4.6 Article

Characterization of a novelPantoeasymbiont allows inference of a pattern of convergent genome reduction in bacteria associated with Pentatomidae

Journal

ENVIRONMENTAL MICROBIOLOGY
Volume 23, Issue 1, Pages -

Publisher

WILEY
DOI: 10.1111/1462-2920.15169

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Funding

  1. Italian Ministry of Education, University and Research (MIUR): Dipartimenti di Eccellenza Program (2018-2022) - Dept. of Biology and Biotechnology 'L. Spallanzani', University of Pavia

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Phytophagous stink bugs carry nutritional symbiotic bacteria in their midgut to balance their diet, with most symbionts in the Pentatomidae affiliated to the genus Pantoea. A novel Pantoea species ('Candidatus Pantoea persica') was discovered in the gut of the pentatomid Acrosternum arabicum, which is important for host development. Comparative analyses showed a convergent pattern of genome reduction in symbionts of pentatomids, following typical models of obligate nutritional symbionts in insects.
Phytophagous stink bugs typically harbor nutritional symbiotic bacteria in their midgut, to integrate their unbalanced diet. In the Pentatomidae, most symbionts are affiliated to the genusPantoea, and are polyphyletic. This suggests a scenario of an ancestral establishment of symbiosis, followed by multiple symbiont replacement events by akin environmental bacteria in different host lineages. In this study, a novelPantoeaspecies ('CandidatusPantoea persica') was characterized from the gut of the pentatomidAcrosternum arabicum, and shown to be highly abundant in a specific portion of the gut and necessary for the host development. The genome of the symbiont (2.9 Mb), while presenting putative host-supportive metabolic pathways, including those for amino acids and vitamin synthesis, showed a high level of pseudogenization, indicating ongoing genome reduction. Comparative analyses with other free-living and symbioticPantoeahighlighted a convergent pattern of genome reduction in symbionts of pentatomids, putatively following the typical phases modelized in obligate nutritional symbionts of insects. Additionally, this system has distinctive traits, as hosts are closely related, and symbionts originated multiple independent times from closely related free-living bacteria, displaying convergent and independent conspicuous genome reduction. Due to such peculiarities, this may become an ideal model to study genome evolutionary processes in insect symbionts.

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