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Final Report Summary - GENESTORY (Assembling genome history from gene stories: Phylogeny aware genome scale inference of ancestral traits and ancient environments)

The GENESTORY project aims to harness recent advances in the phylogeny aware models of genome evolution to construct large scale datasets and proposes to combine the results with metabolic networks reconstruction and models of ancient biodiversity. The results from both of these avenues of investigation have the potential to benefit a wide range of biological research, both in the EU and beyond, by providing timely and relevant information on the evolution of system level traits, ancient environments and extinct or unsampled biodiversity. Due to the interdisciplinary nature of the research questions and methodology, we anticipate that these results will have broad scientific impact and hence make a significant contribution to enhancing the EU’s scientific excellence.

To accomplish these goals, the project brings together the expertise in phylogenetic modeling acquired by the researcher with the interdisciplinary research experience of Imre Derényi and other researchers at the host institution, both at the Department of Biological Physics. At the same time, established collaborations with members of the ANCESTROME project including Bastien Boussau, Nicolas Lartillot and new collaborators such as Tom Williams at the University of Bristol, who provide biological and methodological expertise.

The GENESTORY project has resulted in 10 publications (8 published and 2 submitted), including publications in Systematic Biology (the top ranking journal in Evolutionary Biology), Molecular Biology and Evolution (a journal that consistently ranks among the highest impact journals in Evolutionary Biology) and Physical Review Letters (one of the most influential physics journals):


1. Davin AA, Tannier E, Boussau B, Daubin V, Szollosi GJ*
Gene transfers provide a phylogenetic fossil record for dating the tree of life

2. Williams TA, Szollosi GJ, Spang A, Foster PG, Heaps S, Boussau B, Ettema TJG, Embley TM
Integrative modelling of gene and genome evolution roots the archaeal tree of life
under review at PNAS, major revision requested


3. Szollosi GJ* and Daubin V (2016)
Horizontal gene transfer and the history of life
In: Cold Spring Harbor perspectives in biology 8 (4), a018036 (5 year IF: 11.277)

4. Groussin M, Boussau B, Szollosi GJ, Eme L, Gouy M, Brochier-Armanet C, Daubin V (2016)
Gene acquisitions from bacteria at the origins of major archaeal clades are vastly overestimated.
In: Molecular Biology and Evolution 33(2):305-10.. (5 year IF: 11.667)

5. Jacox E, Chauve C, Szollosi GJ, Ponty J, Scornavacca C
ecceTERA: Comprehensive gene tree-species tree reconciliation using parsimony
In: Bioinformatics 32(13):2056-8. (5 year IF: 6.968)

6. Szollosi GJ*, Davin AA,Tannier E, Daubin V, Boussau B (2015)
Genome-scale phylogenetic analysis finds extensive gene transfer among Fungi. Accepted in: Philosophical Transactions B (5 year Impact Factor: 7.885)

7. Derényi I, Szollosi GJ* (2015)
The effective temperature of mutations.
In: Physical Review Letters 114(5):058101. (5 year IF: 7.360).

8. Scornavacca C, Jacox E, Szollosi GJ* (2015)
Joint amalgamation of most parsimonious reconciled gene trees. In: Bioinformatics 31(6):841-8. (5 year IF: 6.968)

9. Groussin M, Hobbs JK, Szollosi GJ, Gribaldo S, Vickery AL, Manolo G (2015) Towards more accurate ancestral protein genotype–phenotype reconstructions with the use of species tree-aware gene trees.
In: Molecular Biology and Evolution 32(1):13-22. (5 year IF: 11.667)

10. Szollosi GJ*,Tannier E, Daubin V, Boussau B (2015) The inference of gene trees with species trees.
In: Systematic Biology 64 (1), 42-62 (5 year IF: 14.787)

The project has also resulted in the M.Sc. thesis of Kéri Zsófia at the Institute of Physics, Eötvös University and made significant contribution to the M.Sc. thesis of Benjamin Horvilleur at University Lyon 1 Claude Bernard. The GENESTORY project is further expected to constitute a significant part of the PhD theses of Zsofia Keri (expected submission 2018 at Eotvos University, Budapest) and Adrian A Davin (expected submission 2017 at University Claude Bernard, Lyon).

We would like to highlight four of the above publications to showcase the progress of the GENESTORY project:

Our publication currently under review at PNAS (we are about to submit a requested major revision) “Integrative modelling of gene and genome evolution roots the archaeal tree of life” (number 2 above)

The Archaea are one of the primary domains of cellular life, play a major role in modern-day biogeochemical cycles, and are central to debates about the origin of eukaryotic cells. But understanding their origins and evolutionary history is challenging because of the immense time spans involved. Here, we apply a new approach that harnesses the information in patterns of gene family evolution to find the root of the archaeal tree and to resolve the metabolism of the earliest archaeal cells. Our approach robustly distinguishes between published rooting hypotheses, suggests that the first Archaea were anaerobes that made a living by reducing CO2 with H2, and quantifies the cumultative impact of horizontal transfer on archaeal genome evolution.

Our publication in Philosophical Transactions B "Genome-scale phylogenetic analysis finds extensive gene transfer among Fungi" (number 6 above):

Recently there has been accumulating evidence for substantial amounts of transfer in several eukaryotic groups, including metazoans (Boto 2014), in particular sponges (Jackson 2011) and cnidaria (Starcevic 2008, Chapman 2010), and other eukaryotic groups such as Fungi (Gibbons 2013). As shown in Fig.6., in our most recent publication currently under review (Szollosi 2015) examining 11387 gene families from the genomes of 28 Fungi and 7370 gene families from the genomes of 40 Cyanobacteria, we found compelling evidence that gene transfer plays a significant role in the evolution of Fungi comparable to prokaryotes.

Our publication in Molecular Biology and Evolution "Towards more accurate ancestral protein genotype–phenotype reconstructions with the use of species tree-aware gene trees" (number 9 above):

The research involved in "GENESTORY" is not experimental, however, neither is it traditionally theoretical. It aims to extract novel biological information by analysing publicly available raw experimental data, i.e., genomic sequences, that are by themselves unintelligible. The shared advantage with theoretical research is its relatively low cost. A shared shortcoming is the lack of direct experimental validation of the results. To address the latter one of the research objectives of the group we are working on devising and carrying out experimental validation with the help of collaborations. In the above paper we demonstrated that such validation is feasible by preforming biochemical essays on a billion year old protein “resurrected” in vitro by cloning the predicted amino acid sequence. We found that the species tree-aware methods developed as part of the "GENESTORY" project predict amino acid sequences that result in biochemically much more realistic proteins.

Our publication in Systematic Biology "The inference of gene trees with species trees" (number 10 above):

This review publication provides an overview of probabilistic methods currently available and explores possibilities for future development. It explains in detail why we predict that gene tree–species tree methods that can deal with genomic data sets will be instrumental to advancing our understanding of genomic evolution. As the first author Dr. Gergely Szollosi took a central role in writing the paper.

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