Hawaiian Nysius Insects Rely on an Obligate Symbiont with a Reduced Genome That Retains a Discrete Nutritional Profile to Match Their Plant Seed Diet

Abstract

Seed-feeding Nysius insects (Hemiptera: Lygaeidae) have a symbiotic association with distinct intracellular bacteria, "Candidatus Schneideria nysicola" (Gammaproteobacteria). Although many other hemipteran insect groups generally rely on bacterial symbionts that synthesize all ten essential amino acids lacking in their plant sap diets, the nutritional role of Schneideria in Nysius hosts that specialize on a more nutritionally complete seed-based diet has remained unknown. To determine the nutritional and functional capabilities of Schneideria, we sequenced the complete Schneideria genomes from three distantly related endemic Hawaiian Nysius seed bug species. The complete Schneideria genomes are highly conserved and perfectly syntenic among Hawaiian Nysius host species. Each circular chromosome is ∼0.57 Mb in size and encodes 537 protein-coding genes. They further exhibit a strong A + T nucleotide substitution bias with an average G + C nucleotide content of 29%. The predicted nutritional contribution of Schneideria includes four B vitamins and five of the ten essential amino acids that likely match its hosts' seed-based diet. Disrupted and degraded genes in Schneideria suggests that Hawaiian lineages are undergoing continued gene losses observed in the smaller genomes of the other more ancient hemipteran symbionts.

Keywords: Heteroptera; amino acids; genome size; intracellular bacteria; nutrition; symbiosis.

Fig. 1.

Distribution of genes in central cellular processes. Bars represent the number of genes related to protein synthesis and energy, and bacterial replication in Schneideria from the seed bug Nysius blackburni, Sodalis HS (free-living bacteria) (Oakeson et al. 2014), Sodalis BA (obligate symbiont of the seed bug Henestaris halophilus) (Santos-Garcia et al. 2017), and Sulcia ALF and Nasuia ALF (obligate co-symbionts of the Aster Leafhopper Macrosteles quadrilineatus) (Bennett and Moran 2013).

Fig. 2.

Essential amino acid and vitamin contributions of Schneideria. Genes in black font are present, genes in gray font are absent, and dotted lines are pathway links. Nutrients in black font are likely produced by the symbiont. Abbreviations for nutrients are as follows: Pan, pantothenate; Bio, biotin; Fol, folate; Rib, riboflavin; Pyr, pyridoxine; Ile, isoleucine; Val, valine; Leu, leucine; Lys, lysine; Thr, threonine; Met, methionine; Arg, arginine; His, histidine; Trp, tryptophan; Phe, phenylalanine.