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Unifying the global coding sequence space enables the study of genes with unknown function across biomes

View ORCID ProfileChiara Vanni, View ORCID ProfileMatthew S. Schechter, Silvia G. Acinas, Albert Barberán, Pier Luigi Buttigieg, Emilio O. Casamayor, Tom O. Delmont, Carlos M. Duarte, View ORCID ProfileA. Murat Eren, Robert D. Finn, Renzo Kottmann, Alex Mitchell, View ORCID ProfilePablo Sanchez, View ORCID ProfileKimmo Siren, View ORCID ProfileMartin Steinegger, Frank Oliver Glöckner, View ORCID ProfileAntonio Fernandez-Guerra
doi: https://doi.org/10.1101/2020.06.30.180448
Chiara Vanni
1Microbial Genomics and Bioinformatics Research Group, Max Planck Institute for Marine Microbiology, Celsiusstraße 1, 28359, Bremen, Germany
2Jacobs University Bremen, Campus Ring 1, 28759 Bremen, Germany
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Matthew S. Schechter
1Microbial Genomics and Bioinformatics Research Group, Max Planck Institute for Marine Microbiology, Celsiusstraße 1, 28359, Bremen, Germany
3Department of Medicine, University of Chicago, Chicago, IL 60637, USA
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Silvia G. Acinas
4Department of Marine Biology and Oceanography, Institut de Ciènces del Mar, CSIC, Barcelona, Spain
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Albert Barberán
5Department of Environmental Science, University of Arizona, Tucson, 85721 AZ, USA
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Pier Luigi Buttigieg
6Alfred Wegener Institute, Helmholtz Centre for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, Germany
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Emilio O. Casamayor
7Center for Advanced Studies of Blanes CEAB-CSIC, Spanish Council for Research, Blanes, Spain
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Tom O. Delmont
8Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay, 91057 Evry, France
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Carlos M. Duarte
9Red Sea Research Centre (RSRC) and Computational Bioscience Research Center (CBRC), King Abdullah University of Science and Technology, Thuwal 23955, Saudi Arabia
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A. Murat Eren
3Department of Medicine, University of Chicago, Chicago, IL 60637, USA
10Josephine Bay Paul Center, Marine Biological Laboratory, Woods Hole, MA 02543, USA
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Robert D. Finn
11European Molecular Biology Laboratory, European Bioinformatics Institute (EMBL-EBI), Wellcome Genome Campus, Hinxton, Cambridge CB10 1SD, UK
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Renzo Kottmann
1Microbial Genomics and Bioinformatics Research Group, Max Planck Institute for Marine Microbiology, Celsiusstraße 1, 28359, Bremen, Germany
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Alex Mitchell
11European Molecular Biology Laboratory, European Bioinformatics Institute (EMBL-EBI), Wellcome Genome Campus, Hinxton, Cambridge CB10 1SD, UK
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Pablo Sanchez
4Department of Marine Biology and Oceanography, Institut de Ciènces del Mar, CSIC, Barcelona, Spain
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Kimmo Siren
12Section for Evolutionary Genomics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark
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Martin Steinegger
13School of Biological Sciences, Seoul National University, Seoul, 08826, South Korea
14Institute of Molecular Biology and Genetics, Seoul National University, Seoul, 08826, South Korea
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Frank Oliver Glöckner
15University of Bremen, MARUM, Leobener Str. 8, 28359 Bremen, Germany Life Sciences and Chemistry, Campus Ring 1, 28759 Bremen, Germany
16Computing Center, Helmholtz Center for Polar and Marine Research, Am Handelshafen 12, 27570 Bremerhaven, Germany
2Jacobs University Bremen, Campus Ring 1, 28759 Bremen, Germany
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Antonio Fernandez-Guerra
1Microbial Genomics and Bioinformatics Research Group, Max Planck Institute for Marine Microbiology, Celsiusstraße 1, 28359, Bremen, Germany
17Lundbeck GeoGenetics Centre, The Globe Institute, University of Copenhagen, 1350 Copenhagen, Denmark
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  • For correspondence: antonio.fernandez-guerra@sund.ku.dk
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Abstract

One of the biggest challenges in molecular biology is bridging the gap between the known and the unknown coding sequence space. This challenge is especially extreme in microbial systems, where between 40% and 60% of the predicted genes are of unknown function. Discarding this uncharacterized fraction should not be an option anymore. Here, we present a conceptual framework and a computational workflow that bridges this gap and provides a powerful strategy to contextualize the investigations of genes of unknown function. Our approach partitions the coding sequence space removing the known-unknown dichotomy, unifies genomic and metagenomic data and provides a framework to expand those investigations across environments and organisms. By analyzing 415,971,742 genes predicted from 1,749 metagenomes and 28,941 bacterial and archaeal genomes we showcase our approach and its application in ecological, evolutionary and biotechnological investigations. As a result, we put into perspective the extent of the unknown fraction, its diversity, and its relevance in genomic and environmental contexts. By identifying a target gene of unknown function for antibiotic resistance, we demonstrate how a contextualized unknown coding sequence space enables the generation of hypotheses that can be used to augment experimental data.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Title updated. Abstract and main text modified. Supplemental files updated.

  • https://dark.metagenomics.eu/

  • https://doi.org/10.6084/m9.figshare.12459056

  • https://github.com/functional-dark-side/agnostos-wf

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Unifying the global coding sequence space enables the study of genes with unknown function across biomes
Chiara Vanni, Matthew S. Schechter, Silvia G. Acinas, Albert Barberán, Pier Luigi Buttigieg, Emilio O. Casamayor, Tom O. Delmont, Carlos M. Duarte, A. Murat Eren, Robert D. Finn, Renzo Kottmann, Alex Mitchell, Pablo Sanchez, Kimmo Siren, Martin Steinegger, Frank Oliver Glöckner, Antonio Fernandez-Guerra
bioRxiv 2020.06.30.180448; doi: https://doi.org/10.1101/2020.06.30.180448
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Unifying the global coding sequence space enables the study of genes with unknown function across biomes
Chiara Vanni, Matthew S. Schechter, Silvia G. Acinas, Albert Barberán, Pier Luigi Buttigieg, Emilio O. Casamayor, Tom O. Delmont, Carlos M. Duarte, A. Murat Eren, Robert D. Finn, Renzo Kottmann, Alex Mitchell, Pablo Sanchez, Kimmo Siren, Martin Steinegger, Frank Oliver Glöckner, Antonio Fernandez-Guerra
bioRxiv 2020.06.30.180448; doi: https://doi.org/10.1101/2020.06.30.180448

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