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2015 Annual Science Report

University of Montana, Missoula Reporting  |  JAN 2015 – DEC 2015

Executive Summary

The question motivating the “Reliving the Past” team is: What forces bring about major transitions in the evolution of complexity? Our research consists of eight projects organized around five questions related to major transitions in the history of life: 1) How do enzymes and metabolic networks evolve? 2) How did the eukaryotic cell come to be, specifically the cell that contained a mitochondrion? 3) How do symbioses arise? 4) How does multicellularity evolve? and 5) How do pleiotropy, epistasis and mutation rate constrain evolution of novel traits? A unifying theme underlying our questions is: how do cooperative vs. competitive interactions play out when independently replicating entities combine to form a larger, more complex whole? Because the principal actors throughout much of life’s history were microorganisms, we approach these questions via experimental microbial genetics, which enables us to enact the evolutionary play repeatedly and from ... Continue reading.

Field Sites
8 Institutions
9 Project Reports
17 Publications
3 Field Sites

Project Reports

  • Project 1: From Generalist to Specialists (Or Not): A Case Study in Enzyme Evolution

    Metabolic enzymes, although prodigious catalysts, are not perfectly specific for their physiological substrates. They typically possess secondary activities as a consequence of the assemblage of highly reactive functional groups, metal ions and cofactors in their active sites. Secondary activities that are physiologically irrelevant, either because they are too inefficient to contribute to fitness or because the enzyme never encounters the substrate, are termed promiscuous activities.

    Promiscuous activities are important from an evolutionary standpoint because they provide a reservoir of catalytic potential within a proteome that can be drawn upon when the environment changes. A promiscuous activity may become important for fitness when a new source of carbon, nitrogen or phosphorous appears in the environment, or when a previously available compound, such as an amino acid or cofactor, becomes unavailable. A promiscuous activity may also become critical when the organism is exposed to a novel toxin, such as an antibiotic or pesticide.

    A newly recruited promiscuous activity is unlikely to be the optimal solution to an environmental challenge or opportunity. In this project, we are using a model system in E. coli to characterize the genetic changes by which a gene encoding an enzyme whose promiscuous activity has become essential for growth duplicates and diverges to encode a pair of genes encoding efficient specialist enzymes. This work will provide a better understanding of the process by which large superfamilies of enzymes have diverged from generalist enzymes in the last universal common ancestor.

    ROADMAP OBJECTIVES: 5.1 5.3 6.2
  • Project 2: Function by Reduction: Do Extant Symbiont Enzymes Recapitulate Ancient Metabolic Generalists

    The origins of mitochondria and chloroplasts are two of the great unsolved mysteries in biology. It is now clear that these organelles used to be bacteria, but the evolutionary paths taken as they transitioned from bacteria to organelle are not well understood because they happened more than 1.5 billion years ago. Some insect endosymbionts have symbioses with bacteria which resemble organelles in many ways. We use these more recent symbioses as models to better understand the origins of organelles, one of the most critical events in the evolution of complex life.

    ROADMAP OBJECTIVES: 4.2 5.2 6.2
  • Project 3: Consequences of recA Duplication for Recombination, Genome Stability and Fitness

    Homologous recombination (HR) – the exchange of genetic information between similar DNA molecules – is an ancient process that is central to the emergence of biological complexity, diversity and stability. Yet, it must be tightly regulated, as it is likewise an important source of destabilizing genomic rearrangements. Despite the importance of HR, we still have a poor understanding of the balance of these creative, stabilizing and destabilizing contributions to organismal fitness, complexity and genome evolution. We are using the extraordinary genome evolutionary dynamics and duplicated copies of the HR gene recA in the cyanobacterium Acaryochloris as a model to gain novel insights on the fitness consequences that emerge from the interplay between HR-mediated maintenance of genome stability, selectively favored gene duplications and non-adaptive genomic rearrangements.

