Symbiotic Microorganisms Associated with Pentatomoidea 661
14.2.4 Symbiotic Associations in Allied Pentatomids
Prado and Almeida (2009a) showed that not only Nezara viridula but also other pentatomid species,
such as Chinavia hilaris, Murgantia histrionica, Euschistus heros ( F.), Chlorochroa ligata (Say), C. sayi
(Stål), C. uhleri (Stål), Plautia stali Scott, and Thyanta pallidovirens (Stål), carried symbiotic bacteria in
their midgut crypts. Phylogenetic placement estimated by using 16S rRNA gene sequences demonstrated
that all of the crypt-associated symbionts form a clade with plant-associated Erwinia and Pantoea spe-
cies. Recently, it has been observed that other pentatomid stink bugs, including Dichelops melacanthus
Dallas, Edessa meditabunda F., Loxa deducta Wa l ker, Pellaea stictica Dallas, Piezodorus guildinii
( Westwood), Thyanta perditor ( F.), Eurydema rugosa, Eurydema dominulus, and Halyomorpha halys,
house symbionts associated with their midgut crypts (Table 14.1) (Kikuchi et al. 2012, Prado and Zucchi
2012, Kenyon et al. 2015). However, all the symbionts’ gene sequences differed from each other, sug-
gesting that most of the stink bug symbionts occasionally are replaced by other taxonomically similar
bacteria over the evolutionary period, probably due to their postnatal symbiont transmission mechanism
(Prado et al. 2010, Prado and Zucchi 2012, Hosokawa et al. 2016).
14.3 From Eastern Hemisphere to Western Hemisphere:
Candidatus Ishikawaella Capsulata and Its Plataspid Host14.3.1 Overview
Extensive genetic, phylogenetic, and genomic research has helped clarify bacteriocyte symbiosis or the
mutually obligate symbiosis between unculturable endocellular Gammaproteobacteria and their hemip-
teran hosts (Wernegreen 2002, Gil et al. 2004, Baumann 2005, Moran et al. 2008). Hemipterans are the
only insect group to feed throughout their life cycles on nutriently depauperate phloem sap (Douglas
1998, Spaulding and von Dohlen 1998, Baumann 2005). These bacterial endosymbionts, which are ver-
tically transmitted across generations, have severely reduced genomes lacking in replicative genetics
(Wernegreen 2002, Baumann 2005, Moran et al. 2008) that are function specific. They supply dietary
needs, particularly essential amino acids, necessary for host survival and reproduction (Buchner 1965,
Douglas 1998, Sasaki and Ishikawa 1998, Charles and Ishikawa 1999, Shigenobu et al. 2000, Douglas
2003) and have co-evolved with their host over millions of years (Moran et al. 1993; Baumann 2005;
Moran et al. 2008; Bennett and Moran 2013, 2015). Undeterred by food source, these bacteriocyte sym-
bioses often involve invasive pests expanding ranges across myriad environmental niches (Moran 2007,
Pérez-Brocal et al. 2011, Bennett and Moran 2013). But what of vertically transmitted extracellular
microorganisms found in the gut of phloem-feeding Heteroptera in the family Pentatomidae living in
mutually obligate relationships with their hosts? Are their genomes reduced and, if so, for what purpose?
Does the heritable symbiosis foster range expansion into diversified herbivorous ecologies? Does the
obligate symbiont confer pest status on the host?
We have explored these questions by examining the obligate symbiosis between the gut micro-
organism, “Candidatus Ishikawaella capsulata” (Hosokawa et al. 2006), and its plataspid Megacopta
host. Although discovered for the first time in the Western Hemisphere in 2009 (Eger et al. 2010, Jenkins
et al. 2010, Suiter et al. 2010), the obligate symbiosis had been genetically and behaviorally studied in
Japan since 2002 (Fukatsu and Hosokawa 2002; Hosokawa et al. 2005, 2006, 2007a, 2007b, 2008; Nikoh
et al. 2011).
A seminal study by Fukatsu and Hosokawa (2002) showed that the obligate extracellular gamma-
proteobacteria, “Candidatus Ishikawaella capsulata” (i.e., Ishikawaella) (Hosokawa et al. 2006), is associ-
ated with the plataspid Megacopta punctatissima, a pest species of legumes in Japan (Hosokawa et al.
2007b). As with the well-studied intracellular Gammaproteobacteria, Ishikawaella was shown to have an
acutely reduced genome, accelerated protein evolution, and AT-biased codons and to have co-speciated
with its Megacopta host (Hosokawa et al. 2006, Nikoh et al. 2011). These studies provided an extensive
genetic baseline of an orally transmitted microorganism (Fukatsu and Hosokawa 2002) indigenous to the
Eastern Hemisphere that would soon become a problem in the Western Hemisphere. In October 2009,