Exobiology and Evolutionary Biology

Revised: Evolution of Genome Architecture in de novo Yeast Species

PI: Raphael Rosenzweig

Intellectual Merit:
Large-scale chromosomal alterations occur during formation of hybrids, either between two different species or between diverging subtypes within a species. How these alterations are utilized or accommodated after the initial hybridization event determines genome architecture in the new lineage. Although this phenomenon has been most extensively studied in higher plants, evidence for polyploidy, aneuploidy, and other genome rearrangements arising from hybrid formation has also been observed in the ancestral lineages of Animals and Fungi. However, because most studies of hybrid genomes have been performed using species that either hybridized millions of years ago, are impractical to breed in the laboratory, and/or have no genome sequence available, there has been little opportunity to follow genomic changes as they occur during speciation and adaptive evolution.

We propose an innovative experimental approach to address this problem that integrates genomics and experimental evolutionary biology, and utilizes two tractable model organisms, Bakers yeast Saccharomyces cerevisiae and its fully-sequenced congener, Saccharomyces bayanus. These species and their hybrid F1 and F2 progeny will be evolved under long-term resource-limiting and resource-variable conditions. In each evolving lineage, we will assay physiological performance, competitive ability and changes in genome architecture, the last using pulsed field gel electrophoresis in conjunction with newly developed two-species DNA microarrays. Thereby we will be able to link specific large-scale genome rearrangements to changes in physiology and fitness, thereby establishing the degree to which adaptation is guided by genome architectural changes. We will also be able to identify the suite of evolutionary trajectories that are possible or forbidden when newly hybridized genomes stabilize.

Our investigation will constitute the first systematic, genome-wide assessment of the extent and types of genome rearrangements that occur in hybrid organisms during realtime evolution. The ability to generate interspecific hybrid yeasts in the laboratory, coupled with the ability to follow and precisely characterize genome rearrangements during adaptive growth, offers an attractive and attainable experimental program almost certain to yield new insights into hybrid and polyploid genome evolution. We expect our data to yield fundamentally new insight into the role that genome plasticity plays in adaptive evolution and speciation, and to have broad impact on the study of fundamental processes in higher eukaryotic systems, including the progression of cancer.

Relevance to the NASA Mission:
Goal 5 of The Astrobiology Roadmap [http://astrobiology.arc.nasa.gov/roadmap/g5.html ] is to Understand the evolutionary mechanisms and environmental limits of life. The research project we propose specifically addresses all four elements of the Goal 5, Objective 1 research agenda, namely to (a) experimentally investigate and observe the evolution of genes, metabolic pathways, genomes and microbial species; (b) experimentally investigate the forces and mechanisms that shape the structure organization, and plasticity of microbial genomes; (c) examine how these forces control the genotype to phenotype relationship; and (d) conduct environmental perturbation experiments on single microbial species to observe and quantify adaptive evolution. Indeed, a succinct description of our project is that which NASA uses to describe an exemplary Goal 5, Objective 1 investigation: to “examine microbial genome rearrangements, including gene deletion and acquisition processes, in response to nutrient change and physical-chemical stress.”