacteria are harbored (Glasgow, 1914;Miyamoto, 1961;Buchner, 1965;Kikuchi et al, 2008). In the families Pentatomidae, Plataspidae, Acanthosomatidae, Scutelleridae and Parastrachiidae, their gut symbionts belong to distinct lineages in the g-Proteobacteia, indicating multiple evolutionary origins of the symbiotic associations (Fukatsu and Hosokawa, 2002;Hosokawa et al, 2006Hosokawa et al, , 2010Prado et al, 2006;Kikuchi et al, 2009;Prado and Almeida, 2009a, b;Kaiwa et al, 2010). In several species of the families Pentatomidae, Plataspidae, Acanthosomatidae, Parastrachiidae and Cydnidae, symbiont-free insects suffered retarded growth and/or nymphal mortality, suggesting mutualistic nature of the symbiotic associations (Mü ller, 1956;Huber-Schneider, 1957;Schorr, 1957;Abe et al, 1995;Fukatsu and Hosokawa, 2002;Hosokawa et al, 2006;Kashima et al, 2006;Kikuchi et al, 2009;Prado and Almeida, 2009b).…”

Diversity of Symbiotic Organs and Bacterial Endosymbionts of Lygaeoid Bugs of the Families Blissidae and Lygaeidae (Hemiptera: Heteroptera: Lygaeoidea)

“…In plant-sucking stinkbugs of the superfamily Pentatomoidea (Heteroptera: Pentatomomorpha), most species of the families Acanthosomatidae, Cydnidae, Parastrachiidae, Pentatomidae, Plataspidae, and Scutelleridae harbor specific bacterial symbionts, which belong to distinct lineages in the Gammaproteobacteria, extracellularly in separated sections of the posterior midgut called crypts or ceca (8,9,17,18,20,24,29,40,44). Typically, the symbionts harbored in the midgut crypts are transmitted vertically by postnatal transmission mechanisms such as egg smearing.…”