Facultatively intra-bacterial localization of a planthopper endosymbiont as an adaptation to its vertical transmission

Abstract

AbstractTransovarial transmission is the most reliable way of passing on essential nutrient- providing endosymbionts from mothers to offspring. However, not all endosymbiotic microbes follow the complex path through the female host tissues to oocytes on their own. Here we demonstrate an unusual transmission strategy adapted by one of the endosymbionts of the planthopperTrypetimorpha occidentalis(Hemiptera: Tropiduchidae) from Bulgaria. In this species, anAcetobacteraceaeendosymbiont is transmitted transovarially within deep invaginations of cellular membranes of an ancient endosymbiontSulcia- strikingly resembling recently described plant virus transmission. However, in males,Acetobacteraceaecolonizes the same bacteriocytes asSulciabut remains unenveloped. Then, the unusual endobacterial localization ofAcetobacteraceaeobserved in females appears to be a unique adaptation to maternal transmission. Further, symbiont’s genomic features, including encoding essential amino acid biosynthetic pathways and very similar to a recently described psyllid symbiont, suggest a unique combination of ability to horizontally transmit among species and confer nutritional benefits. The close association withAcetobacteraceaesymbiont correlates with the so-far- unreported level of genomic erosion of ancient nutritional symbionts of this planthopper. InSulcia, this is reflected in substantial changes in genomic organization, reported for the first time in the symbiont renown for its genomic stability. InVidania, substantial gene loss resulted in one of the smallest genomes known, at 109 kb. Thus, the symbionts ofT. occidentalisdisplay a combination of unusual adaptations and genomic features that expand our understanding of how insect-microbe symbioses may transmit and evolve.Significance StatementReliable transmission across host generations is a major challenge for bacteria that associate with insects, and independently established symbionts have addressed this challenge in different ways. The facultatively endobacterial association ofAcetobacteraceaesymbiont, enveloped by cells of ancient nutritional endosymbiontSulciain females but not males of the planthopperTrypetimorpha occidentalis, appears to be a unique adaptation to maternal transmission. Acetobacteraceae’s genomic features indicate its unusual evolutionary history, and the genomic erosion experienced by ancient nutritional symbionts demonstrates apparent consequences of such close association. Combined, this multi-partite symbiosis expands our understanding of the diversity of strategies that insect symbioses form and some of their evolutionary consequences.