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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.

SUBMITTER: Stever H

PROVIDER: S-EPMC8412300 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Plants are a difficult food resource to use, and herbivorous insects have evolved a variety of mechanisms that allow them to fully exploit this poor nutritional resource. One such mechanism is the maintenance of bacterial symbionts that aid in host plant feeding and development. The majority of these intracellular symbionts have highly eroded genomes that lack many key regulatory genes; consequently, it is unclear if these symbionts can respond to changes in the insect's diet to facilitate host plant use. There is emerging evidence that symbionts with highly eroded genomes express small RNAs (sRNAs), some of which potentially regulate gene expression. In this study, we sought to determine if the reduced genome of the nutritional symbiont (Buchnera) in the pea aphid responds to changes in the aphid's host plant diet. Using transcriptome sequencing (RNA-seq), Buchnera sRNA expression profiles were characterized within two Buchnera life stages when pea aphids fed on either alfalfa or fava bean. Overall, this study demonstrates that Buchnera sRNA expression changes not only with life stage but also with changes in aphid host plant diet. Of the 321 sRNAs characterized in this study, 47% were previously identified and 22% showed evidence of conservation in two or more Buchnera taxa. Functionally, 13 differentially expressed sRNAs were predicted to target genes related to pathways involved in essential amino acid biosynthesis. Overall, results from this study reveal that host plant diet influences the expression of conserved and lineage-specific sRNAs in Buchnera and that these sRNAs display distinct host plant-specific expression profiles among biological replicates.IMPORTANCE In general, the genomes of intracellular bacterial symbionts are reduced compared to those of free-living relatives and lack many key regulatory genes. Many of these reduced genomes belong to obligate mutualists of insects that feed on a diet that is deficient in essential nutrients, such as essential amino acids. It is unclear if these symbionts respond with their host to changes in insect diet, because of their reduced regulatory capacity. Emerging evidence suggests that these symbionts express small RNAs (sRNAs) that regulate gene expression at the posttranscriptional level. Therefore, in this study, we sought to determine if the reduced genome of the nutritional symbiont Buchnera in the pea aphid responds to changes in the aphid's host plant diet. This study demonstrates for the first time that Buchnera sRNAs, some conserved in two or more Buchnera lineages, are differentially expressed when aphids feed on different plant species and potentially target genes within essential amino acid biosynthesis pathways.

Project description:Background: The best studied insect-symbiont system is that of aphids and their primary bacterial endosymbiont Buchnera aphidicola. Buchnera inhabits specialized host cells called bacteriocytes, provides nutrients to the aphid and has co-speciated with its aphid hosts for the past 150 million years. We have used a single microarray to examine gene expression in the pea aphid, Acyrthosiphon pisum, and its resident Buchnera. Very little is known of gene expression in aphids, few studies have examined gene expression in Buchnera, and no study has examined simultaneously the expression profiles of a host and its symbiont. Expression profiling of aphids, in studies such as this, will be critical for assigning newly discovered A. pisum genes to functional roles. In particular, because aphids possess many genes that are absent from Drosophila and other holometabolous insect taxa, aphid genome annotation efforts cannot rely entirely on homology to the best-studied insect systems. Development of this dual-genome array represents a first attempt to characterize gene expression in this emerging model system. Results: We chose to examine heat shock response because it has been well characterized both in Buchnera and in other insect species. Our results from the Buchnera of A. pisum show responses for the same gene set as an earlier study of heat shock response in Buchnera for the host aphid Schizaphis graminum. Additionally, analyses of aphid transcripts showed the expected response for homologs of known heat shock genes as well as responses for several genes with unknown functional roles. Conclusions: We examined gene expression under heat shock of an insect and its bacterial symbiont in a single assay using a dual-genome microarray. Further, our results indicate that microarrays are a useful tool for inferring functional roles of genes in A. pisum and other insects and suggest that the pea aphid genome may contain many gene paralogs that are differentially regulated. Keywords: Stress response

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

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