Journal Article

Signatures of host/symbiont genome coevolution in insect nutritional endosymbioses

Wilson, Alex C. C, Rebecca P. Duncan

2015

Overview

The role of symbiosis in bacterial symbiont genome evolution is well understood, yet the ways that symbiosis shapes host genomes or more particularly, host/symbiont genome coevolution in the holobiont is only now being revealed. Here, we identify three coevolutionary signatures that characterize holobiont genomes. The first signature, host/symbiont collaboration, arises when completion of essential pathways requires host/endosymbiont genome complementarity. Metabolic collaboration has evolved numerous times in the pathways of amino acid and vitamin biosynthesis. Here, we highlight collaboration in branched-chain amino acid and pantothenate (vitamin B5) biosynthesis. The second coevolutionary signature is acquisition, referring to the observation that holobiont genomes acquire novel genetic material through various means, including gene duplication, lateral gene transfer from bacteria that are not their current obligate symbionts, and full or partial endosymbiont replacement. The third signature, constraint, introduces the idea that holobiont genome evolution is constrained by the processes governing symbiont genome evolution. In addition, we propose that collaboration is constrained by the expression profile of the cell lineage from which endosymbiont-containing host cells, called bacteriocytes, are derived. In particular, we propose that such differences in bacteriocyte cell lineage may explain differences in patterns of host/endosymbiont metabolic collaboration between the sap-feeding suborders Sternorrhyncha and Auchenorrhynca. Finally, we review recent studies at the frontier of symbiosis research that are applying functional genomic approaches to characterization of the developmental and cellular mechanisms of host/endosymbiont integration, work that heralds a new era in symbiosis research.

• Publisher: National Academy of Sciences,National Acad Sciences
• Subject: amino acid biosynthesis / Amino acids / Amino Acids - chemistry / Amino Acids, Branched-Chain - chemistry / Animals / bacteria / Bacteria - genetics / bacteriocytes / Biological Sciences / Biosynthesis / Buchnera - genetics / Cell Lineage / coevolution / Cytoplasm - metabolism / endosymbionts / Evolution, Molecular / Evolutionary biology / gene duplication / Gene Expression Profiling / Gene Transfer, Horizontal / Genome / Genome, Bacterial / Genomes / genomics / Hemiptera - genetics / Hemiptera - microbiology / horizontal gene transfer / insect nutritional / Insects / pantothenic acid / Pantothenic Acid - chemistry / Sternorrhyncha / Symbioses Becoming Permanent: The Origins and Evolutionary Trajectories of Organelles Sackler / Symbiosis / Vitamin B / vitamin biosynthesis