Parallel histories of horizontal gene transfer facilitated extreme reduction of endosymbiont genomes in sap-feeding insects

Abstract

Bacteria confined to intracellular environments experience extensive genome reduction. In extreme cases, insect endosymbionts have evolved genomes that are so gene-poor that they blur the distinction between bacteria and endosymbiotically derived organelles such as mitochondria and plastids. To understand the host's role in this extreme gene loss, we analyzed gene content and expression in the nuclear genome of the psyllid Pachypsylla venusta, a sap-feeding insect that harbors an ancient endosymbiont (Carsonella) with one of the most reduced bacterial genomes ever identified. Carsonella retains many genes required for synthesis of essential amino acids that are scarce in plant sap, but most of these biosynthetic pathways have been disrupted by gene loss. Host genes that are upregulated in psyllid cells housing Carsonella appear to compensate for endosymbiont gene losses, resulting in highly integrated metabolic pathways that mirror those observed in other sap-feeding insects. The host contribution to these pathways is mediated by a combination of native eukaryotic genes and bacterial genes that were horizontally transferred from multiple donor lineages early in the evolution of psyllids, including one gene that appears to have been directly acquired from Carsonella. By comparing the psyllid genome to a recent analysis of mealybugs, we found that a remarkably similar set of functional pathways have been shaped by independent transfers of bacterial genes to the two hosts. These results show that horizontal gene transfer is an important and recurring mechanism driving coevolution between insects and their bacterial endosymbionts and highlight interesting similarities and contrasts with the evolutionary history of mitochondria and plastids.

Keywords: Pachypsylla venusta; amino acid biosynthesis; endosymbionts; lateral gene transfer; psyllids.

Fig. 1.

Differential gene expression between psyllid bacteriome and remaining body tissues. Each point represents a Trinity subcomponent (“gene”), with the x axis indicating overall gene expression and the y axis indicating differential expression between tissue types. Genes identified by edgeR as being significantly upregulated or downregulated in the bacteriome are in red.

Fig. 2.

Inferred amino acid biosynthesis pathways in the Pachypsylla venusta bacteriome. For each host-encoded gene, the fold increase in expression relative to the rest of the body is shown with absolute bacteriome expression in transcripts per million (TPM) shown in parentheses.

Fig. 3.

Quantitative PCR analysis of ASL gene expression (cDNA) and genomic copy number (genomic DNA) in bacteriome, head, and body tissues from Pachypsylla venusta. Abundance values were normalized to the psyllid nuclear gene encoding the ribosomal protein (Rp)L18e. Error bars represent one standard error.

Fig. 4.

Phylogenetic analysis of argH-derived ASL genes in Pachypsylla venusta. Bootstrap values are indicated for nodes with ≥50% support. The terminal branch for Carsonella ruddii PV was scaled to half its length to improve readability.