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). While 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 megabases 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.

A complex interplay of evolutionary forces continues to shape ancient co-occurring symbiont genomes

“…In contrast, the biological roles of insect symbionts are arguably less integrated into system-wide biological functions of their host insects. Nutritional symbionts are sequestered to distinct organs in the host, retaining relatively enriched genetic autonomy, distinct population sizes, and distinct cellular replication and repair capabilities ( Buchner, 1965 ; Mira and Moran, 2002 ; Koga et al., 2012 ; Bennett et al., 2014 ; Chong and Moran, 2016 ; Mao and Bennett, 2020 ; Stever et al., 2021 ). As a result, they likely do not experience the same patterns and processes of molecular evolution as their partner symbionts, mitochondria, or host nuclear genes.…”

Differential gene expression in the insect vector Anasa tristis in response to symbiont colonization but not infection with a vectored phytopathogen

“…Though our study lacks the power to examine these differences in depth, we did find downregulation of genes related to bacterial motility in crypt symbionts relative to those in culture, as well as upregulation of genes necessary for the production of essential amino acids that are lacking in the insect plant sap diet (Douglas, 2016;Michalik et al, 2023). Nutritional symbioses are common in herbivorous insects (Gündüz and Douglas, 2008;Shan et al, 2021;Stever et al, 2021), often providing otherwise limiting nutrients that enable host development. Though preliminary, these findings provide a first insight into the specific role of Caballeronia symbionts in A. tristis' development.…”

Symbioses shape feeding niches and diversification across insects

“…For example, certain ant and beetle lineages have evolved tyrosine-supplementing symbioses that are thought to help thicken their heavily sclerotized cuticles 47 , 53 , 58 . Specialized herbivores have evolved symbioses to solve a variety of problems, from including the production of digestive enzymes to breakdown of plant cell walls 23 and the synthesis of specific amino acids missing from plant-based diets 35 . Similarly, transitions to feeding on plant phloem and xylem are well known to be associated with essential amino acid provisioning by bacteria in insects 2 , 24 , 52 .…”

“…These feeding niches are, however, also deficient in B vitamins, a common feature of symbiont-associated diets, including those rich in amino acids, such as blood feeding. The widespread need for B-vitamin supplementation is also reflected in the genomes of symbionts that retain metabolic pathways to synthesize B vitamins across a diversity of host feeding niches 32 – 35 . Further insights into the consistent need for B-vitamin supplementation may be gained by extending such genomic analyses to compare the synthesis pathways of B vitamins with those of other nutrients, such as amino acids, in both symbionts and their insect hosts.…”

“…Dietary studies have also confirmed that mutualistic Wolbachia provide essential B vitamins for Cimex bed bugs 30 ; and metabolic homeostasis is restored in symbiont-free Dysdercus cotton stainers when B vitamins are supplemented, or hosts are re-infected with their actinobacterial symbionts 31 . In addition, genome studies have shown that the metabolic pathways to biosynthesize B vitamins have been retained in the genomes of symbionts from insects that occupy diverse feeding niches (for example, blood 32 , plant sap 33 , 34 and seeds 35 ), suggesting their widespread importance in maintaining symbioses. A useful future step would be to assess whether B-vitamin pathways are more highly conserved in symbiont genomes, compared with pathways that encode other host-beneficial factors.…”