Evolution of substrate specificity in a retained enzyme driven by gene loss
The connection between gene loss and the functional adaptation of retained proteins is still poorly understood. We apply phylogenomics and metabolic modeling to detect bacterial species that are evolving by gene loss, with the finding that Actinomycetaceae genomes from human cavities are undergoing...
| Main Authors: | , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2017-03-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/22679 |
| _version_ | 1811227638513008640 |
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| author | Ana Lilia Juárez-Vázquez Janaka N Edirisinghe Ernesto A Verduzco-Castro Karolina Michalska Chenggang Wu Lianet Noda-García Gyorgy Babnigg Michael Endres Sofía Medina-Ruíz Julián Santoyo-Flores Mauricio Carrillo-Tripp Hung Ton-That Andrzej Joachimiak Christopher S Henry Francisco Barona-Gómez |
| author_facet | Ana Lilia Juárez-Vázquez Janaka N Edirisinghe Ernesto A Verduzco-Castro Karolina Michalska Chenggang Wu Lianet Noda-García Gyorgy Babnigg Michael Endres Sofía Medina-Ruíz Julián Santoyo-Flores Mauricio Carrillo-Tripp Hung Ton-That Andrzej Joachimiak Christopher S Henry Francisco Barona-Gómez |
| author_sort | Ana Lilia Juárez-Vázquez |
| collection | DOAJ |
| description | The connection between gene loss and the functional adaptation of retained proteins is still poorly understood. We apply phylogenomics and metabolic modeling to detect bacterial species that are evolving by gene loss, with the finding that Actinomycetaceae genomes from human cavities are undergoing sizable reductions, including loss of L-histidine and L-tryptophan biosynthesis. We observe that the dual-substrate phosphoribosyl isomerase A or priA gene, at which these pathways converge, appears to coevolve with the occurrence of trp and his genes. Characterization of a dozen PriA homologs shows that these enzymes adapt from bifunctionality in the largest genomes, to a monofunctional, yet not necessarily specialized, inefficient form in genomes undergoing reduction. These functional changes are accomplished via mutations, which result from relaxation of purifying selection, in residues structurally mapped after sequence and X-ray structural analyses. Our results show how gene loss can drive the evolution of substrate specificity from retained enzymes. |
| first_indexed | 2024-04-12T09:45:33Z |
| format | Article |
| id | doaj.art-8757720966d641749ea07358e6bb7cad |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T09:45:33Z |
| publishDate | 2017-03-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-8757720966d641749ea07358e6bb7cad2022-12-22T03:37:57ZengeLife Sciences Publications LtdeLife2050-084X2017-03-01610.7554/eLife.22679Evolution of substrate specificity in a retained enzyme driven by gene lossAna Lilia Juárez-Vázquez0Janaka N Edirisinghe1Ernesto A Verduzco-Castro2Karolina Michalska3Chenggang Wu4Lianet Noda-García5Gyorgy Babnigg6Michael Endres7Sofía Medina-Ruíz8Julián Santoyo-Flores9Mauricio Carrillo-Tripp10Hung Ton-That11Andrzej Joachimiak12Christopher S Henry13Francisco Barona-Gómez14https://orcid.org/0000-0003-1492-9497Evolution of Metabolic Diversity Laboratory, Unidad de Genómica Avanzada (Langebio), Cinvestav-IPN, Irapuato, MexicoComputing, Environment and Life Sciences Directorate, Argonne National Laboratory, Lemont, United States; Computation Institute, University of Chicago, ChicagoEvolution of Metabolic Diversity Laboratory, Unidad de Genómica Avanzada (Langebio), Cinvestav-IPN, Irapuato, MexicoMidwest Center for Structural Genomics, Biosciences Division, Argonne National Laboratory, Lemont, United States; Structural Biology Center, Biosciences Division, Argonne National Laboratory, Lemont, United StatesDepartment of Microbiology and Molecular Genetics, University of Texas Health Science Center, Houston, United StatesEvolution of Metabolic Diversity Laboratory, Unidad de Genómica Avanzada (Langebio), Cinvestav-IPN, Irapuato, MexicoMidwest Center for Structural Genomics, Biosciences Division, Argonne National Laboratory, Lemont, United StatesMidwest Center for Structural Genomics, Biosciences Division, Argonne National Laboratory, Lemont, United StatesEvolution of Metabolic Diversity Laboratory, Unidad de Genómica Avanzada (Langebio), Cinvestav-IPN, Irapuato, MexicoCinvestav-IPN, MexicoCinvestav-IPN, MexicoDepartment of Microbiology and Molecular Genetics, University of Texas Health Science Center, Houston, United StatesMidwest Center for Structural Genomics, Biosciences Division, Argonne National Laboratory, Lemont, United States; Department of Microbiology and Molecular Genetics, University of Texas Health Science Center, Houston, United States; Department of Biochemistry and Molecular Biology, University of Chicago, Chicago, United StatesComputing, Environment and Life Sciences Directorate, Argonne National Laboratory, Lemont, United States; Computation Institute, University of Chicago, ChicagoEvolution of Metabolic Diversity Laboratory, Unidad de Genómica Avanzada (Langebio), Cinvestav-IPN, Irapuato, MexicoThe connection between gene loss and the functional adaptation of retained proteins is still poorly understood. We apply phylogenomics and metabolic modeling to detect bacterial species that are evolving by gene loss, with the finding that Actinomycetaceae genomes from human cavities are undergoing sizable reductions, including loss of L-histidine and L-tryptophan biosynthesis. We observe that the dual-substrate phosphoribosyl isomerase A or priA gene, at which these pathways converge, appears to coevolve with the occurrence of trp and his genes. Characterization of a dozen PriA homologs shows that these enzymes adapt from bifunctionality in the largest genomes, to a monofunctional, yet not necessarily specialized, inefficient form in genomes undergoing reduction. These functional changes are accomplished via mutations, which result from relaxation of purifying selection, in residues structurally mapped after sequence and X-ray structural analyses. Our results show how gene loss can drive the evolution of substrate specificity from retained enzymes.https://elifesciences.org/articles/22679evolution by gene lossgenome decayenzyme substrate specificityActinomycesHistidine and tryprophan biosynthesisphosphoribosyl isomerase A |
| spellingShingle | Ana Lilia Juárez-Vázquez Janaka N Edirisinghe Ernesto A Verduzco-Castro Karolina Michalska Chenggang Wu Lianet Noda-García Gyorgy Babnigg Michael Endres Sofía Medina-Ruíz Julián Santoyo-Flores Mauricio Carrillo-Tripp Hung Ton-That Andrzej Joachimiak Christopher S Henry Francisco Barona-Gómez Evolution of substrate specificity in a retained enzyme driven by gene loss eLife evolution by gene loss genome decay enzyme substrate specificity Actinomyces Histidine and tryprophan biosynthesis phosphoribosyl isomerase A |
| title | Evolution of substrate specificity in a retained enzyme driven by gene loss |
| title_full | Evolution of substrate specificity in a retained enzyme driven by gene loss |
| title_fullStr | Evolution of substrate specificity in a retained enzyme driven by gene loss |
| title_full_unstemmed | Evolution of substrate specificity in a retained enzyme driven by gene loss |
| title_short | Evolution of substrate specificity in a retained enzyme driven by gene loss |
| title_sort | evolution of substrate specificity in a retained enzyme driven by gene loss |
| topic | evolution by gene loss genome decay enzyme substrate specificity Actinomyces Histidine and tryprophan biosynthesis phosphoribosyl isomerase A |
| url | https://elifesciences.org/articles/22679 |
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