    ROADMAP OBJECTIVES: 4.2 5.1 5.3 6.1 6.2
  • Project 4: Co-Evolution of Escherichia Coli and Its Parasite Bdellovibrio Bacteriovorus: An Experimental Model for Eukaryogenesis

    This project seeks to address a long-standing question in the early evolution of life on Earth: how and why did simpler cell types (prokaryotes) transition into more complex (eukaryotic) cells (i.e. eukaryogeneis)? Because this conversion happened millions of years ago and left scant fossil evidence, we have been attempting to “re-create” a similar transformation in the lab that can be easily manipulated and studied in detail. A greater understanding of the events that ocurred both before and after eukaryogenesis will not only help NASA scientists predict what extraterrestrial life might look like, it will also help us understand how modern eukaryotic cells function and evolve.

    ROADMAP OBJECTIVES: 3.3 3.4 5.1 6.2
  • Project 5: Adaptation, Mutation Supply, and Evolution of Synergy in Biofilm Communities

    We will quantify the dynamics of adaptation and identify the mutational causes in evolving biofilms with high precision, and therefore illustrate how microbes colonizing a new surface can transform their environment and set the stage for primitive multicellularity. Biofilms resemble tissues in their subdivided labor, varied physical structure and shared metabolism. We predict that the stability of this ecological cooperation rests on population-genetic controls on selfish lineages associated with mutators, much as tissues are liable to selfish invasion by cancers.

    ROADMAP OBJECTIVES: 4.2 5.1 5.2 6.1 6.2
  • Project 6: The Evolution of Complexity via Multicellularity and Cellular Differentiation

    The evolution of multicellular organisms from single-celled ancestors set the stage for unprecedented increases in complexity, especially in land plants and animals. We have used the unicellular green alga Chlamydomonas reinhardtii to generate de novo origins of simple (undifferentiated) multicellularity in two separate experiments. Using these experimentally evolved algae, we will ascertain the genetic bases underlying the evolution of multicellularity, evaluate the role of genetic assimilation in the evolution of multicellularity, and observe the evolutionary origin of multicellular development in real time.

    ROADMAP OBJECTIVES: 4.2 5.1 6.2
  • Project 7: Error Rate and the Origin and Early Evolution of Life

    Our project investigates the evolutionary relationship between rates of genetic mutation and genetic recombination. It addresses very general questions about the stability of heredity and the implications of that stability for adaptation and persistence of organisms. Such questions are likely to apply wherever and whenever life evolves. In prior theory work we have shown that the mutation rate of a population will tend towards ever-higher values in the absence of genetic recombination. Because mutation is the ultimate source of the variation required for the evolution of a population, it might be thought that a high mutation rate would enable more rapid evolutionary adaptation. We and others have shown, however, that too high a mutation rate can cause extinction of a population. Because early life probably had very high mutation rates, early life would have been at considerable risk of evolving a lethal mutation rate. This should have produced strong pressure for genetic recombination to evolve. In our project we are using experimental evolution, analytical theory, and computer simulations to test the effect that recombination has on mutation rate evolution, the effect that high mutation rates have on population adaptation and persistence, and the effect of mutation on the evolution of cooperation among life forms.

    ROADMAP OBJECTIVES: 4.2 5.2 6.2
  • Project 8: Limits to Optimality in Adaptive Evolution

    The goal of this project is to determine how the genetic makeup of an organism influences its future evolution. We have developed a tracking system that allows us to track the emergence of mutations that make an organism more fit in a certain environment – we will be deploying this system to track such emergences in yeast strains with slightly different genetic makeup. This will allow us to see how the genetic makeup influences the evolutionary process.

  • Theoretical Integration: Evolutionary Dynamics of Ecosystems Controlled by Multiple Autonomous Genomes

    The work of Co-I Smith during 2015 centered on two aspects of the role of ecosystem feedback in determining the relations among fitness functions and the co-evolutionary dynamics of multiple genomes.

    The first task concerns the optimal degree of genomic autonomy to carry out the aggregate metabolic functions of an ecosystem: when is it preferable to combine the control of multiple pathways within a single genome, and when is splitting the control among multiple autonomous genomes more stable under coevolution?

    The second task concerns the stochastic dynamics and the descriptive statistics of populations evolving under the control of feedbacks from potentially-complex ecological stoichiometric constraints. It incorporates recent methods in computational chemistry to produce exactly solvable, and biologically relevant, models of complex stoichiometric constraint that couple multiple evolving lineages.