Adaptation, Tradeoffs and Specialized Metabolism in Experimental and Natural Populations

Harvard University, Cambridge MA

Investigators

Abstract

What underlies the relationship between adaptation of organisms to their environment and loss of ancestral capacities that result in specialization? One possibility is an absence of selection for certain capacities in the current niche such that mutations that degrade unused systems can accumulate neutrally (i.e. "you don't use it you lose it"). Alternatively, there may be particular mutations that have multiple (i.e. pleiotropic) effects: they may increase fitness in one environment but have antagonistic physiological side-effects that decrease performance in another environment. This project will combine the use of laboratory-evolved and natural populations to address the mechanistic bases that underlie tradeoffs in the adaptation of bacteria to different growth environments. The primary approach of this one-year project is to examine experimental populations of Methylobacterium extorquens AM1 that have been evolved on methanol and/or succinate, two substrates that require very different metabolic pathways. The observation across numerous bacteria that acquisition of the ability to grow on single-carbon (C1) compounds such as methanol has repeatedly and independently been associated with loss of the ability to grow on many or all multiple-carbon compounds makes this a naturally relevant system to examine such tradeoffs. Based upon competitive fitness assays the laboratory populations, already propagated for over 1200 generations, have clearly adapted and specialized to their respective growth substrate. The first aim of this project is to extend and integrate the examination of adaptation and specialization across a variety of system-wide phenotypic levels using physiological, analytical and functional genomics approaches. Second, a new ultra-low-cost resequencing technique will be employed to comprehensively identify the genotypic changes (point mutations and/or genome rearrangements) that will then be rigorously tested for their contribution to adaptation and/or specialization. Finally, tradeoffs between C1 and multi-carbon metabolism will be extended to natural population through an examination of isolates from across the Methylobacterium genus. This project will provide a model for the integration of experimental studies of evolution with a comparative analysis of the same processes across natural isolates. Broader impacts of this work include increased understanding of the processes through which bacterial populations adapt and specialize to their environment. This is critical for understanding the origin and maintenance of biological diversity at the microbial level. Given the key role of microbes in mediating biochemical cycling, degradation of toxic compounds, and their diverse positive and negative interactions with multi-cellular organisms, this information has significant practical benefit. Finally, this ongoing project will provide valuable opportunities for both graduate and undergraduate students to be exposed to and involved in highly interdisciplinary research at the intersection of evolution, ecology, microbiology, and systems biology. Such broad training and experience is critical for tackling important but difficult questions that transcend the boundaries of traditional academic fields.