The power of paired genomes

Abstract

Species interactions are fundamental to ecology. Classic studies of competition, predation, parasitism and mutualism between macroscopic organisms have provided a foundation for the discipline, but many of the most important and intimate ecological interactions are microscopic in scale. These microscopic interactions include those occurring between eukaryotic hosts and their microbial symbionts. Such symbioses, ubiquitous in nature, provide experimental challenges because the partners often cannot live outside the symbiosis. With respect to the symbionts, this precludes utilizing classical microbiological and genetic techniques that require in vitro cultivation. Genomics, however, has rapidly changed the study of symbioses. In this issue of Molecular Ecology, MacDonald et al. (2011), coupling symbiont whole-genome sequencing, experimental studies and metabolic modelling, provide novel insights into one of the best-studied symbioses, that between aphids and their obligate, nutrient-provisioning, intracellular bacteria, Buchnera aphidicola (Fig. 1). MacDonald and colleagues assessed variation in the ability of aphid–Buchnera pairs to thrive on artificial diets missing different amino acids. As shown previously (e.g. Wilkinson & Douglas 2003), aphid–Buchnera pairs can differ in their requirements for external sources of essential amino acids. Such phenotypic variation could result from differences in Buchnera’s amino acid biosynthetic capabilities or in the ability of aphids to interact with their symbionts. Whole-genome sequencing of the Buchnera genomes from four aphid lines with alternate nutritional phenotypes revealed that the environmental nutrients required by the aphid–Buchnera pairs could not be explained by sequence variation in the symbionts. Instead, a novel metabolic modelling approach suggested that much of the variation in nutritional phenotype could be explained by host variation in the capacity to provide necessary nutrient precursors to their symbionts. MacDonald et al.’s work complements a recent study by Vogel & Moran (2011), who through crossing experiments investigating the inheritance of a nutritional phenotype associated with a frameshift mutation in a Buchnera amino acid biosynthesis gene powerfully demonstrated that different host genotypes paired with the same symbiont genome could exhibit substantially different nutritional requirements.† Thus, while there is little doubt that Buchnera are evolutionarily central to the nutritional ecology of aphids, the current work by MacDonald et al. (2011) together with that of Vogel & Moran (2011) surprisingly demonstrates host dominance in defining and controlling the ecological niche of this particular symbiosis.