Symbiotic Microorganisms Associated with Pentatomoidea 645
perfectly mirrors the aphid phylogeny, indicating the ancient origin of the symbiosis and the strict verti-
cal transmission during evolution. Such long-term associations have resulted in greater host–symbiont
dependency: the symbiont cannot survive outside the host cells (i.e., in an uncultivable state), whereas
the host aphid suffers from retarded growth, high mortality, and sterility if the symbiont is eliminated
by antibiotic treatments.
Such highly developed (or highly interdependent) host–symbiont associations also have been identified
in diverse insect groups such as Wigglesworthia symbionts in tsetse flies (Aksoy 2000), Baumannia sym-
bionts in sharpshooters (Moran et al. 2005, Wu et al. 2006), Carsonella symbionts in psyllids (Thao et al.
2000), Tre m bl a ya symbionts in mealybugs (Thao et al. 2002), Blochmannia symbionts in carpenter ants
(Sauer et al. 2000), and Nardonella symbionts in weevils (Lefevre et al. 2004). In addition to such nutri-
tional metabolic roles, recent studies have unveiled more diverse functions of symbiotic microorganisms
in insects. For example, antibiotic-producing actinomycete symbionts that protect the host from pathogenic/
harmful microorganisms have been discovered from leaf-cutting ants (Currie et al. 1999, Currie 2001),
ambrosia beetles (Scott et al. 2008), and beewolves (Kaltenpoth et al. 2005). Staphylinid beetles possess
gammmaproteobacterial symbionts that produce a toxic compound, pederine, that protects the insect
against predators (Kellner 2002). Antlions employ a heat-shock protein produced by symbiotic bacteria
as a venom for predation (Yoshida et al. 2001).
14.1.3 Microbial Symbiosis in Pentatomorphan Insects
14.1.3.1 Overview
The heteropteran group is divided into seven infraorders including Enicocephalomorpha, Dipsocoromorpha,
Gerromorpha, Nepomorpha, Leptopodomorpha, Cimicomorpha, and Pentatomomorpha (Schuh and Slater
1995, Weirauch and Schuh 2011). Of these, symbiotic bacteria have been reported from the Cimicomorpha
and Pentatomomorpha (Glasgow 1914, Buchner 1965, Dasch et al. 1984). In the Cimicomorpha, blood-
sucking species representing the families Reduviidae (assassin bugs) and Cimicidae (bed bugs) harbor sym-
biotic bacteria in their gut cavity and in bacteriocytes, respectively (Glasgow 1914, Buchner 1965, Usinger
1966, Dasch et al. 1984, Hosokawa et al. 2010b). Almost all pentatomomorphans, except for the predatory
Asopinae and the mycophagous Aladoidae, are phytophagous, most of which possess symbiotic bacteria.
Although sap-feeding hemipterans usually possess intracellular symbiosis and well-developed bac-
teriomes (Baumann 2005, Moran 2007), pentatomomorphan species harbor symbiotic bacteria in their
gut extracellularly. The insect gut generally is divided into three regions, namely the foregut, midgut
(mesenteron, ventriculus), and hindgut. The foregut and hindgut are lined with cuticle, which serves as
a barrier for most digestion and absorption. The midgut, however, lacks cuticle, and, therefore, most of
these two processes take place in this portion of the gut. In many insects, the midgut is simply organized
and consists of only two or three different sections (Lehane and Billingsley 1996). On the other hand,
the midgut of pentatomomorphan species often is divided anatomically into four distinct sections: (1) the
voluminous first section (M1), (2) the tubular second section (M2), (3) the ovoid third section (M3),
and (4) the fourth section (M4) with numerous sacs or tubular-outgrowths, called as crypts, which are
densely populated by specific bacterial symbionts (Figure 14.1A–H). The M4 crypts commonly are
developed in phytophagous species of the superfamilies Pentatomoidea, Coreoidea, and Lygaeoidea. The
biological roles of the four sections are not known exactly, although it has been suggested that the M1
serves for transient food storage and digestion, the M2 and the M3 perform food digestion and absorp-
tion, and the M4 is specialized for harboring the symbiotic bacteria.
Although the association of microbes with the midgut crypts of Pentatomidae has been known since
the late 1800s, these microbes remained unidentified. The first comprehensive work on their identification
was authored by Glasgow (1914), who revealed that, although bacteria from the midgut crypts of differ-
ent hosts were morphologically different, their morphology remained constant for each species, and they
always were present in a monoculture. Rosenkranz (1939) suggested that these bacteria played significant
roles in relation to insect nutrition. Furthermore, he discussed the possibility that mother stink bugs
covered their eggs with bacteria that were acquired orally by nymphs soon after hatching. Thereafter,
classic histological observations and recent molecular works have unveiled many other different types