Evolution of host support for two ancient bacterial symbionts with differentially degraded genomes in a leafhopper host

Abstract

Plant sap-feeding insects (Hemiptera) rely on bacterial symbionts for nutrition absent in their diets. These bacteria experience extreme genome reduction and require genetic resources from their hosts, particularly for basic cellular processes other than nutrition synthesis. The host-derived mechanisms that complete these processes have remained poorly understood. It is also unclear how hosts meet the distinct needs of multiple bacterial partners with differentially degraded genomes. To address these questions, we investigated the cell-specific gene-expression patterns in the symbiotic organs of the aster leafhopper (ALF), Macrosteles quadrilineatus (Cicadellidae). ALF harbors two intracellular symbionts that have two of the smallest known bacterial genomes: Nasuia (112 kb) and Sulcia (190 kb). Symbionts are segregated into distinct host cell types (bacteriocytes) and vary widely in their basic cellular capabilities. ALF differentially expresses thousands of genes between the bacteriocyte types to meet the functional needs of each symbiont, including the provisioning of metabolites and support of cellular processes. For example, the host highly expresses genes in the bacteriocytes that likely complement gene losses in nucleic acid synthesis, DNA repair mechanisms, transcription, and translation. Such genes are required to function in the bacterial cytosol. Many host genes comprising these support mechanisms are derived from the evolution of novel functional traits via horizontally transferred genes, reassigned mitochondrial support genes, and gene duplications with bacteriocyte-specific expression. Comparison across other hemipteran lineages reveals that hosts generally support the incomplete symbiont cellular processes, but the origins of these support mechanisms are generally specific to the host-symbiont system.

Keywords: DNA replication and repair; eukaryotic genome evolution; nutritional symbiosis; transcription; translation.

Fig. 1.

Comparison of HTGs involved in nutrition synthesis, CIP, bacterial cell wall synthesis, population regulation, and plant or fungal cell wall degradation in the M. quadrilineatus leafhopper and 10 other hemipteran lineages (three mealybugs harboring all of the HTGs identified in mealybug species are included). Host and symbiont names are given on phylogenetic tips. Phylogenetic relationships between hosts are based on Cryan and Urban (111). HTGs represented by boxes are grouped by their functions. Shaded boxes are genes that are found in each host genome and unshaded ones are not present.

Fig. 2.

Host compensation of missing CIP genes in Sulcia and Nasuia. Symbiont genes are colored in gray. HTGs are shown in bold and labeled with an asterisk. More highly expressed host genes in bacteriocytes relative to body tissues are colored based on the log₂ FC ratio (see inset legend in Fig. 3). Genes grouped by dashed boxes are predicted to interact directly within the bacterial cytosol.

Fig. 3.

The inferred metabolism in Sulcia and Nasuia bacteriocytes. (A) Integrated nutrition pathways in Sulcia and Nasuia bacteriocytes. Relevant genes underlying precursor metabolites synthesized by the bacteria and host are shown. (B) The GS/GOGAT cycle for recycling NH₃. More highly expressed host genes in bacteriocytes relative to body tissues are colored based on the genome they occur in and the log₂ FC ratio. See inset legend for additional details and explanation of metabolite abbreviations. See text for full names of gene products. HTGs are shown in bold and labeled with an asterisk.