Metabolic Coevolution in the Bacterial Symbiosis of Whiteflies and Related Plant Sap-Feeding Insects

Abstract

Genomic decay is a common feature of intracellular bacteria that have entered into symbiosis with plant sap-feeding insects. This study of the whitefly Bemisia tabaci and two bacteria (Portiera aleyrodidarum and Hamiltonella defensa) cohoused in each host cell investigated whether the decay of Portiera metabolism genes is complemented by host and Hamiltonella genes, and compared the metabolic traits of the whitefly symbiosis with other sap-feeding insects (aphids, psyllids, and mealybugs). Parallel genomic and transcriptomic analysis revealed that the host genome contributes multiple metabolic reactions that complement or duplicate Portiera function, and that Hamiltonella may contribute multiple cofactors and one essential amino acid, lysine. Homologs of the Bemisia metabolism genes of insect origin have also been implicated in essential amino acid synthesis in other sap-feeding insect hosts, indicative of parallel coevolution of shared metabolic pathways across multiple symbioses. Further metabolism genes coded in the Bemisia genome are of bacterial origin, but phylogenetically distinct from Portiera, Hamiltonella and horizontally transferred genes identified in other sap-feeding insects. Overall, 75% of the metabolism genes of bacterial origin are functionally unique to one symbiosis, indicating that the evolutionary history of metabolic integration in these symbioses is strongly contingent on the pattern of horizontally acquired genes. Our analysis, further, shows that bacteria with genomic decay enable host acquisition of complex metabolic pathways by multiple independent horizontal gene transfers from exogenous bacteria. Specifically, each horizontally acquired gene can function with other genes in the pathway coded by the symbiont, while facilitating the decay of the symbiont gene coding the same reaction.

The draft genome of whitefly Bemisia tabaci MEAM1, a global crop pest, provides novel insights into virus transmission, host adaptation, and insecticide resistance

“…In this study, we provide multiple lines of evidence to support the identified HGTs, including the alignments of paired-end and mate pair DNA reads and polyA-enriched strand-specific RNA-Seq reads (see Methods for details; Additional file 1: Figure S9; Additional files 17 and 18). In addition, our RNA-Seq data indicated that most of the HGTs were moderately or highly expressed, and 10 HGTs of bacterial origin were previously confirmed by qPCR [24]. Together, our data strongly support the high confidence of the identified HGTs in the B. tabaci genome.…”

“…Approximately 22% of the Rickettsia genes are homologous to transposable elements, suggesting that the genome is highly dynamic. Comparative analysis of the B. tabaci genome with the Portiera and Hamiltonella genomes identified genes coding for complementary reactions in multiple metabolic pathways, including essential amino acid biosynthesis (Additional file 1: Figure S8 and Additional file 16), as reported previously [24, 44]. Analysis of the Rickettsia genome also shows the absence of genes for non-essential amino acid biosynthesis (Additional file 1: Figure S8 and Additional file 16) .…”

Repeated replacement of an intrabacterial symbiont in the tripartite nested mealybug symbiosis

“…In each of these cases, no other bacterial genes or pseudogenes were found within the scaffolds (Tables S2 and S3), suggesting that these HGTs resulted from the transfer of small DNA fragments or that flanking bacterial DNA from larger fragments was lost after the transfer was established. The origin of some of these transfers [7,8-diaminopelargonic acid synthase and biotin synthase (bioAB)] likely predates the entire mealybug lineage, because they are found in the genome of the whitefly Bemisia tabaci (11).…”

“…For example, deep sea tube worms, some protists, and many sap-feeding insects are completely dependent on intracellular bacteria for essential nutrient provisioning (5)(6)(7). Some of these symbioses can form highly integrated organismal and genetic mosaics that, in many ways, resemble organelles (8)(9)(10)(11). Like organelles, these endosymbionts have genomes encoding few genes (12,13), rely on gene products of bacterial origin that are encoded on the host genome (9-11, 14, 15), and in some cases, import protein products encoded by these horizontally transferred genes back into the symbiont (16,17).…”

“…symbionts themselves (9)(10)(11)14). Another solution to avoid host extinction is to replace the degenerating symbiont with a fresh one or supplement it with a new partner.…”