The evolution of bacterial gene expression: integrating new functions into complex biology

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Bacteria exhibit a remarkable ability to adapt and evolve. A primary means by which bacteria evolve new traits is through horizontally acquiring foreign DNA that encodes a potentially beneficial function. However, in order to benefit the organism, the acquired genes must be expressed at suitable levels and in appropriate situations. Although a great deal is known about bacterial regulatory mechanisms, far less is known about how these systems evolve to accommodate new genes and functions. The overarching goal of my research program is to characterize the evolutionary and regulatory processes that enable new genetic material to be integrated into bacterial regulatory networks. To explore this topic, we use the bacterial species Salmonella enterica (S. enterica) as a model system. S. enterica is comprised of more than 2000 serological variants (serovars) that are remarkably diverse with respect to their ecological niche and the behaviors they exhibit. The short-term aims described here use a comparative genomic approach to explore the regulatory evolution of horizontally-acquired genes and regulatory networks that have played important roles in generating this diversity. These aims address key aspects of the overarching goal of my research program and provide a framework for future studies that will build on these results to provide a more comprehensive understanding of this subject. Short-term goals: Aim 1: Analyze the evolutionary path by which a horizontally-acquired gene was integrated into an ancestral regulatory circuit. This aim exploits the discovery of closely-related homologous genes that are regulated in a different manner to explore how a gene can evolve new regulatory connections. Aim 2: Compare the regulatory evolution of functionally similar horizontally-acquired genetic factors. This aim compares how functionally-similar genes that are independently acquired by different members of a species are integrated into their regulatory networks. Aim 3: Define the evolutionary adaptations of a master regulator of horizontally-acquired genes. Particular master regulators often control the expression of large numbers of horizontally-acquired genes. This aim explores how the properties of these systems are altered over evolutionary time in order to accommodate the biology of genes they come to regulate. Impact: This research program will shed light on a central but poorly-understood aspect of how bacteria acquire new traits. It promises to make important contributions to our understanding of prokaryotic evolution and gene regulation and has direct applications for the field of synthetic biology. In addition to its contribution to science, an important goal of this research is to provide a first-rate training opportunity for HQP. This research program is designed to build a highly-desirable skillset to prepare HQP for careers in a wide range of disciplines.