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Early Microbial Evolution

Periodic Reporting for period 3 - eMicrobevol (Early Microbial Evolution)

Reporting period: 2018-11-01 to 2020-04-30

What is at the focus of this project about early microbial evolution? The goals of the project are to obtain a better understanding of early microbial evolution. In the foreground are general questions like: Which lineages of microbes are the most ancient, how and where did the first cells on Earth live, how did complex cells (eukaryotes) arise from simple cells (prokaryotes)? Those questions need to be placed in the context of Earth history. The Earth is 4.5 billion years old. The first signs of life on Earth appear almost 4 billion years ago, while the first life on land appeared less than 500 million years ago. That means that the first 3.5 billion years of evolution took place in aquatic environments. The first truly multicellular organisms comprised of complex cells (cells with a true nucleus: eukaryotes) appeared about 1.2 billion years ago. In other words, the first 2.8 billion years of life's history took place at the level of unicellular organisms that are only visible under the microscope — microbes. Microbes have very little to offer in the way of a fossil record. Isotope data from ancient sediments can tell us about what kinds of processes were going on, but not which lineages of modern microbes (if any) were involved. Our richest source of information about microbial evolution is genomes.

Why is this project important for society? It is part of human nature to want to know more about our biological past — in our human lineage, in our animal ancestors and back to the origin of the first living things. Every human society has a narrative about how everything began, where the living things in the world we know came from, where the first humans came from and, roughly, how that links to our current direct experience in modern times. There is also a set of scientific narratives that is at least as diverse as those found across societies. The present work is roughly cast in that context, and the objective is to extract a rendering of microbial history from genomes, ideally one that meshes with the rest of the natural sciences. Humans generally want to know about the past. That appears to be important, and it is a main reason why we are doing this research, in addition to the circumstance that the investigators themselves who are doing this work also want to know about our past. The basic motivation is scientific curiosity, humans are generally curious beings. It is basic research, yes, but it is very difficult to predict where findings from basic research might have applications.

What are the objectives? Just like the Earth records its own history, genomes record the history of life. But reading the history of life in microbial genomes is complicated, almost irremediably so, by lateral gene transfer (LGT). LGT is a pervasive factor in prokaryotic genome evolution and it was important at the origin of mitochondria, the powerhouses of eukaryotic cells, that were present in the eukaryote common ancestor. If we want to read early microbial history from genomes, we need to find ways to deal with LGT in such a way as to separate wheat (true evolutionary signals) from chaff (spurious evolutionary signals) in genome data. That means that we need to find ways to identify genes that have been affected by LGT, and the simplest way to do that, we contend, is to make trees from all genes — a new frontier that has not been extensively explored outside the ongoing projects in our group.
Our main findings to date in this project have uncovered interesting and new genome-based insights into eukaryote origins [1], into LGT in early microbial evolution [2] and into the nature of the first cells as revealed when trees affected by LGT between domains are filtered out [3]. These results have been published and lay the groundwork for further investigations into the topics.

[1] Ku C, Nelson-Sathi S, Roettger M, Sousa FL, Lockhart PJ, Bryant D, Hazkani-Covo E, McInerney JO, Landan G, Martin WF: Endosymbiotic origin and differential loss of eukaryotic genes. Nature 524:427–432 (2015).

[2] Nelson-Sathi S, Sousa FL, Roettger M, Lozada-Chávez N, Thiergart T, Janssen A, Bryant D, Landan G, Schönheit P, Siebers B, McInerney JO, Martin WF: Origins of major archaeal clades correspond to gene acquisitions from bacteria. Nature 517:77–80 (2015).

[3] Weiss MC, Sousa FL, Mrnjavac N, Neukirchen S, Roettger M, Nelson-Sathi S, Martin WF: The physiology and habitat of the last universal common ancestor. Nature Microbiology 1:16116 (2016).

Overall our progress in the project has generated 60 publications so far.
We have found ways to make trees from all genes and to extract information from those trees using computers so that specific questions can be posed to sets of thousands (or hundreds of thousands) of trees. We have developed tests to determine whether two sets of trees are drawn from the same distribution by comparting their sets of splits, also for the case that the trees have overlapping but non-identical leaf sets. This has proved very useful in discriminating vertical from lateral modes of inheritance for specified biological groups. Our approach to analyze all genes is finding considerable resonance in the literature.
Mitochondrial origin in a prokaryotic hos
Evolution of anaerobes and the plastid
LUCA reconstructed from genome data
Distribution of taxa in eukaryote–prokaryote clusters
Archaeal gene acquisition network