Genome-Wide Transcriptional Dynamics in the Companion Bacterial Symbionts of the Glassy-Winged Sharpshooter (Cicadellidae: Homalodisca vitripennis) Reveal Differential Gene Expression in Bacteria Occupying Multiple Host Organs

Abstract

The agricultural pest known as the glassy-winged sharpshooter (GWSS) or Homalodisca vitripennis (Hemiptera: Cicadellidae) harbors two bacterial symbionts, “Candidatus Sulcia muelleri” and “Ca. Baumannia cicadellinicola,” which provide the 10 essential amino acids (EAAs) that are limited in the host plant-sap diet. Although they differ in origin and symbiotic age, both bacteria have experienced extensive genome degradation resulting from their ancient restriction to specialized host organs (bacteriomes) that provide cellular support and ensure vertical transmission. GWSS bacteriomes are of different origins and distinctly colored red and yellow. While Sulcia occupies the yellow bacteriome, Baumannia inhabits both. Aside from genomic predictions, little is currently known about the cellular functions of these bacterial symbionts, particularly whether Baumannia in different bacteriomes perform different roles in the symbiosis. To address these questions, we conducted a replicated, strand-specific RNA-seq experiment to assay global gene expression patterns in Sulcia and Baumannia. Despite differences in genomic capabilities, the symbionts exhibit similar profiles of their most highly expressed genes, including those involved in nutrition synthesis and protein stability (chaperonins dnaK and groESL) that likely aid impaired proteins. Baumannia populations in separate bacteriomes differentially express genes enriched in essential nutrient synthesis, including EAAs (histidine and methionine) and B vitamins (biotin and thiamine). Patterns of differential gene expression further reveal complexity in methionine synthesis. Baumannia’s capability to differentially express genes is unusual, as ancient symbionts lose the capability to independently regulate transcription. Combined with previous microscopy, our results suggest that the GWSS may rely on distinct Baumannia populations for essential nutrition and vertical transmission.

Paleocene origin of a streamlined digestive symbiosis in leaf beetles

“…These patterns are in line with the transcriptomes of obligate endosymbionts in other insect groups, where genes coding for chaperones and host-beneficial factors (e.g. essential amino acids) are among the most highly expressed 41 . But given the symbiont’s extracellular localization within its host and during transmission, 7 , we aimed to quantify the symbiont’s transcriptional plasticity relative to host development and nutritional requirements.…”

Cellular and potential molecular mechanisms underlying transovarial transmission of the obligate symbiont Sulcia in cicadas

“…Within the M. mongolica / Sulcia integration, most genes related to the biosynthesis of EAAs were highly expressed (FPKM >100) in all the samples, no matter whether they were samples of nymphs or adults (Figure 6; Table S8), which suggest the highly produced EAAs of Sulcia in all cicada life stages. This is congruent with genome‐wide transcriptome level gene expression estimates of Sulcia in the glassy‐winged sharpshooter Homalodisca vitripennis (Bennett & Chong, 2017). The expression pattern of genes related to the biosynthesis of EAAs supports the prediction that the genome of Sulcia encodes pathway genes for most essential amino acid biosynthesis for the host insects (Matsuura et al, 2018; McCutcheon & Moran, 2010).…”

Symbiont Digestive Range Reflects Host Plant Breadth in Herbivorous Beetles

“…Our annotation also revealed that genes related to protein folding and stability are shared throughout, including the GroES-GroEL chaperonin complex and the bacterial heat shock protein 70 (Hsp70) (Figure S1A). Suggestive of an important role in the biology of bacterial symbionts [33], such chaperones are among the most highly expressed enzymes within the bacteriomes of aphids [34], cicadas [35], tsetse flies [36], sharpshooters [37], and leaf beetles [11]. In contrast, pathways for the synthesis of essential amino acids, cofactors, and lipids are missing, as are genes encoding signal transduction, cell surface structures, and motility (Figure 2; Data S1).…”