A wide diversity of Pantoea lineages 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.