Differential Genome Evolution Between Companion Symbionts in an Insect-Bacterial Symbiosis

Abstract

Obligate symbioses with bacteria allow insects to feed on otherwise unsuitable diets. Some symbionts have extremely reduced genomes and have lost many genes considered to be essential in other bacteria. To understand how symbiont genome degeneration proceeds, we compared the genomes of symbionts in two leafhopper species, Homalodisca vitripennis (glassy-winged sharpshooter [GWSS]) and Graphocephala atropunctata (blue-green sharpshooter [BGSS]) (Hemiptera: Cicadellidae). Each host species is associated with the anciently acquired “Candidatus Sulcia muelleri” (Bacteroidetes) and the more recently acquired “Candidatus Baumannia cicadellinicola” (Gammaproteobacteria). BGSS “Ca. Baumannia” retains 89 genes that are absent from GWSS “Ca. Baumannia”; these underlie central cellular functions, including cell envelope biogenesis, cellular replication, and stress response. In contrast, “Ca. Sulcia” strains differ by only a few genes. Although GWSS “Ca. Baumannia” cells are spherical or pleomorphic (a convergent trait of obligate symbionts), electron microscopy reveals that BGSS “Ca. Baumannia” maintains a rod shape, possibly due to its retention of genes involved in cell envelope biogenesis and integrity. Phylogenomic results suggest that “Ca. Baumannia” is derived from the clade consisting of Sodalis and relatives, a group that has evolved symbiotic associations with numerous insect hosts. Finally, the rates of synonymous and nonsynonymous substitutions are higher in “Ca. Baumannia” than in “Ca. Sulcia,” which may be due to a lower mutation rate in the latter. Taken together, our results suggest that the two “Ca. Baumannia” genomes represent different stages of genome reduction in which many essential functions are being lost and likely compensated by hosts. “Ca. Sulcia” exhibits much greater genome stability and slower sequence evolution, although the mechanisms underlying these differences are poorly understood.

Symbiotic microorganisms of the leafhopper Deltocephalus pulicaris (Fallén, 1806) (Insecta, Hemiptera, Cicadellidae: Deltocephalinae): molecular characterization, ultrastructure and transovarial transmission

“…Results of earlier histological studies (MÜLLER 1962, BUCHNER 1965) and more recent ultrastructural and molecular analyses , 2005, TAKIYA et al 2006, MCCUTCHEON et al 2009, MICHALIK et al 2014a, NODA et al 2012, ISHII et al 2013, KOGA et al 2013, BENNETT et al 2014, KOGA & MORAN 2014 have shown that representatives of Cicadomorpha are characterized by an enormous diversity of their symbionts. MORAN et al (2005) and KOGA et al (2013) suggested that the common ancestor of the Cicadomorpha and Fulgoromorpha acquired the bacterium Sulcia and the betaproteobacterial symbiont over 260 million years ago.…”

Heritable symbiosis: The advantages and perils of an evolutionary rabbit hole

“…With more genome sequencing, it became apparent that Buchnera genomes in different aphid lineages continue to undergo irreversible gene loss, over long and short time scales (52)(53)(54)(55)(56). Similar ongoing gene loss is evident in every obligate symbiont clade for which multiple genomes have been sequenced (16,57,58). Many show far more extreme genome reduction than does Buchnera.…”

Genome expansion via lineage splitting and genome reduction in the cicada endosymbiont Hodgkinia

“…Sulcia has been noted to have a very low DNA substitution rate in various insects, usually with its partner coprimary symbiont showing a more rapid rate of sequence evolution (2,44,45). For example, in sharpshooters, Sulcia has a five-times slower rate of DNA substitution than its partner symbiont Baumannia cicadellinicola (45).…”

“…For example, in sharpshooters, Sulcia has a five-times slower rate of DNA substitution than its partner symbiont Baumannia cicadellinicola (45). Thus, symbiont pairs that are present in the same host can have different rates of sequence evolution, perhaps because of mechanical differences in their DNA replication machinery (44).…”