A wide diversity ofPantoealineages are engaged in mutualistic symbiosis and cospeciation processes with stinkbugs

Abstract

Pantoea are emerging as widespread bacteria engaged in associations with a variety of hosts, including plants, insects and humans. Recently, mutualistic Pantoea gut symbionts have also been reported in pentatomid stinkbugs. In the present study, we examine the incidence and evolutionary history of these Pantoea symbionts in pentatomid stinkbug populations from 14 species, characterising the processes that shape their diversity. We identify midgut crypts of pentatomid stinkbugs as harboring a remarkable diversity of Pantoea. Present in 10 of the 14 sampled host species, multi-locus typing revealed the presence of 10 novel Panteoa lineages, all highly differentiated from the known Panteoa species. Rearing experiments of two pentatomid stinkbug species confirmed that these novel Panteoa are maternally inherited through egg smearing and engaged in mutualistic interactions with their hosts. Phylogenetic investigations further revealed that the Pantoea evolutionary history in pentatomid stinkbugs was notably complex: it has been shaped not only by horizontal transfers with frequent host turnover but also by strict vertical transmission over long evolutionary periods, resulting in host-symbiont codiversification.

Recurrent evolution of gut symbiotic bacteria in pentatomid stinkbugs

“…These phylogenetic patterns indicate that the gut symbiotic bacteria are polyphyletic in the stinkbug family Pentatomidae, as has been suggested in previous studies [13, 20, 22, 23]. Among diverse pentatomid species, presumably, their gut symbiotic bacteria have evolved in a dynamic manner, repeatedly acquired from environmental bacteria, horizontally transferred from different stinkbug species, and/or replacing pre-existing symbiotic bacteria.…”

“…In the families Plataspidae, Acanthosomatidae and Urostylididae, for example, the symbiont phylogeny mirrors the host phylogeny and the symbiont genomes are drastically reduced to less than 1 Mb, indicating stable host-symbiont co-speciation and degenerative genome evolution based on strict vertical symbiont transmission over evolutionary time [11, 12, 18]. In the families Pentatomidae and Cydnidae, by contrast, the symbiont phylogeny is not concordant with the host phylogeny, and the symbiont genomes exhibit no or moderate size reduction, suggesting relatively younger host–symbiont associations through acquisitions, horizontal transfers, and/or replacements of the symbiotic bacteria [13, 17, 20, 22, 23, 25]. Recent studies have revealed the striking diversity and dynamic evolutionary trajectories of gut symbiotic bacteria in the stinkbug family Pentatomidae: all gut symbiotic bacteria belong to the Enterobacteriaceae of the γ-Proteobacteria [10, 13–15, 20–24, 26–28]; however, the symbiotic bacteria are polyphyletic and their phylogeny does not reflect the phylogeny of their host stinkbugs, suggesting multiple evolutionary origins of the symbiotic bacteria from Pantoea spp.…”

“…Recent studies have revealed the striking diversity and dynamic evolutionary trajectories of gut symbiotic bacteria in the stinkbug family Pentatomidae: all gut symbiotic bacteria belong to the Enterobacteriaceae of the γ-Proteobacteria [10, 13–15, 20–24, 26–28]; however, the symbiotic bacteria are polyphyletic and their phylogeny does not reflect the phylogeny of their host stinkbugs, suggesting multiple evolutionary origins of the symbiotic bacteria from Pantoea spp. and allied γ-proteobacteria [13, 20, 22, 23, 27, 28]; some symbionts are uncultivable whereas others can be cultivated outside the host body [22]. In some cases, multiple obligate symbiotic bacteria may coexist in the same host species, different stinkbug species may share the same symbiont species, and some environmental bacteria can establish stable infection and mutualistic association with these stinkbug species [22].…”

A Transcriptome Survey Spanning Life Stages and Sexes of the Harlequin Bug, Murgantia histrionica

“…microbe was present: only seven PUTs corresponded to genes observed in the Nosema genus, and these were predominantly associated with retrotransposable elements. In contrast, 653 and 67 PUTs exhibited high levels of sequence similarity with known Pantoea and Erwinia genes, respectively, consistent with the notion that these genera likely comprise the primary microbial endosymbionts of M. histrionica , as well as several other pentatomids [57,58]. …”

Microbial Communities of Lycaenid Butterflies Do Not Correlate with Larval Diet

“…On the other hand, Pantoea strains have been isolated from the guts of several animals, including other insects. Although the nature of Pantoea -host associations is largely unknown, recent studies have demonstrated that Pantoea are important mutualistic symbionts in stinkbugs (Duron and Noël, 2016; Hosokawa et al, 2016). The potential for Pantoea to act as pathogenic or mutualistic gut bacteria in Lepidopteran larvae remains unexplored.…”