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Functional and evolutionary significance of unknown genes from uncultivated taxa

View ORCID ProfileÁlvaro Rodríguez del Río, Joaquín Giner-Lamia, Carlos P. Cantalapiedra, Jorge Botas, Ziqi Deng, Ana Hernández-Plaza, Lucas Paoli, Thomas S.B. Schmidt, View ORCID ProfileShinichi Sunagawa, Peer Bork, View ORCID ProfileLuis Pedro Coelho, Jaime Huerta-Cepas
doi: https://doi.org/10.1101/2022.01.26.477801
Álvaro Rodríguez del Río
1Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid (UPM) - Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA-CSIC), Campus de Montegancedo-UPM, 28223, Madrid, Spain
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  • ORCID record for Álvaro Rodríguez del Río
Joaquín Giner-Lamia
1Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid (UPM) - Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA-CSIC), Campus de Montegancedo-UPM, 28223, Madrid, Spain
2Departamento de Biotecnología-Biología Vegetal, Escuela Técnica Superior de Ingeniería Agronómica, Alimentaria y de Biosistemas, Universidad Politécnica de Madrid (UPM), Madrid, Spain
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Carlos P. Cantalapiedra
1Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid (UPM) - Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA-CSIC), Campus de Montegancedo-UPM, 28223, Madrid, Spain
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Jorge Botas
1Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid (UPM) - Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA-CSIC), Campus de Montegancedo-UPM, 28223, Madrid, Spain
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Ziqi Deng
1Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid (UPM) - Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA-CSIC), Campus de Montegancedo-UPM, 28223, Madrid, Spain
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Ana Hernández-Plaza
1Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid (UPM) - Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA-CSIC), Campus de Montegancedo-UPM, 28223, Madrid, Spain
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Lucas Paoli
3Department of Biology, Institute of Microbiology and Swiss Institute of Bioinformatics, ETH Zürich, Zürich 8093, Switzerland
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Thomas S.B. Schmidt
4Structural and Computational Biology Unit, European Molecular Biology Laboratory, D-69117 Heidelberg, Germany
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Shinichi Sunagawa
3Department of Biology, Institute of Microbiology and Swiss Institute of Bioinformatics, ETH Zürich, Zürich 8093, Switzerland
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Peer Bork
4Structural and Computational Biology Unit, European Molecular Biology Laboratory, D-69117 Heidelberg, Germany
5Max Delbrück Centre for Molecular Medicine, Berlin, Germany
6Yonsei Frontier Lab (YFL), Yonsei University, Seoul, South Korea
7Department of Bioinformatics, Biocenter, University of Würzburg, Würzburg, Germany
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Luis Pedro Coelho
8Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, China
9MOE Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence, and MOE Frontiers Center for Brain Science, Shanghai, China
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Jaime Huerta-Cepas
1Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid (UPM) - Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA-CSIC), Campus de Montegancedo-UPM, 28223, Madrid, Spain
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  • For correspondence: j.huerta@csic.es
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Abstract

Most microbes on our planet remain uncultured and poorly studied. Recent efforts to catalog their genetic diversity have revealed that a significant fraction of the observed microbial genes are functional and evolutionary untraceable, lacking homologs in reference databases. Despite their potential biological value, these apparently unrelated orphan genes from uncultivated taxa have been routinely discarded in metagenomics surveys. Here, we analyzed a global multi-habitat dataset covering 151,697 medium and high-quality metagenome assembled genomes (MAGs), 5,969 single-amplified genomes (SAGs), and 19,642 reference genomes, and identified 413,335 highly curated novel protein families under strong purifying selection out of previously considered orphan genes. These new protein families, representing a three-fold increase over the total number of prokaryotic orthologous groups described to date, spread out across the prokaryote phylogeny, can span multiple habitats, and are notably overrepresented in recently discovered taxa. By genomic context analysis, we pinpointed thousands of unknown protein families to phylogenetically conserved operons linked to energy production, xenobiotic metabolism and microbial resistance. Most remarkably, we found 980 previously neglected protein families that can accurately distinguish entire uncultivated phyla, classes, and orders, likely representing synapomorphic traits that fostered their divergence. The systematic curation and evolutionary analysis of the unique genetic repertoire of uncultivated taxa opens new avenues for understanding the biology and ecological roles of poorly explored lineages at a global scale.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://github.com/AlvaroRodriguezDelRio/NovFamilies/raw/main/Supplementary%20tables.xlsx

  • https://novelfams.cgmlab.org/

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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Posted January 27, 2022.
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Functional and evolutionary significance of unknown genes from uncultivated taxa
Álvaro Rodríguez del Río, Joaquín Giner-Lamia, Carlos P. Cantalapiedra, Jorge Botas, Ziqi Deng, Ana Hernández-Plaza, Lucas Paoli, Thomas S.B. Schmidt, Shinichi Sunagawa, Peer Bork, Luis Pedro Coelho, Jaime Huerta-Cepas
bioRxiv 2022.01.26.477801; doi: https://doi.org/10.1101/2022.01.26.477801
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Functional and evolutionary significance of unknown genes from uncultivated taxa
Álvaro Rodríguez del Río, Joaquín Giner-Lamia, Carlos P. Cantalapiedra, Jorge Botas, Ziqi Deng, Ana Hernández-Plaza, Lucas Paoli, Thomas S.B. Schmidt, Shinichi Sunagawa, Peer Bork, Luis Pedro Coelho, Jaime Huerta-Cepas
bioRxiv 2022.01.26.477801; doi: https://doi.org/10.1101/2022.01.26.477801

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