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A biological network approach to the study of biochemical origins, early cellular evolution, and gene distributions across genomes

Final Report Summary - NETWORKORIGINS (A biological network approach to the study of biochemical origins, early cellular evolution, and gene distributions across genomes)

Questions about early evolution — in particular about life's origin and the evolution of life forms that inhabited the early Earth — are of broad interest to scientists and the general public alike. Geochemical evidence has it that there are clear signs of life in rock 3.8 billion years of age. But the fossil record of multicellular life only goes back for about one third of that history. The first 2 billion years of evolution on Earth is microbial evolution. How did microbial life start? How did the major transitions take place? How can we understand the transitions from inanimate matter to prokaryotes (the smallest and simplest kinds of cells we know), and what drove the transition from prokaryotes to eukaryotes (the larger, complex kinds of cells that have a nucleus and that make up all multicellular life)? It is the job of evolutionary biologists to address these questions. Genomes harbour vast information about the ancient past. The history of life is written in genome sequences, but we are still learning how to decipher the message.
This ERC project — NETWORKORIGINS — aimed to advance our understanding of early evolution. The main goals were to address three pivotal evolutionary issues. The first goal was to develop a network-based approach to the study of prokaryotic evolution that incorporates lateral gene transfer. The second goal was to better understand the prokaryote-to-eukaryote transition. The third goal was to investigate how the transition from geochemistry to biochemistry was possible. We made tangible progress on all three fronts.
We explored and developed the use of networks to study genome evolution in prokaryotes. At the outset of our work, it was known that the basic process of prokaryote evolution fundamentally differs from that in multicellular life: Multicellular organisms inherit their genes vertically within species, while prokaryotes acquire their genes from sources well outside the species boundary. This process, called lateral gene transfer (LGT), has well-characterized mechanisms in prokaryotes, and generates evolutionary networks among genomes over time, rather than evolutionary trees. We used evolutionary networks to obtain a new way to understand genome relationships among prokaryotes, one that far better models their natural evolutionary mechanisms than the traditional bifurcating tree.
Regarding the prokaryote-to-eukaryote transition, we made two kinds of progress in understanding the role of symbiosis in eukaryote origins. First, we were able to better specify the number and nature of gene acquisitions surrounding the endosymbiotic origin of mitochondria and plastids — the energy-conserving organelles of eukaryotic cells. This in turn enriches our understanding of the biology of the prokaryotic ancestors of plastids and mitochondira respectively. We also obtained important insights into understanding the singularity of eukaryote origins. Eukaryote cells are vastly more complex than prokaryote cells, and it went long overlooked that this increased complexity has an energetic price. By investigating the energetics of genome complexity we were able to uncover why eukaryote evolution started with the origin of mitochondria; it is because mitochondrial power was required to finance the origin of eukaryotic specific traits.
With regard to the transition from geochemical reactions to biological cells, we made progress in understanding energetic aspects of the problem. Our attention has come to focus on what some microbiologists think are the most primitive forms of prokaryotic life: acetogens and methanogens. These microbes live from spontaneous, energy-releasing chemical reactions that still take place today, geochemically, in some types of hydrothermal vents. As microbiologists uncover more about how these prokaryotes harness energy for life, the more striking their similarities to geochemical chemical reactions become. This work has served to further underscore the importance of energy in evolution.