Assessing the role of host-microbe interaction in adaptation using Drosophila melanogaster and acetic acid bacteria as a model

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Although it is becoming more and more evident that host associated microbes are important facilitators of adaptation, most studies today that aim at understanding how organisms adapt to their environment still focus on the host organism alone. We aim at broadening this perspective by assessing how hosts and microbes interact in adaptation using D. melanogaster and acetic acid bacteria (AAB) as a model. D. melanogaster and AAB live in an environment where the primary food source, ripe fruit, is ephemeral, often patchy, high in sugar-, and low in amino acid content. Under amino acid poor conditions in the laboratory, AAB can promote Drosophila growth and shorten development time by up to 10 days. Because we and others have shown that AAB are commonly associated with wild-caught D. melanogaster, it seems reasonable to assume that they could contribute to fly fitness and adaptation under natural conditions as well. Accordingly, associating with, and transporting growth promoting AAB to new food sources and oviposition sites should be adaptive for flies. At the same time, immotile bacteria could benefit from fly-mediated dispersal on an ephemeral and patchy resource. As a consequence, genetic variants that favor association of D. melanogaster with beneficial AAB can contribute to adaptation of both partners and should show footprints of positive selection in bacteria and flies. The proposed research will focus on the microbial symbiont side that has received less attention so far. We will study the mechanisms and molecular underpinnings of host-mediated dispersal and how they contribute to fly fitness. Therefore, we will (i) measure fly mediated bacterial dispersal and associate this trait with bacterial genes and variants in a pan-genome wide association study (pan-GWAS), (ii) find genes via transcriptional profiling that are active when primarily beneficial bacteria interact with Drosophila, and (iii) perform evolutionary analysis on the genes and variants found in the pan-GWAS and the transcriptional profiling. Finally, bacterial dispersal and fly fitness related functions of the genes from pan-GWAS and transcriptional profiling that show evidence for positive selection will be analyzed using knockout techniques and available continental scale microbial community data to understand their function in environmental adaptation. While other studies, in which Drosophila-microbe interaction is investigated, focus mostly on lab-derived bacteria or bacteria that rarely encounter flies under natural conditions, we will focus on bacteria that were isolated from wild-caught D. melanogaster, and hence could be evolutionarily relevant. Using the Drosophila-AAB model we can draw on the large population genomic and genetic resources for the host as well as a full set of genetic engineering tools for the microbes. The proposed research has the power to transform our understanding of how organisms adapt.