Contrasting genomic trajectories of Bartonellaceae symbionts of planthoppers

Symbioses with microorganisms have shaped the nutritional biology and evolution of many insects. For example, several ant clades have adapted to nutrient-poor diets through symbiosis with a specific clade of bacteria in the family Bartonellaceae (Hyphomicrobiales), notorious for also including virulent vertebrate pathogens. Here we show that Bartonellaceae phylogenetically placed within the clade that has only encompassed ant symbionts to date - Candidatus genus Tokpelaia - have established as symbionts in four different clades of planthoppers (Insecta: Hemiptera: Fulgoromorpha). Genome size and contents indicate different levels of integration of these strains into the planthopper host biology and their diverse roles. Symbionts infecting one of the clades have some of the largest genomes among Bartonellaceae, at ca. 2 Mb, two others are under 700 kb, and the fourth is reduced to barely 158 kb. The planthopper-associated Tokpelaia strains with larger genomes, similarly to ant symbionts, encode multiple amino acid and vitamin biosynthesis genes, complementing the degraded nutritional capabilities of their hosts ancient heritable endosymbionts. Strikingly, the smallest Tokpelaia genome lacks any genes linked to essential amino acid biosynthesis, in contrast to all other known insect-associated bacteria with genomes of comparable size. We identified a single vitamin biosynthesis gene and iron-sulfur cluster assembly genes as its only putative contributions to the host biology. Our results broaden the host spectrum of non-pathogenic Bartonellaceae, indicating that they have contributed to nutrition and symbiotic consortium function in diverse diet-restricted host clades. They also highlight an unexpectedly broad range of evolutionary outcomes for this important bacterial group. SignificanceMany insects rely on bacterial partners to overcome nutrient-poor diets, yet the diversity and evolutionary trajectories and outcomes for these associations remain unclear. Our discovery of Bartonellaceae bacteria in planthoppers improves the understanding of the host range of these broadly relevant bacteria best-known as vertebrate pathogens. The finding that these planthopper symbionts generally have the capacity to produce essential amino acids and vitamins relevant to hosts and likely form long-term symbiotic associations agree with the expectations for sap-sucking hemipteran symbionts. However, the breadth of sizes and functions of the newly assembled genomes substantially expand the known range of states for Bartonellaceae, and their evolutionary trajectories. In particular, the identification of a strain with an ultra-reduced genome of only 158kb with no amino acid biosynthetic functions contrasts with all other known insect-symbiotic bacteria with genomes in a similar size range. This study also indicates how symbionts may enable the degeneration, functional loss, and evolution of other bacteria residing in the same host.